TYPE Review

PUBLISHED 17 January 2025

DOI 10.3389/fmicb.2024.1510036

The role of Bacillus species in the

OPEN ACCESS management of plant-parasitic
nematodes
EDITED BY
Pramod Kumar Sahu,
National Bureau of Agriculturally Important
Microorganisms (ICAR), India

REVIEWED BY Prabhakaran Vasantha-Srinivasan 1, Ki Beom Park 2,

Kgabo Martha Pofu, Kil Yong Kim 3, Woo-Jin Jung 3* and Yeon Soo Han 1*
University of Limpopo, South Africa
Ugur Azizoglu, 1
Department of Applied Biology, Institute of Environmentally Friendly Agriculture (IEFA), College of
Kayseri University, Türkiye Agriculture and Life Sciences, Chonnam National University, Gwangju, Republic of Korea, 2 Research
*CORRESPONDENCE
and Development Center, Invirustech Co., Inc., Gwangju, Republic of Korea, 3 Department of
Yeon Soo Han Agricultural Chemistry, Institute of Environmentally-Friendly Agriculture (IEFA), College of Agriculture
[email protected] and Life Sciences, Chonnam National University, Gwangju, Republic of Korea
Woo-Jin Jung
[email protected]
Plant-parasitic nematodes (PPNs), including root-knot nematodes (Meloidogyne
RECEIVED 12 October 2024
ACCEPTED 18 December 2024
spp.), cyst nematodes (Heterodera and Globodera spp.), and other economically
PUBLISHED 17 January 2025 significant nematode species, pose severe threats to global agriculture. These
CITATION nematodes employ diverse survival strategies, such as dormancy in cysts or robust
​ asantha-Srinivasan P, Park KB, Kim KY, Jung
V infective juvenile stages. Consequently, their management is challenging. Traditional
W-J and Han YS (2025) The role of Bacillus
control methods, such as the use of chemical nematicides, are increasingly
species in the management of plant-parasitic
nematodes. scrutinized because of environmental and health concerns. This review focuses
Front. Microbiol. 15:1510036. on the specific mechanisms employed by Bacillus spp., including nematicidal
doi: 10.3389/fmicb.2024.1510036
compound production, systemic resistance induction, and cuticle degradation,
COPYRIGHT to target root-knot and cyst nematodes. These mechanisms offer sustainable
© 2025 Vasantha-Srinivasan, Park, Kim, Jung
and Han. This is an open-access article
solutions for managing nematodes and promoting soil health by enhancing microbial
distributed under the terms of the Creative diversity and nutrient cycling. An integrated approach leveraging Bacillus-based
Commons Attribution License (CC BY). The biocontrol is proposed to maximize efficacy and agricultural sustainability.
use, distribution or reproduction in other
forums is permitted, provided the original
author(s) and the copyright owner(s) are KEYWORDS
credited and that the original publication in
plant-parasitic nematodes, biocontrol, Bacillus spp., nematicidal compounds,
this journal is cited, in accordance with
accepted academic practice. No use, integrated pest management
distribution or reproduction is permitted
which does not comply with these terms.

Introduction
Overview of nematode infestations in crops and their
impact on agriculture

Nematode infestations significantly threaten global agriculture, causing substantial

economic losses of over USD 80 billion annually (Nicol et al., 2011; Abd-Elgawad, 2024).
Plant-parasitic nematodes (PPNs) are highly diverse and include various species, such as root-
knot nematodes (Meloidogyne spp.), cyst nematodes (Heterodera and Globodera spp.), lesion
nematodes (Pratylenchus spp.), and reniform nematodes (Rotylenchulus reniformis). These
nematodes exhibit unique parasitic mechanisms. Hence, their management in agricultural
systems is challenging.
Root-knot nematodes invade root tissues and induce the formation of specialized feeding
structures called giant cells, diverting host resources and stunting plant growth. Bacillus subtilis
produces nematicidal enzymes, such as proteases, which degrade nematode cuticles, reducing
mobility and infectivity. Secondary metabolites, such as fengycin and surfactin, exhibit potent
activity by disrupting nematode cell membranes, causing cell lysis and death (Jiang et al.,
2021). Moreover, these metabolites inhibit egg hatching and juvenile development, effectively
suppressing the nematode life cycle. On the other hand, cyst nematodes form syncytia in root
tissues, resulting in long-term nutrient extraction. Lesion nematodes produce migratory

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lesions that compromise root integrity and increase susceptibility to Major phytopathogenic nematodes in
secondary infections (Gupta et al., 2023). These adaptations result in global agriculture
yield losses, with root-knot nematodes alone accounting for an
estimated loss of over 5% globally. Their adaptability and multiple life Phytopathogenic nematodes pose a significant threat to global
cycles in warm climates exacerbate this damage (Subbotin et al., 2021). agriculture. They impact a wide range of crops by feeding on plant
Similarly, cyst nematodes survive under unfavorable conditions by roots, disrupting nutrient uptake, and serving as vectors for other
forming resilient cysts containing eggs, enabling extended dormancy pathogens. The most harmful genera include Meloidogyne,
in the soil (Moens et al., 2018). B. amyloliquefaciens plays a crucial role Heterodera, Globodera, Pratylenchus, Radopholus, Rotylenchulus,
in managing cyst nematodes by inducing systemic resistance in plants, Ditylenchus, and Bursaphelenchus, each exhibiting unique life
thereby suppressing the formation of syncytia within root tissues. This cycles, modes of action, and seasonal habitats that contribute to
bacterium also produces chitinases to degrade cyst shells, preventing pathogenicity (Mesa-Valle et al., 2020; Palomares-Rius
hatching and subsequent infestations (Ngalimat et al., 2021). Given et al., 2020).
these functions of Bacillus spp. and their role in improving plant vigor, Root-knot nematodes (Meloidogyne spp.), including M. incognita,
they are effective against cyst nematodes in diverse agricultural systems. M. javanica, and M. arenaria, are particularly damaging. Their life
The survival strategies of nematodes demand tailored cycles progress from eggs to infective juveniles and adults, with
management approaches that account for the distinct biological traits juveniles primarily causing damage by penetrating plant roots. These
of each group. For instance, root-knot nematodes secrete effector nematodes thrive in warm climates and cause peak damage during
proteins that suppress key host plant defense pathways, such as those spring and summer, contributing to significant yield losses in various
mediated by jasmonic acid (JA) and salicylic acid (SA), while cyst crops, such as tomatoes, soybeans, and cotton in Brazil, China, and
nematodes release effector proteins that alter root architecture to other regions (Blouin et al., 1998; Subbotin et al., 2021). Cyst
facilitate syncytium formation (Ahmad et al., 2021). Moreover, lesion nematodes (Heterodera and Globodera spp.) pose unique challenges
nematodes disrupt cell walls enzymatically, contributing to extensive because of their ability to form cysts containing eggs. Consequently,
root decay. Understanding these intricate molecular interactions is they can survive for long durations under adverse conditions. The
crucial for devising effective and sustainable management strategies. soybean cyst nematode H. glycines and the golden potato cyst
Traditional control methods, such as crop rotation, the use of nematode G. rostochiensis cause substantial crop losses, particularly in
resistant cultivars, and the use of chemical nematicides, are limited by temperate regions. Their dormant cysts hatch under favorable
the biological versatility of nematodes and the environmental environmental conditions, typically in spring, aligning with the
concerns associated with chemical usage. The ability of root-knot planting season (He et al., 2022). Lesion nematodes (Pratylenchus
nematodes to overcome resistant cultivars further complicates spp.) are migratory endoparasites that create lesions in root tissues as
breeding efforts (Pradhan et al., 2023). Moreover, although chemical they feed, significantly impairing plant health. These nematodes are
nematicides are initially effective, they pose risks to nontarget active throughout the year in warm, moist environments, such as
organisms and contribute to environmental degradation (Kumar et al., those in tropical agricultural regions, causing severe yield losses in
2017). These limitations underscore the need for safer, various crops, such as banana, coffee, and soybean (Saikai and
eco-friendly alternatives. MacGuidwin, 2022; Riascos-Ortiz et al., 2022). Similarly, burrowing
Recent advances in biocontrol have demonstrated the potential of nematodes (Radopholus similis) and stem nematodes (Ditylenchus
Bacillus spp. in combating specific PPNs. Bacillus spp. employ various dipsaci) exhibit seasonal activity, with the former thriving in wet
mechanisms, such as the production of nematicidal metabolites (e.g., tropical climates and the latter affecting bulbous plants in cooler
lipopeptides and proteases), the induction of systemic resistance in climates (Mathew and Opperman, 2019; Sturhan and Brzeski, 2020).
plants, and competition with nematodes for resources (Patil et al., The global burden of these nematodes is substantial. Hence, there is
2019; Jiang et al., 2021). For instance, B. subtilis produces fengycin and an urgent need for sustainable, effective management strategies to
surfactin lipopeptides, which disrupt root-knot nematode cuticles, mitigate the impact of these nematodes on global food security.
while B. amyloliquefaciens induces systemic resistance in plants,
enhancing defenses against cyst nematodes (Lin et al., 2020).
Understanding the mechanisms underlying these distinct interactions Traditional methods of nematode control
is crucial for optimizing their applications in nematode management and their limitations
programs and ensuring that they also contribute positively to soil
health. This review emphasizes the targeted use of Bacillus spp. against Traditional nematode management approaches, including cultural
root-knot and cyst nematodes, detailing their distinct survival practices, biocontrol methods, and chemical treatments, have been
strategies and biocontrol mechanisms. widely implemented to mitigate the detrimental effects of nematodes
Given the diversity of PPNs and the limitations of conventional and maintain crop health and productivity (Elango et al., 2020).
management strategies, this review focuses on Bacillus spp. as Cultural methods, such as crop rotation, soil solarization, and
biocontrol agents, discussing their mechanisms, efficacy, and potential sanitation, aim to interrupt the life cycle of nematodes, thereby
for integration into sustainable nematode management programs. The diminishing their populations in the soil (Oka, 2010). Biocontrol
discussion covers multiple PPNs, focusing on crop nematodes, methods leverage natural predators and antagonistic plants to
especially root-knot, cyst, lesion, and reniform nematodes. The maintain the ecological balance of nematode populations (El-Saadony
literature is sourced from reputable databases, including Elsevier, et al., 2021). Chemical treatments, which involve the application of
Springer, and MDPI, ensuring the inclusion of high-quality and nematicides, can directly target nematodes and rapidly reduce
relevant studies. their populations.

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Despite their extensive use, these conventional methods have Aimani et al., 2022). Furthermore, predatory fungi, such as
several limitations that undermine their long-term efficacy and Paecilomyces and Arthrobotrys spp., can trap and digest nematodes,
sustainability (Sikora and Roberts, 2018). Although cultural practices, while endophytic fungi, such as Trichoderma spp., can colonize plant
such as crop rotation, are theoretically effective, they require extensive roots and produce enzymes and metabolites that can inhibit nematode
knowledge and labor and can yield inconsistent results because of activity and enhance plant resistance (Singh et al., 2019). The
environmental variations (Grubišić et al., 2018). Biocontrol methods, incorporation of organic amendments, such as compost and green
including the use of antagonistic plants, such as marigold (Tagetes manure, into the soil can also boost the populations of beneficial
spp.) and neem (Azadirachta indica), offer environmentally friendly microbes that compete with or directly antagonize nematodes. These
alternatives; however, they often fail to exhibit adequate suppressive biocontrol strategies can not only reduce the reliance on chemical
effects and may require considerable time to be effective (Waller and nematicides but also promote sustainable agricultural practices by
Thamsborg, 2004). Moreover, the efficacy of biocontrol methods can enhancing soil health and biodiversity. The schematic representation
significantly vary depending on the species involved and the of comparison of chemical pesticide-based nematode management
environmental conditions. with Bacillus-based biocontrol approaches, showcasing differences in
Although chemical treatments provide rapid and effective mode of action, scalability, production costs, environmental impacts,
nematode control, they pose significant risks to human health, non-target species effects, soil health, economic value, and
nontarget organisms, and the environment. The persistent use of sustainability was displayed (Figure 1).
nematicides has led to the emergence of resistant nematode strains, Bacterial antagonists are among the most promising biocontrol
thereby diminishing their long-term effectiveness (Timper, 2014). The agents. They suppress PPNs through multiple mechanisms, including
regulatory restrictions posed on many effective nematicides because the production of nematicidal lipopeptides, such as surfactin and
of their adverse environmental impacts have further limited their fengycin, which disrupt nematode cuticles and membranes. Bacillus
availability and use (Grubišić et al., 2018). spp. produce various enzymes, such as chitinases and proteases, which
These inherent limitations of traditional nematode control degrade nematode eggshells and cuticles, effectively reducing juvenile
methods highlight the need for innovative and sustainable approaches. development and reproduction (Yang et al., 2013). In particular,
Integrated pest management (IPM) strategies that combine traditional B. subtilis triggers systemic resistance in plants by activating JA and
practices with modern technological advancements present a SA signaling pathways, thereby enhancing the natural defenses of
promising solution. These strategies aim to enhance the effectiveness plants against nematode attacks (Chowdhury et al., 2015). The
of nematode control while minimizing the associated environmental antagonistic effects of Paenibacillus elgii HOA73 and P. illinoisensis
and health risks. KJA-424 were evaluated through in vitro nematicidal assays and
greenhouse experiments. Key methodologies included assessing
nematode motility and mortality using bacterial supernatants and
Biocontrol strategies for nematodes with a evaluating the activity of enzymes, such as chitinases and proteases.
focus on Bacillus spp Greenhouse trials confirmed reductions in nematode gall formation
and reproduction in infested tomato plants (Jung et al., 2002; Nguyen
Biocontrol strategies are being recognized as sustainable and et al., 2013). Bacillus spp., in particular, are a diverse group of gram-
environmentally friendly alternatives to chemical nematicides for positive, rod-shaped, endospore-forming bacteria commonly found
managing nematode infestations. Various microbial agents and in soil and plant environments. They can produce various bioactive
botanical extracts have shown potential for reducing nematode compounds, including enzymes, antibiotics, and toxins, which
populations. For instance, fungal strains, such as Auxarthron enhance their effectiveness in controlling plant pathogens and
reticulatum DY-2, Verticillium saksenae A-1, Lecanicillium psalliotae promoting plant health (El Aimani et al., 2022). Some Bacillus spp. are
A-1, and L. antillanum B-3, have been explored for their effectiveness notably effective against nematodes and other plant pathogens,
in parasitizing and reducing nematode populations (Oh et al., 2014a,b; making them valuable for sustainable agricultural practices.
Nguyen et al., 2014). Additionally, extracts of Cinnamomum cassia Bacillus spp. produce various nematicidal compounds, including
bark and C. aromaticum have demonstrated enzyme-inhibitory and lipopeptides, proteases, and chitinases, which target nematodes at
nematicidal properties, thereby serving as potential agents for various life stages (Tran et al., 2019). These soil-dwelling bacteria
botanical interventions (Nguyen et al., 2009, 2012; Nguyen and Jung, produce spores that can endure extreme environmental conditions,
2014). Nguyen et al. (2011) demonstrated that treatment with C. cassia making them ideal candidates for sustainable nematode management
crude extracts significantly reduced gall formation and nematode (Singh et al., 2019). They can directly antagonize nematodes by
growth in a dose-dependent manner in root-knot nematode-infested producing toxins, enzymes, and other bioactive compounds that
cucumber plants. This treatment also enhanced the activities of impact nematode mobility, development, and reproduction
antioxidative enzymes, such as SOD, CAT, and APX, in cucumber (Migunova and Sasanelli, 2021). Bacillus spp., such as B. thuringiensis
leaves, indicating a strengthened defense response against the (Bt) and B. firmus, have been extensively studied for their nematicidal
nematode. Furthermore, bark extracts of Terminalia nigrovenulosa activities (Zuckerman et al., 1993). For instance, Bt produces crystal
and related compounds have been found to disrupt nematode life (Cry) proteins that are toxic to a broad range of nematodes and can
cycles (Seo et al., 2013). cause cell lysis and death upon ingestion (Forghani and Hajihassani,
In addition to fungi and botanical extracts, entomopathogenic 2020). Similarly, B. firmus produces enzymes and secondary
nematodes (EPNs), such as Steinernema and Heterorhabditis spp., are metabolites that degrade the nematode cuticle and interfere with
known for their ability to release symbiotic bacteria (e.g., Xenorhabdus physiological processes. The use of Bacillus spp. not only reduces the
and Photorhabdus spp.) that produce toxins lethal to nematodes (El reliance on chemical nematicides, thereby mitigating environmental

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FIGURE 1
Schematic representation of comparison of conventional and Bacillus-based nematode management strategies.

impacts, but also promotes soil health by maintaining beneficial nematodes, causing cell lysis and death (Forghani and Hajihassani,
microbial populations (Tran et al., 2019). 2020; Diyapoglu et al., 2022). B. firmus produces chitinase, an enzyme
Bacillus spp. can effectively manage PPN infestations through that breaks down chitin in nematode eggshells, thereby preventing
various biocontrol strategies (Tian et al., 2007; Gamalero and Glick, hatching and reducing nematode populations (Tran et al., 2019).
2020; Diyapoglu et al., 2022). The nematicidal activity of B. subtilis was Additionally, B. subtilis produces lipopeptides, such as surfactin and
assessed through in vitro bioassays focusing on lipopeptides, such as fengycin, which disrupt nematode cell membranes, causing the loss of
surfactin and fengycin, which can cause significant disruption of cell integrity and cell death (El Aimani et al., 2022). B. amyloliquefaciens
nematode cell membranes, resulting in mortality (El Aimani et al., produces proteases, which degrade nematode cuticles and interfere
2022). Similarly, studies on B. amyloliquefaciens have revealed its with their physiological processes, resulting in reduced viability and
efficacy in IPM programs. By producing antifungal and antibacterial reproduction (Cetintas et al., 2018). The primary modes of action
metabolites, the bacterium could exhibit dual efficacy against PPNs through which Bacillus spp. target nematodes include direct toxicity
and secondary infections in plants under controlled and field by producing toxins and enzymes, the inhibition of egg hatching and
conditions (Cetintas et al., 2018). These strategies highlight the juvenile development, the induction of systemic resistance in plants,
versatility of Bacillus spp. as biocontrol agents through multiple and the disruption of physiological processes by degrading structural
mechanisms, including direct toxicity, the inhibition of nematode components (e.g., cuticles) and interfering with metabolic pathways
development, and the enhancement of plant resistance. These bacteria essential for nematode survival (Shafi et al., 2017). The detailed
also induce systemic resistance in plants, enhancing their defensive mechanisms of action underlying the efficacy of Bacillus spp. against
capabilities against nematode attacks (Yang et al., 2022). They produce PPNs are presented in Figure 2.
chitinase and other enzymes that can degrade nematode eggshells,
thereby reducing hatching rates and subsequent infection levels. Field
trials have also revealed that formulations containing Bacillus spp. can Historical perspective on the use of
significantly reduce root galling and improve plant health, Bacillus spp. as biocontrol agents
demonstrating their practical applicability in agricultural settings
(Forghani and Hajihassani, 2020). The historical development of Bacillus spp. as biocontrol agents
In summary, Bacillus spp. employ various proteins and secondary against plant pathogens, particularly nematodes, highlights significant
metabolites to exhibit nematicidal effects. The key proteins include advancements in scientific understanding and practical applications.
Cry proteins from Bt, which act by forming pores in the gut cells of Bacillus spp. were first identified by Ferdinand Cohn in the late 19th

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FIGURE 2
Mode of action of Bacillus spp. against plant-parasitic nematodes. The figure illustrates the sequential mechanisms of Bacillus species, including the
entry of spores into the nematode body via ingestion or adhesion to the cuticle, enzymatic degradation of structural components (such as cuticles and
eggshells), and disruption of intestinal cells through Cry and Cyt toxin-induced pore formation. The figure also highlights the inhibition of nematode
reproduction, the disruption of cellular metabolism, and systemic physiological collapse, ultimately resulting in nematode mortality.

century. Early research highlighted their roles in improving soil health (Carmona-Hernandez et al., 2019). Given the commercial success of
and promoting plant growth through the production of nematicidal Bacillus-based products, these biocontrol agents were further
compounds, such as enzymes and secondary metabolites (Brzezinska integrated into IPM systems, offering sustainable alternatives to
et al., 2020). chemical nematicides (Castillo et al., 2013). Current research
The mid-20th century marked a pivotal advancement with the underscores the role of Bacillus spp. in promoting soil biodiversity and
discovery of Bt and its insecticidal Cry proteins, forming the enhancing plant microbiomes, which contribute to long-term
foundation for experimental biocontrol applications (Sanahuja et al., nematode suppression (Calvo et al., 2010). Biotechnological advances,
2011). A timeline highlighting significant milestones in the including CRISPR and synthetic biology, have further expanded the
development of Bacillus species as biocontrol agents, from their initial potential of Bacillus spp., enhancing their stability, specificity, and
discovery to advancements in genetic engineering and sustainable ability to produce nematicidal compounds (Baptista et al., 2022). Key
agricultural practices, emphasizing their expanding role in integrated Bacillus spp., including Bt, B. subtilis, and B. cereus, are crucial because
pest management, is presented (Figure 3). Initial studies on nematode they produce diverse nematicidal compounds, such as Cry proteins,
management focused on nematicidal compounds, such as chitinases chitinases, and lipopeptides, which exhibit broad-spectrum activity
and proteases, (Bacon et al., 2006). By the 1970s and 1980s, researchers against nematodes (Jouzani et al., 2017; Saxena et al., 2020; Ahmad
identified specific toxins and enzymes produced by Bacillus spp., et al., 2021). Comparative studies have demonstrated the unique
revealing their targeted actions against nematodes (Van strengths of Bacillus spp., providing insights into their compatibility
Frankenhuyzen, 2009, 2013). Field trials in the 1990s evaluated the with specific crops and soil environments. For example, B. subtilis
efficacy of Bacillus-based biocontrol agents under various induces systemic resistance in plants, Bt acts through direct toxin-
environmental and agronomic conditions. These studies highlighted mediated gut disruption, and B. cereus enhances soil health through
the importance of application methods, soil properties, and microbial microbial synergism (Diyapoglu et al., 2022; Tran et al., 2019). This
interactions in achieving consistent nematode suppression (Etesami historical trajectory highlights the evolution of Bacillus spp. from their
et al., 2023; Serrão et al., 2024). With advancements in genomic initial discovery to becoming cornerstones of sustainable agriculture.
technologies, researchers unraveled genes and regulatory pathways The roles of Bacillus spp. in nematode biocontrol highlight their
responsible for the biocontrol properties of Bacillus spp. in the early potential as integral components of IPM strategies, addressing key
21st century. This enabled the development of genetically enhanced challenges in plant health management (Sanahuja et al., 2011;
strains with improved efficacy and environmental resilience Raymond and Federici, 2017).

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FIGURE 3
Timeline of Bacillus species development as biocontrol agents. This timeline highlights significant milestones in the development of Bacillus species as
biocontrol agents, from their initial discovery to advancements in genetic engineering and sustainable agricultural practices.

Key Bacillus spp. and their efficacy against secondary infections (Bravo et al., 2007). Cyt proteins complement
nematodes Bt Cry proteins by targeting the lipid components of nematode cell
membranes, thereby inducing cell lysis through distinct pore-forming
Bt is widely recognized for its potent nematicidal activity, mechanisms (Gill et al., 1992; Wei et al., 2003). In laboratory assays,
primarily mediated by the production of insecticidal Cry and cytolytic Cry5B has been found to interact with glycosylphosphatidylinositol-
(Cyt) proteins. These proteins, synthesized as protoxins during anchored proteins in the gut cells of M. incognita, causing cell swelling
sporulation, exhibit significant efficacy against various PPNs, and epithelial rupture. Cry6A specifically targets aspartyl protease and
including Meloidogyne and Heterodera spp. (Verduzco-Rosas et al., alkaline phosphatase receptors, initiating apoptosis and disrupting gut
2021; Kahn et al., 2021). Experimental studies on the efficacy of Bt integrity (Barros dos Santos et al., 2022; Shi et al., 2020). These
toxins generally utilize nematode bioassays, in which second-stage experiments typically involve histological analysis of nematode
juveniles (J2) of Meloidogyne spp. are exposed to varying midgut tissues and the use of advanced imaging techniques to confirm
concentrations of Cry and Cyt proteins under controlled receptor interactions and cellular damage. The specificity and
environmental conditions. Mortality, hatching inhibition, and effectiveness of Bt toxins vary among nematode species because of
mobility reduction are the commonly measured endpoints in such differences in gut receptor structures and proteolytic activation.
studies. Upon ingestion, the alkaline gut environment of nematodes Nematodes can use innate defenses, such as enzyme detoxification and
solubilizes these protoxins, which are then activated by specific gut pH modulation, to mitigate Bt toxicity, highlighting the complexity of
proteases. The activated Cry proteins bind to gut epithelial receptors, host–pathogen interactions (Zhang et al., 2012). These interactions
such as cadherin-like proteins, aminopeptidases, and alkaline underscore the versatility and adaptability of Bt in managing diverse
phosphatases, inducing structural changes that facilitate membrane nematode infestations. Advances in molecular biology have facilitated
insertion and pore formation (Griffitts et al., 2005; Schnepf et al., the engineering of transgenic crops expressing Cry proteins,
1998). This pore formation disrupts osmotic balance, causing cell lysis, conferring continuous protection against nematodes. For example, in
gut paralysis, and eventual nematode death due to starvation or field trials, transgenic rice expressing Cry6A exhibited significant

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resistance to M. graminicola, with the nematode populations 2017; Basiouny and Abo-Zaid, 2018). In field trials, these methods
decreasing by 80% and yield improving by 30% (Lilley et al., 2011; can be assessed through randomized designs to monitor nematode
Berlitz et al., 2014). Such experiments typically involve randomized levels and yield improvements. When integrated into IPM
field plots, and the efficacy of treatments is compared with those of frameworks, B. subtilis performs synergistically with organic
chemical nematicides and untreated controls. Nematode population amendments and other biocontrol agents, enhancing efficacy and
dynamics and yield data are analyzed to assess efficacy. The integration promoting soil health (Cavalcanti et al., 2024). These combined
of Bt formulations with organic amendments, such as chitin or neem strategies can maximize nematicidal potential and support
extracts, can further enhance their efficacy through synergistic effects sustainable agriculture. The multifaceted actions of B. subtilis
(Chen et al., 2000; Radwan, 2007). Field applications of Bt-based highlight its pivotal role in reducing nematode infestations and
biopesticides can be evaluated using standardized protocols. For promoting eco-friendly pest management practices.
instance, Cry55A-containing formulations have shown notable
efficacy in reducing M. incognita populations under greenhouse and
field conditions, with Cry55A-treated soil exhibiting 70% lower B. cereus
nematode gall formation than untreated controls. These findings
highlight the potential of Cry55A as a soil inoculant (Manivannan B. cereus exhibits robust nematicidal activity against PPNs
et al., 2019; Ramalakshmi et al., 2020). Innovative delivery systems, through diverse mechanisms. It secretes metalloproteinases, such as
such as seed treatments and soil inoculants, ensure early and sustained neutral protease (Npr) and bacillolysin (BlyA), which degrade
activity throughout the growing season (Etesami et al., 2023). These nematode cuticle proteins, thereby causing structural collapse and
advancements align with sustainable agricultural practices, offering death (Yin et al., 2021a,b; Kulkova et al., 2023). Enzyme assays have
an eco-friendly alternative to chemical nematicides (Hui et al., 2012; confirmed the degradation of nematode cuticles, correlating
Chen et al., 2024). Given its robust mechanisms of action, adaptability enzymatic activity with nematode mortality. Lipopeptides, such as
to various nematode species, and compatibility with sustainable surfactin and fengycin, disrupt nematode cell membranes via pore
practices, Bt plays a crucial role in modern nematode management formation, causing cell leakage and lysis (Tong-Jian et al., 2013; Hu
frameworks. Comparative insights across species and delivery systems et al., 2020). Fluorescent dyes have been used to validate
underscore its effectiveness as a cornerstone of nematode membrane disruption.
biocontrol strategies. B. cereus also produces siderophores, such as bacillibactin, which
can chelate iron, thereby depriving nematodes of essential nutrients
(Köhl et al., 2019). Furthermore, they produce bacteriocins, such as
B. subtilis cerein, which can act as antibiotics and target nematode cellular
processes. Bioassays have confirmed nutrient depletion and reduced
B. subtilis, a versatile PGPR, exhibits remarkable efficacy against viability in treated nematodes. Nano-bioformulations have further
PPNs through diverse mechanisms. This bacterium produces improved the stability and bioavailability of these bioactive
lipopeptides, such as surfactins, fengycins, and iturins, which disrupt compounds, ensuring prolonged nematode suppression in diverse
nematode cell membranes, causing cell lysis and death (Heerklotz soils (Kumar et al., 2021). Field trials have highlighted their extended
and Seelig, 2007; Henry et al., 2011). In vitro studies can confirm activity and reduced application frequencies. Optimized delivery
these effects by exposing Meloidogyne juveniles to purified methods include soil drenching, seed treatments, and foliar sprays.
lipopeptides and assessing mortality through microscopic Soil drenching ensures uniform root-zone colonization, while seed
observations and viability staining. Additionally, B. subtilis secretes treatments enable early protection during crucial growth stages
hydrolytic enzymes, such as chitinases and proteases, which degrade (Ahmed et al., 2019). Randomized trials have revealed significant
nematode eggshells and cuticles, thereby inhibiting juvenile reductions in M. incognita populations and improvements in yield.
emergence and reproduction (Hu et al., 2007; Huang et al., 2008). When combined with mycorrhizal fungi, B. cereus exhibits synergistic
Enzymatic activity is often assessed using substrate degradation effects, enhancing soil microbial diversity and plant resilience (Hu
assays, in which enzymatic activity is correlated with nematode et al., 2017). Genetic engineering approaches, including CRISPR, are
population decline. B. subtilis also induces systemic resistance in being used to enhance the production of bioactive compounds and
plants by activating JA and SA pathways, thereby enhancing the target-specific nematicidal properties (Mohamed et al., 2021).
production of phenolics and defense proteins that limit nematode Through its diverse mechanisms of action, including enzyme
penetration (Adiwena et al., 2023). In greenhouse studies, RT-qPCR secretion, nutrient competition, and direct nematode disruption,
and phenolic quantification assays can be used to validate these B. cereus offers a sustainable biocontrol option for PPN management.
responses. Volatile organic compounds (VOCs), such as Its integration into IPM strategies and compatibility with sustainable
2,3-butanediol and acetoin, further suppress nematode motility and agriculture highlight its crucial role in reducing chemical nematicide
reproduction while promoting rhizosphere health (Henry et al., usage while improving crop health and productivity.
2011). These VOCs can be identified through GC–MS analysis, and
their inhibitory effects can be confirmed by performing bioassays.
The applications of B. subtilis include seed treatments, soil drenching, B. megaterium
and foliar sprays. Seed treatments ensure early root colonization,
while soil drenching targets root zones for sustained nematode B. megaterium is a robust biocontrol agent that has been proven
suppression. Foliar sprays activate induced systemic resistance (ISR) to be effective against PPNs by producing various bioactive
pathways, indirectly reducing nematode infestations (Barnawal et al., compounds and enzymes. It secretes proteases, such as neutral and

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Vasantha-Srinivasan et al. 10.3389/fmicb.2024.1510036

serine proteases, which degrade structural proteins in nematode lipopeptides). Its compatibility with agronomic practices, such as seed
cuticles, causing severe damage and death (Padgham and Sikora, treatments and soil drenching, facilitates early root colonization and
2007). Lipopeptides, such as surfactin and iturin, disrupt nematode uniform metabolite distribution, enhancing field performance.
cell membranes through pore formation, causing cell leakage and lysis Furthermore, its synergy with mycorrhizal fungi and other beneficial
(Pueyo et al., 2009). Additionally, B. megaterium synthesizes microbes enhances nutrient cycling and plant resilience, creating a
siderophores, such as bacillibactin, which can chelate iron in the holistic defense against nematodes (Carriel and Soto, 2022). Through
rhizosphere, thereby depriving nematodes of vital nutrients and its multifaceted actions and adaptability, B. pumilus exhibits significant
suppressing their populations while promoting a balanced microbial potential for integration into IPM strategies. Further research on
community. These processes have been validated through enzyme genetic optimization, delivery systems, and formulations is warranted
assays, correlating siderophore activity with nematode suppression to sustainably maximize its agricultural impact.
(Huang et al., 2010). Nano-bioformulations have further enhanced the
stability and bioavailability of B. megaterium metabolites, ensuring
prolonged nematode suppression and reduced application frequency B. licheniformis
(Kumar et al., 2021). Various application techniques, including soil
drenching and seed treatments, have been optimized for efficient B. licheniformis employs diverse mechanisms, including enzymatic
delivery. Soil drenching ensures deep root penetration, while seed degradation, antimicrobial activity, and soil microbiome modulation,
treatments facilitate early root colonization, offering sustained to manage PPNs. Its nematicidal activity is attributed to the secretion
protection during crucial growth stages (Padgham and Sikora, 2007; of hydrolytic enzymes, such as proteases and chitinases, which target
Raza et al., 2024). These strategies have been effective against root- the cuticles and eggshells of nematodes, impairing their mobility,
knot nematodes, such as M. incognita, significantly improving plant reproduction, and viability (Park et al., 2015). For example, strain
health and yields in field trials (Mostafa et al., 2018). Genetic MH48 effectively degrades nematode structures, particularly in
engineering approaches, such as the overexpression of genes B. xylophilus (Jeong et al., 2015). Additionally, B. licheniformis
responsible for lipopeptide synthesis and VOC production, have been produces lipopeptides, such as bacillomycin and fengycin, which
employed to enhance nematicidal efficacy. These efforts have shown disrupt nematode and fungal cell membranes, causing ion leakage and
promise in increasing activity against nematodes while maintaining cytoplasmic loss. Thus, it exhibits dual functionality as a biocontrol
environmental safety (Grage et al., 2017; Hartz et al., 2021). Through agent (Stoica et al., 2019). B. licheniformis strains, such as strain XF32,
its multifaceted nematicidal mechanisms, B. megaterium serves as an have exhibited enhanced production of fengycin through genetic
eco-friendly alternative to chemical nematicides. Its adaptability and modifications, highlighting their potential for agricultural and
integration into IPM strategies make it a cornerstone of sustainable industrial applications (Zhaojian et al., 2021). Furthermore, strain
pest management. It can support agricultural productivity while JF-22 was found to reduce M. incognita populations and enrich
minimizing environmental impacts. beneficial microbial communities in tomato rhizospheres, promoting
soil health and plant resilience (Du et al., 2022). Unlike Bt, which relies
on Cry proteins, or B. pumilus, which relies on nutrient deprivation,
B. pumilus B. licheniformis integrates enzymatic lysis with microbiome
enhancement to suppress nematodes. It also supports plant defenses
B. pumilus employs diverse nematicidal mechanisms, making it a indirectly. Studies have indicated its ability to bolster the resistance of
powerful biocontrol agent against PPNs. It acts by secreting proteolytic C. elegans to bacterial infections through hormonal signaling
enzymes, such as subtilisin, which can degrade nematode cuticle pathways, such as those involving serotonin, suggesting its potential
proteins, causing osmotic imbalance and eventual death (Ramezani for inducing systemic resistance in plants (Yun et al., 2014). Advances
Moghaddam et al., 2014). Lipopeptides, such as pumilacidin and in genetic engineering, such as promoter and ribosome binding site
bacilysin, disrupt nematode cell membranes and induce pore engineering, have increased the capacity of B. licheniformis to produce
formation, ion leakage, and cytoplasmic efflux, thereby causing rapid antimicrobial compounds and enzymes, enhancing its biocontrol
cell lysis (Dobrzyński et al., 2023). B. pumilus also synthesizes potential (Xiao et al., 2024). Field trials have highlighted its dual role
siderophores, such as bacillibactin, which can chelate iron and other in managing nematodes and promoting plant growth. For instance,
essential nutrients, depriving nematodes of crucial resources and strain MH48 was found to reduce fungal infections and improve
fostering beneficial microbial competition in the rhizosphere (Lee nutrient availability in pine seedlings (Won et al., 2018). The synergy
et al., 2016). Additionally, B. pumilus produces antimicrobial of B. licheniformis with other biocontrol agents further enhances its
compounds, including bacteriocins, which disrupt nematode effectiveness in IPM strategies.
metabolic pathways. A guanidine compound from B. pumilus strain
LYMC-3 exhibited potent activity against Bursaphelenchus xylophilus;
the LC50 values were 113.5 and 62.5 mg/L after 24 and 48 h, B. firmus
respectively, highlighting its targeted efficacy (Li et al., 2018). Nano-
bioformulations have improved the stability and bioavailability of B. firmus exhibits remarkable versatility in suppressing nematode
B. pumilus metabolites, ensuring consistent nematode suppression in populations and enhancing plant growth. As an alkaliphilic,
different agricultural conditions (Mahmoud et al., 2016). B. pumilus endospore-forming bacterium, it thrives in various soil environments,
differentiates itself by integrating siderophore-mediated nutrient making it suitable for diverse agricultural systems (Settu et al., 2024).
deprivation with enzymatic and antimicrobial strategies, unlike Bt It is distinguished from other Bacillus spp. by its ability to colonize
(which relies on Cry proteins) or B. cereus (which relies on plant roots and induce systemic resistance, exhibiting both direct

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Vasantha-Srinivasan et al. 10.3389/fmicb.2024.1510036

nematicidal effects and indirect plant-protective effects (Huang et al., B. nematocida

2021). A primary mode of action of B. firmus involves the production
of lytic enzymes, such as chitinases and proteases. These enzymes B. nematocida is a spore-forming bacterium with distinct
target the structural integrity of nematode eggshells and cuticles, nematicidal properties. Thus, it is a pivotal agent for managing
resulting in the degradation and reduced viability of eggs and PPNs. This bacterium is predominantly found in soil and plant
juveniles. Genomic studies on B. firmus strains, such as strain TNAU1, rhizospheres. It utilizes a multifaceted approach involving enzymatic,
have identified genes like chiA and chiB, which are involved in the biochemical, and molecular strategies, which collectively contribute
synthesis of chitinase, an enzyme crucial for breaking down the to its efficacy (Huang et al., 2005). Its nematicidal action is attributed
chitinous components of nematode structures (Settu et al., 2024). This to its ability to secrete lytic enzymes, such as chitinases and
enzymatic degradation not only disrupts nematode development but proteases, which are encoded by genes like chiA, chiB, aprE, and
also facilitates nutrient recycling in the rhizosphere, indirectly nprB. These enzymes target and damage the structural integrity of
benefiting plant health. Moreover, B. firmus produces antimicrobial nematode eggshells and cuticles, directly impairing nematode
peptides, including surfactin and fengycin, which disrupt nematode survival and reproduction. The breakdown of these protective
cell membranes. These lipopeptides interact with membrane lipids, structures not only suppresses nematode populations but also
forming pores that cause ion imbalance, cytoplasmic leakage, and releases essential nutrients, thereby enhancing soil fertility (Sun
eventual nematode death (Daulagala, 2021). For example, strain et al., 2024). Moreover, B. nematocida produces antimicrobial
YBf-10 can significantly reduce M. incognita populations by lipopeptides, such as fengycin, surfactin, and bacillomycin. These
producing these bioactive compounds, effectively suppressing bioactive metabolites disrupt nematode cell membranes by
nematode-induced damage, such as gall formation and egg mass interfering with lipid bilayers, resulting in pore formation, ion
production (Xiong et al., 2015). Among Bacillus spp., B. firmus is leakage, and eventual mortality (Niu et al., 2006; Niu et al., 2011; Niu
distinguished by its efficacy in reducing nematode reproductive et al., 2016; Bo et al., 2022). This biochemical disruption
potential. Strain I-1582, widely studied for its nematicidal efficacy, can demonstrates the potent antagonistic effects of the bacterium on
suppress egg hatching and juvenile viability by producing proteases nematode physiology. A unique aspect of the mode of action of
and secondary metabolites. These metabolites interfere with nematode B. nematocida is the synthesis of 2-heptanone, a volatile compound
signaling pathways essential for reproduction and development, that acts as a nematode attractant. These chemical lures nematodes
offering a comprehensive mechanism for population control (Huang toward the bacterium, enhancing its ability to target and infect
et al., 2021). Furthermore, B. firmus promotes plant growth by nematodes with high precision. This mechanism exemplifies an
enhancing nutrient uptake and root colonization, thereby effectively evolutionary adaptation for host–pathogen interactions, as
mitigating the damage caused by nematode infestations. Comparative highlighted by Zhu et al. (2019). Such attractant-based pathogenicity
analyses have revealed that B. firmus differentiates itself from other differentiates B. nematocida from other Bacillus spp., adding a layer
Bacillus spp. through its robust adaptability to diverse soil pH levels of specificity to its biocontrol efficacy. Recent studies have identified
and its ability to induce systemic resistance. Unlike Bt, which relies on adaptive molecular responses in B. nematocida under stress
Cry proteins for specific gut receptor targeting, or B. subtilis, which is conditions. For example, Sun et al. (2018) reported that protein
known for its VOC-mediated effects, B. firmus integrates multiple acetylation modulates the enzymatic activity of the bacterium,
mechanisms, including enzymatic degradation, lipopeptide enhancing its nematicidal efficacy. This adaptive regulation reflects
production, and systemic resistance induction, to combat nematodes a dynamic interaction between B. nematocida and its nematode
and support plant health. The dual role of B. firmus in nematode targets, showcasing the ability of the bacterium to respond to
suppression and plant growth promotion highlights its suitability for environmental stimuli. Comparative analyses have revealed that
sustainable agricultural practices. Recent advancements in genomic B. nematocida utilizes a highly specialized approach compared with
studies have further elucidated the biocontrol potential of B. firmus. other Bacillus spp. Unlike B. subtilis, which primarily induces
For instance, strain TNAU1 harbors genes encoding nematode- systemic resistance in plants and produces VOCs, or Bt, which relies
virulent proteases and other antimicrobial compounds, which can on Cry proteins for gut-specific toxicity, B. nematocida integrates
enhance its specificity and efficacy against PPNs. Additionally, enzymatic degradation, membrane disruption, and chemical
B. firmus YBf-10 can modulate microbial communities in the attraction to exhibit nematicidal effects. This multipronged strategy
rhizosphere, enriching beneficial microbes and suppressing harmful underscores its effectiveness in managing PPNs while minimizing
pathogens. Thus, it can play a role in IPM strategies (Marin-Bruzos collateral effects on nontarget organisms. The practical application
et al., 2021). Field applications of B. firmus include soil drenching and of B. nematocida has shown promising results in field trials, with its
seed treatments, which ensure effective delivery of bioactive soil drench formulations and seed treatments effectively reducing
compounds to nematode hotspots. Pot experiments using soil- nematode populations and enhancing plant growth. The specificity
drenched YBf-10 revealed substantial reductions in nematode of B. nematocida for nematodes reduces the ecological risks often
populations and an increase in overall plant growth, showcasing its associated with broad-spectrum chemical nematicides. Furthermore,
practical applicability in real-world agricultural systems (Xiong et al., its potential for integration into IPM strategies highlights its role in
2015). B. firmus employs a multifaceted approach involving enzymatic promoting sustainable agriculture. B. nematocida is an advanced
lysis, antimicrobial activity, and systemic resistance induction for biocontrol agent characterized by enzymatic degradation,
managing nematodes. Its ability to thrive in diverse soil environments, biochemical toxicity, and adaptive molecular interactions. Its unique
its biocontrol efficacy, and its plant growth-promoting properties mechanisms of action and its specificity for nematodes make it a
underscore its potential as a key agent in sustainable nematode promising alternative to chemical nematicides, contributing to
management and IPM strategies. environmentally sustainable agricultural practices.

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Vasantha-Srinivasan et al. 10.3389/fmicb.2024.1510036

B. amyloliquefaciens component of sustainable agricultural practices. Overall,

B. amyloliquefaciens employs a synergistic blend of biochemical,
B. amyloliquefaciens exhibits robust nematicidal activity. It is enzymatic, and ecological strategies to control PPNs and enhance
distinct from other Bacillus spp. because of the production of diverse plant health. Continued research on its genetic pathways, interaction
enzymes and bioactive secondary metabolites. Its efficacy is mainly mechanisms, and field applications can further enhance its role in
attributed to its ability to synthesize lipopeptides, such as fengycin and IPM and sustainable agriculture (Table 1).
iturin, which disrupt nematode cell membranes. These lipopeptides
interact with lipid bilayers and cause pore formation and subsequent
cell lysis, resulting in nematode mortality (Ngalimat et al., 2021). B. velezensis
Moreover, B. amyloliquefaciens secretes hydrolytic enzymes, such as
chitinases and proteases, which enzymatically degrade nematode B. velezensis, a species closely related to B. amyloliquefaciens,
cuticles and eggshells, thereby inhibiting juvenile development and exhibits substantial nematicidal activity by producing diverse bioactive
reducing nematode reproduction rates (Migunova and Sasanelli, compounds, making it a key player in sustainable agriculture. Its
2021). Genomic studies have highlighted the roles of various genes, effects are mainly attributed to the production of lipopeptides
such as fenA and ituD, in the biosynthesis of these lipopeptides, (surfactin, fengycin, and iturin), polyketides, and siderophores, which
underscoring the genetic adaptability of the bacterium for biocontrol collectively target PPNs and other phytopathogens (Rabbee et al.,
applications (Luo et al., 2022). In addition to exhibiting direct 2019, 2023). These compounds act by disrupting cell membranes,
nematicidal effects, B. amyloliquefaciens significantly contributes to interfering with metabolic pathways, and creating a hostile
soil health and plant growth. It stimulates plant development by environment for pathogens. Moreover, B. velezensis contributes to soil
producing phytohormones and promotes nutrient availability by health by promoting beneficial microbial communities and enhancing
altering the soil microbiome. For instance, VOCs produced by nutrient cycling, making it a multifunctional agent in IPM systems.
B. amyloliquefaciens not only suppress pathogens but also enhance The nematicidal efficacy of B. velezensis has been well documented in
root growth and nutrient uptake, reinforcing its dual role as a controlled environments (Wu et al., 2023). For instance, strain YS-AT-
biocontrol agent and a growth promoter (Chowdhury et al., 2015). DS1 was found to significantly reduce M. incognita infection rates in
Strain FZB42 exhibits these attributes by inducing systemic resistance tomato plants by affecting water and solute transport mediated by TIP
in plants. ISR is achieved through the activation of JA and ethylene genes, without activating the JA or SA pathway (Hu et al., 2022). This
(ET) signaling pathways, resulting in the increased production of finding highlights the unique mode of action of the strain compared
defense-related enzymes and antimicrobial compounds that protect with other Bacillus spp., which often rely heavily on ISR through JA/
plants from nematodes and other pathogens (Chowdhury et al., 2015). SA pathway activation. Another prominent strain, GB03, has been
The genetic manipulation of B. amyloliquefaciens has further enhanced extensively studied for its ability to enhance plant growth and
its efficacy. For example, the fusion of B. amyloliquefaciens SA5 with immunity by producing VOCs that prime plant defenses by inducing
Lysinibacillus sphaericus created a hybrid strain (Bas8) with elevated systemic resistance (Jang et al., 2023). Strain GB03 is recognized for
chitinase production. This strain exhibited significant nematicidal its practical applications. It has also been validated by the U.S. EPA as
effects against M. incognita in controlled trials (Abdel-Salam et al., an eco-friendly alternative to synthetic pesticides. Its ability to
2018). Similarly, Liu et al. (2013) demonstrated that the deletion of the suppress nematodes, fungi, and bacteria while concurrently promoting
gene RBAM_007470, responsible for the synthesis of plantazolicin, plant health underscores its versatility. Genome sequencing of
reduced the nematicidal efficacy of strain FZB42, highlighting the B. velezensis strains, such as strains Ag109 and FZB42, has provided a
importance of specific metabolites in biocontrol strategies. Field and robust genetic basis for secondary metabolite production. The genome
greenhouse trials have substantiated the biocontrol potential of of these strains has been found to contain 13 gene clusters responsible
B. amyloliquefaciens. For example, applications of this bacterium at for the synthesis of antimicrobial compounds (Borriss et al., 2019).
varying concentrations (50–200%) effectively suppressed M. javanica These metabolites, including surfactin, bacillomycin, and fengycin,
in common beans by inhibiting juvenile hatching and reducing not only inhibit nematode activity but also suppress fungal pathogens,
motility. These effects were observed both in vitro and in vivo, providing a comprehensive biocontrol solution. In one study, strain
showcasing its adaptability across different environmental conditions Ag109 was found to reduce M. javanica and P. brachyurus populations
(Messa et al., 2019). Furthermore, the spiral nematode Helicotylenchus by 69 and 45%, respectively, while exhibiting notable antifungal
dihystera was effectively controlled in soybean fields treated with properties (Mian et al., 2024). Greenhouse studies further validated
B. amyloliquefaciens-based formulations, with the nematicidal effects the nematicidal potential of B. velezensis. Strains BMH and INV
being comparable to those of chemical nematicides, such as caused over 90% reductions in M. incognita gall formation and egg
abamectin. Improvements were also noted in soybean yield and soil masses while concurrently enhancing tomato growth (Cruz‐
health (Camatti et al., 2023). Compared with other Bacillus spp., Magalhães et al., 2022). However, combining these strains did not
B. amyloliquefaciens uniquely combines potent direct nematicidal enhance efficacy, suggesting that competitive interactions among
mechanisms with plant growth-promoting traits. While Bt primarily strains limit their synergistic potential. A novel approach combining
relies on Cry proteins for nematode control and B. subtilis relies on B. velezensis with T. harzianum and gamma radiation-induced
systemic resistance induction, B. amyloliquefaciens integrates mutants caused significant reductions in M. javanica egg hatching
membrane disruption, enzymatic degradation, and systemic resistance (16–45%) and juvenile mortality (30–46%). This synergistic approach,
induction, making it a versatile and holistic agent for nematode when supplemented with chitosan, led to a 94% reduction in
management. Its ability to modulate the soil microbiome and enhance nematode reproduction factors under greenhouse conditions
nutrient cycling further distinguishes it as an indispensable (Rostami et al., 2021, 2024). While B. velezensis has gained widespread

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 TABLE 1 Mode of actions of different isolates or proteins from Bacillus species against major pytopathogenic nematodes.
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Vasantha-Srinivasan et al.
S. no. Bacillus species Isolates/protein name Target species Actions References
1 B. velezensis BMH INV M. incognita Reduction in the number of galls and eggs in tomato roots Cruz‐Magalhães et al. (2022)

2 B. subtilis AP-3 Meloidogyne spp. Effective nematode control when applied post-emergence in sugarcane crops Mazzuchelli et al. (2020)
Pratylenchus spp.

3 B. paralicheniformi FMCH001 Meloidogyne spp. Decreased egg hatching and juvenile survival Díaz-Manzano et al. (2023)
B. subtilis FMCH002

4 B. thuringiensis KYC Meloidogyne incognita Structural damage to nematode eggs and second-stage juveniles Choi et al. (2020)
B. velezensis CE 100

5 B. cereus 09B18 Heterodera filipjevi High mortality of second-stage juvenile nematodes and reduced egg hatchability Zhang et al. (2016)

6 B. subtilis OKB105 Aphelenchoides besseyi Significant inhibition of growth and increased mortality percentage Xia et al. (2011)
B. amyloliquefaciens FZB42 Ditylenchus destructor
Bursaphelenchus xylophilus
M. javanica

7 B. subtilis Bbv 57 M. incognita Reduction in egg hatching capacity and increased juvenile mortality Ramyabharathi et al. (2020)

8 Bacillus cereus 137JC M. exigua High mortality of second-stage juvenile nematodes Oliveira et al. (2014)
B. subtilis 18JC

9 B. velezensis BZR 86 M. incognita Decreased egg hatchability and number of root galls in tomato and cucumber Migunova et al. (2021)
11

plants

10 B.thuringiensis (crystal proteins) Cry55Aa, Cry6Aa, Cry5Ba M. hapla Midgut toxicity in second-stage juveniles Zhang et al. (2012)

11 B. thuringiensis YBT-1518 M. hapla Toxic to second-stage juveniles Guo et al. (2008)

12 B.thuringiensis (crystal proteins) Cry6A M. hapla Toxicity to second-stage juveniles, reduced galling index, and egg masses Yu et al. (2015)

13 B.thuringiensis (crystal proteins) Cry5Ca1 Cry5Da1 M. incognita Negative effects on nematode lifespan, fertility, and survival Geng et al. (2017)

14 B. megaterium YMF3.25 M. incognita Decreased egg hatchability and reduced nematode infections by producing Huang et al. (2010)
nematicidal volatile compounds

15 B. cereus Bc-cm103 M. incognita Over 90% mortality rate in second-stage juveniles (J2) Yin et al. (2021a)

16 B. altitudinis AMCC 1040 M. incognita Volatile compounds block nematode growth Ye et al. (2022)

17 B. velezensis BZR 86 M. incognita High nematicidal activity with improved cucumber plant growth under Asaturova et al. (2022)
BZR 277 greenhouse conditions

18 B. firmus I-1582 H. schachtii Negative impact on nematode reproduction, pathogenicity, and development of the Huang et al. (2021)

10.3389/fmicb.2024.1510036
next generation

19 B. amyloliquefaciens BV03, PTA4838 Helicotylenchus dihystera Bacillus filtrates reduce nematode growth and survival Camatti et al. (2023)
B. firmus MBI600
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B. licheniformis Bf-I1582
B. subtilis FMC001
FMC002

(Continued)
 TABLE 1 (Continued)
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Vasantha-Srinivasan et al.
S. no. Bacillus species Isolates/protein name Target species Actions References
20 B. firmus I-1582 M. incognita Degrades eggshells, colonizes eggs, and improves systematic resistance in tomato Ghahremani et al. (2020)
plants

21 B. cereus IBCBb130 M. incognita High mortality rates (>68%) in second-stage juveniles (J2) Amorim et al. (2024)
B. proteolyticus IBCBb116

22 B. velezensis YS-AT-DS1 M. incognita Reduced infection rate of second-stage juveniles (J2) and the number of galls and Hu et al. (2022)
egg masses on tomato roots

23 B. velezensis Pt-RP9 Bursaphelenchus xylophilus Over 90% mortality rate and lower reproduction rate Sun et al. (2024)

24 B. cereus, Bacillus sp. mixture filtrate M. arenaria 85–90% immobility of Meloidogyne spp. (J2) after 96 h Engelbrecht et al. (2022)
B. megaterium, M. incognita
B. subtilis M. javanica
B. thuringiensis M. enterolobii

25 Bacillus Sp. Bacterial volatiles M. graminicola Lethal to second-stage juveniles (J2) and significantly reduced infection of Bui et al. (2020)
susceptible rice

26 B. velezensis Bv-25 M. incognita Achieved 100% J2 mortality, decreased expression of ord-1, mpk-1, and flp-18 Tian et al. (2022)
genes in M. incognita, and elevated expression of defense genes (pr1, pr3, and lox1)
in cucumber plants

27 B. halotolerans DDWA M. incognita Suppressed M. incognita up to 69.96% under greenhouse conditions and increased Liu et al. (2020)
12

B. kochii DDWB tomato yield

B. oceanisediminis DDWC
B. pumilus DDWD
B. toyonensis DDWNEI
B. cereus DDWWAI
B. pseudomycoides JNC

28 B. altitudinis AMCC1040 M. incognita Reduced root-knot nematode damage to ginger Wang et al. (2021a)

29 B. cereus AMA3 Bursaphelenchus xylophilus Reduced survival, fecundity, and host adaptability Yuan et al. (2023)
AA3
YW4

30 B. cereus KMT-5 M. javanica Declined egg hatchability (96%) and 89% second-stage juvenile (J2) mortality Antil et al. (2022a)
B. megaterium KMT-8

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31 B. subtilis MTCC441 M. incognita Egg mortality of 85% at 35 ppm dosage and maximum ovicidal activity (83%) Nadeem et al. (2021)

32 B. megaterium GIUBAM-2020 M. incognita Volatile organic compounds induced oxidative stress leading to mortality Maqsood et al. (2024)

33 B. cereus NJSZ-13 B. xylophilus Protease isolated from B. cereus causes cuticle degradation Li et al. (2023)
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(Continued)
 TABLE 1 (Continued)
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Vasantha-Srinivasan et al.
S. no. Bacillus species Isolates/protein name Target species Actions References
34 B. cereus RBI2AB2.1 Meloidogyne Sp. Decreased the number of eggs and second-stage juveniles (J2) Habazar et al. (2021)
B. mycoides RBI2AB2.2
B. subtilis RBIKDA2.2
Bacillus sp. IR.1.3.4
RBI1IBPL2.3
RBIKDA1.2
RZ21AP1
RZ22AG2

35 B. aryabhattai KMT-4 M. javanica 73% reduction in eggs and 80% reduction in galls in plant roots (S. lycopersicum) Antil et al. (2021)

36 B. subtilis Culture filtrate M. incognita Eggs were infected up to 48% Singh et al. (2021)

37 B. subtilis AP-3 M. incognita Promoted reduction of nematode reproduction factor and gall index in the roots Bavaresco et al. (2021)

38 B. velezensis AP03 M. incognita Increased second-stage juvenile (J2) mortality and inhibited egg hatchability Pacifico et al. (2021)
S2527
S2545

39 B. paralicheniformis TB197 M. incognita Showed >95% of nematicidal activity under in vitro and in vivo conditions Chavarria-Quicaño et al.
(2023a,b)

40 B. velezensis FC37 M. hapla Reduced plant disease severity, crown incidence and severity, and petiole Camacho et al. (2023)
13

colonization

41 B. simplex Sneb545 H. glycines Improved disease resistance in soybean roots Kang et al. (2020)

42 B. megaterium Sneb207 H. glycines Reduced the number of cysts, SCN juveniles, and eggs and promoted soybean Zhou et al. (2021)
growth

43 B. cereus Bc-cm103 M. incognita Volatile compounds delivered fumigation activity and higher mortality rates Yin et al. (2021b)
(97.2%) of j2.

44 B. flexus DK-Sa-A1 G. rostochiensis ≥50% cyst and egg mortality Widianto et al. (2021)
B. pumilus KB-Se-A2
B. cereus KT-Se-A2
B. megaterium PB-Sa-A2
B. subtilis SRJ-Sa-A1

45 B. subtilis MCC 0067 M. javanica Decreased the nematode numbers (36%) in combination with Glomus mosseae and Sohrabi et al. (2020)

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Trichoderma harzianum

46 B. velezensis VB7 M. incognita Increased juvenile mortality by 87.9% and Induced MAMP-triggered nematode Kamalanathan et al. (2023)
immunity increasing the expression of defense genes WRKY, LOX, PAL, MYB, and
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PR

(Continued)
 TABLE 1 (Continued)
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Vasantha-Srinivasan et al.
S. no. Bacillus species Isolates/protein name Target species Actions References
47 B. altitudinis 123.en M. incognita Reduced the number of galls, egg masses, and juvenile populations in the soil, and Banihashemian et al. (2023)
increased expression of pathogenesis-related genes (PR-1 and PR-5) in treated kiwi
fruit plants

48 B. subtilis - M. incognita Bacteria grown with MnCl2 and CuCl2 significantly increased juvenile mortality Adiwena et al. (2023)
and suppressed their chemotaxis response to tomato roots

49 B. atrophaeus GBSC56 M. incognita GBSC56 volatiles caused high juvenile mortality, induced oxidative stress, and Ayaz et al. (2021)
enhanced defense gene expression in tomato plants

50 B. amyloliquefaciens D747 M. enterolobii reduced nematode eggs and gall index on cucumber roots in combination with de Paula et al. (2024)
Purpureocillium lilacinum

51 B. cereus NRC12 M. incognita Protoplast fusion between B. cereus and B. thuringiensis produced a fusant strain Mohamed et al. (2021)
that significantly increased nematode mortality and enhanced eggplant growth

52 B. amyloliquefaciens SA5 M. javanica Fusant strains of B. amyloliquefaciens and Lysinibacillus sphaericus delivered Osman et al. (2020)
significant inhibition of nematode

53 B. altitudinis KMS-6 M. javanica reduced nematode infestations and enhanced eggplant growth compared to Antil et al. (2022b)
Carbofuran treatment

54 B. thuringiensis B7 Meloidogyne ssp. high inhibitory activity, killing up to 89.67% nematode eggs and 100% of J2 within Khanh (2020)
10 h
14

55 B. cereus BCM2 M. incognita BCM2 extracellular proteins caused 100% mortality by damaging the nematode Hu et al. (2020)
cuticle and eggshell, leading to content leakage

56 B. megaterium C3 M. javanica Inhibition of Egg-hatchability (20–28%) Rostami et al. (2021)

B. safensis VW3

57 B. subtilis SJ19 Meloidogyne spp. controlled 67.75% of tomato root-knot nematodes in combination with other Shu et al. (2021)
biological compounds

58 B. megaterium – M. incognita nematicidal potential and significant chitinolytic activity combination with Serratia Abdellatif et al. (2021)
B. subtilis marcescens

59 Bacillus Sp. GBSC56 Aphelenchoides besseyi Compounds of Bacillus sp. demonstrated high nematicidal activity against and Ali et al. (2023)
SYST2 enhanced growth and defense gene expression in rice seedlings
FZB42

60 B. amyloliquefaciens QST713 M. incognita Effectively manage nematode in cotton through direct antagonistic capabilities and Gattoni et al. (2022)

10.3389/fmicb.2024.1510036
B. firmus I-1582 systemic resistance involving JA and SA pathways

61 B. subtilis MN252542.1 M. javanica Showed 100% mortality and hatching inhibition of nematodes in combination with Das et al. (2021)
P. fluorescens
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62 Brevibacillus laterosporus F5 strain M. incognita over 90% mortality of juveniles Hamze and Ruiu (2022)

63 B. wiedmannii MW405861 M. incognita significantly reduced nematode galls and egg masses in tomatoes in combination Moslehi et al. (2021)
with S. liquefaciens

(Continued)
 TABLE 1 (Continued)
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Vasantha-Srinivasan et al.
S. no. Bacillus species Isolates/protein name Target species Actions References
64 B. pumilus MZ675428 M. incognita Reduced nematode root galling and reproduction on tomatoes, enhancing plant Devindrappa et al. (2023)
B. megaterium MZ675429 defense gene expression and enzyme activity than chemical nematicide fluopyram
B. subtilis MZ675430
B. cereus MZ675431

65 B. subtilis - M. incognita Lettuce roots treated with B. subtilis made root exudates repellent to J2 Cavalcanti et al. (2024)

66 B. pumilus S1-10 M. incognita Volatile compound (2-(methylamino)-ethanol (2-ME)) reduced nematodes growth Dai et al. (2023)
and eggs

67 B. wiedmannii AzBw1 M. arenaria Siderophores, protease, and chitinase from Bacillus sp. with protease activity Fallahzadeh-Mamaghani et al.
nematicidal effect reducing egg hatching by 34% and increasing juvenile mortality (2023)
by 33.5%.

68 Bacillus Sp. Soil filtrate M. incognita Reduced the growth and development of J2. Engelbrecht et al. (2020)

69 B. thuringiensis App6Aa2 B. xylophilus Toxic proteins delivered higher toxicity and severe intestinal damage to nematode Guo et al. (2022)
Cry13Aa1 Cry12Aa1 Cry5Ba3
Xpp55Aa1
Cyt8Aa1

70 B. amyloliquefaciens FR203A M. ethiopica Reduced nematode index damage and reproductive indices in grapevine roots Aballay et al. (2020)
B. megaterium FB133M X. index
15

B. thuringiensis FS213P
B. weihenstephanensis FB833T
B. frigoritolerans FB25M
FB37BR

71 Bacillus Sp. 85 isolates M. incognita Twenty-three Bacillus isolates caused >75% mortality of juveniles, and 10 strains Wang et al. (2021b)
inhibited nematode development in pot experiments

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FIGURE 4
Major Bacillus species and their diverse array of proteins and secondary metabolites against the plant-parasitic nematodes. Information adapted from
[1] Kahn et al. (2021), [2] Ghahremani et al. (2020), [3] Kulkova et al. (2023), [4] Niu et al. (2006), [5] Jamal et al. (2017), [6] Manju and Subramanian, 2017,
and [7] Hu et al. (2022).

recognition for its biocontrol properties, its dual nature requires protection to seedlings by colonizing the root zone and creating a
careful management. Reports of pathogenicity in various crops, such hostile environment for nematodes. Additionally, foliar sprays with
as peaches, onions, and potatoes, necessitate stringent application Bacillus formulations can induce systemic resistance in plants, thereby
strategies to avoid unintended consequences (Rabbee et al., 2019). activating defense mechanisms that reduce nematode penetration and
Hence, understanding strain-specific interactions and environmental reproduction. Biofertilizers incorporating Bacillus strains can
conditions is crucial to optimize its use. Compared with other Bacillus be directly applied to the soil or used for root drenching, thereby
spp., B. velezensis has unique strengths, including its genetic diversity, enhancing nutrient availability and promoting robust plant growth.
robust secondary metabolite production ability, and ability to This can help plants withstand nematode attacks.
influence plant physiology through nontraditional ISR pathways. For In IPM programs, Bacillus strains are often combined with other
its integration into sustainable agriculture, further research should biocontrol agents, chemical treatments, or cultural practices,
be conducted on its ecological interactions and application providing a multifaceted approach for the management of nematodes.
methodologies to ensure that its potential is maximized and risks are For instance, integrating B. subtilis with organic amendments and
minimized. The major Bacillus spp. and their diverse array of proteins reducing the use of chemical nematicides have led to enhanced
and secondary metabolites against PPNs are schematically displayed efficacy against root-knot nematodes, thereby lowering infestations
in Figure 4. and improving crop yields. Such synergistic approaches can reduce
reliance on chemical inputs while maintaining nematode suppression.
B. amyloliquefaciens formulations have exhibited notable efficacy in
Application methods and strategies field trials by reducing cyst nematode populations and promoting
plant health through the induction of systemic resistance. This
Various methods and strategies can be used for the application of approach reduces reliance on chemical nematicides and promotes
Bacillus spp. to effectively manage phytopathogenic nematodes. A sustainable agricultural practices. Bacillus strains are being
widely used approach is soil amendment, which involves mixing increasingly recognized for their potential for managing PPNs because
Bacillus inoculants with organic matter, such as compost or manure, of their diverse modes of action and adaptability to different
to improve soil structure and health. This method indirectly agricultural environments. They produce various secondary
suppresses nematode populations by fostering beneficial microbial metabolites, such as lipopeptides, enzymes, and antibiotics, which
communities and enhancing plant resilience (Fabiyi, 2024). Seed directly inhibit nematodes through a process known as direct
treatment is another effective strategy. It involves the coating of seeds antagonism (Iftikhar et al., 2020). These metabolites disrupt nematode
with Bacillus spores before planting. This approach confers early membranes, degrade their structural proteins, or interfere with their

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FIGURE 5
Graphical representation of how the application of Bacillus strains as soil amendments alone or in combination with organic matter enhances soil
health and structure and reduces nematode proliferation through several interrelated mechanisms.

signaling pathways, resulting in reduced nematode viability and conferred resistance against the pathogen H. glycines in soybeans.
infectivity (Bhat et al., 2023). The detailed mechanisms of the different Among these compounds, the cyclic dipeptide Val-Pro, tryptophan,
application strategies of Bacillus spp. for managing nematodes are and uracil were particularly effective in inducing defense-related gene
outlined below and presented in Figure 5. expression in soybeans, offering potential novel agents for managing
this destructive nematode.

ISR
Soil amendments and biofertilizers
Bacillus strains can trigger plant defense mechanisms, enhancing
the ability of plants to resist nematode infections (Choudhary and The application of Bacillus strains as soil amendments alone or in
Johri, 2009). ISR is achieved through the upregulation of plant combination with organic matter can significantly improve soil health
defense-related genes, resulting in the production of pathogenesis- and structure, creating an environment less conducive to nematode
related proteins and other defense-related compounds that inhibit proliferation. Bacillus-based biofertilizers not only enhance plant
nematode invasion and reproduction (Mahapatra et al., 2022). Bacillus growth but also foster beneficial microbial communities in the
strains produce specific elicitors, such as lipopeptides, VOCs, and rhizosphere, in turn antagonizing nematodes (Fabiyi, 2024). For
secondary metabolites, which prime the plants to enhance defense instance, Tong-Jian et al. (2013) demonstrated that the use of B. cereus
responses. Upon nematode attacks, these primed plants exhibit strain X5 in combination with bio-organic fertilizers and
accelerated production of pathogenesis-related proteins, oxidative biofumigation materials significantly improved plant biomass and
enzymes, and secondary metabolites, thereby reducing nematode reduced nematode infestation under greenhouse and field conditions.
penetration, nematode reproduction, and overall damage. Adam et al. This suggests its potential for integrated nematode management in
(2014) found that certain B. subtilis strains, known for their antifungal agricultural systems. Moreover, a consortium of three plant growth-
properties, can effectively reduce root-knot nematode infestations in promoting rhizobacteria—B. cereus (AR156), B. subtilis (SM21), and
tomatoes, primarily through ISR rather than direct antagonism. This Serratia sp. (XY21)—was found to reduce root-knot nematode disease
demonstrates the potential of multipurpose bacteria for IPM in severity in cucumbers by up to 72%. This consortium not only
nematode–fungal disease complexes. Additionally, Xing et al. (2020) enhanced yield and fruit quality but also improved soil properties by
identified six ISR-active compounds from B. simplex Sneb545 that increasing the abundance of disease-suppressive bacterial genera in

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the rhizosphere. The resulting changes in the microbial community including the colonization of the rhizosphere, induction of systemic
positively correlated with improvements in soil chemical properties, resistance, enhancement of soil microbial communities, production of
contributing to nematode suppression and overall plant health (Zhang antimicrobial compounds, improvement of soil structure, and reduction
et al., 2024). The several interrelated mechanisms through which of phytopathogens (Figure 6). When seeds are treated with Bacillus
Bacillus spp. improve soil health and reduce nematode proliferation strains, these beneficial bacteria colonize the root zone as the plant
when used as soil amendments alone or in combination with organic germinates and grows. This early colonization creates a protective
matter are illustrated in Figure 5. microbial shield around the roots, i.e., the rhizosphere, which acts as the
first line of defense against nematode invasion. Bacillus strains occupy
key ecological niches in the soil and outcompete nematodes for space
Seed treatment and nutrients, thereby reducing the likelihood of nematode attachment
and penetration into plant roots (Hu et al., 2017). Moreover, Bacillus
Treating seeds with Bacillus spores confers early protection to strains induce systemic resistance in plants through seed treatment,
seedlings against nematodes. As the seeds germinate, Bacillus spp. priming the immune system of plants to respond more robustly to
colonize the root system, forming a protective barrier that hinders nematode attacks by activating JA and ET pathways (Choudhary and
nematode penetration and colonization (Diyapoglu et al., 2022). Seeds Johri, 2009). The introduction of Bacillus strains via seed treatment
are treated with Bacillus strains using different methods, such as dry enriches the soil microbiome. These beneficial bacteria promote the
coating, wet coating, or pelletization, to ensure even distribution and growth of other advantageous microorganisms, such as mycorrhizal
firm adherence of the bacteria to the seeds. After coating, the seeds are fungi and nitrogen-fixing bacteria, collectively improving soil health and
carefully dried and packaged to preserve bacterial viability. Upon structure. A rich and diverse microbial community enhances nutrient
planting, Bacillus spores germinate alongside the seeds. They colonize cycling, organic matter decomposition, and soil aggregation, creating a
the root zone and confer protection against nematodes while more stable and fertile soil environment that can support healthy plant
promoting plant growth and soil health (Migunova and Sasanelli, 2021). growth and reduce nematode populations (Chernov and Semenov,
Seed treatment with Bacillus strains can improve soil health and 2021). Additionally, antimicrobial compounds produced by Bacillus
reduce nematode proliferation through several key mechanisms, strains can degrade nematode eggs, inhibit juvenile development, and

FIGURE 6
Graphical representation of how seed treatment with Bacillus spp. enhances plant growth, improves soil health, and reduces nematode populations.

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reduce nematode motility, thereby limiting the ability of nematodes to significantly affect overall soil health through biochemical, microbial,
infect plant roots. The persistence of these antimicrobial substances in and ecological interactions (Vasques et al., 2024). They enhance soil
the rhizosphere helps maintain a soil environment hostile to nematodes microbial diversity and activity by producing various secondary
(Diyapoglu et al., 2022). Moreover, when applied to seeds, Bacillus strains metabolites, such as lipopeptides, antibiotics, and VOCs, which act as
colonize the rhizosphere—the area of soil directly affected by root antagonists to soilborne pathogens. These bioactive compounds
exudates and associated soil microorganisms—and produce extracellular disrupt the growth of phytopathogenic fungi, bacteria, and nematodes,
polymeric substances (EPS). These complex organic molecules are thereby fostering a healthier and more balanced soil microbiome
crucial for improving soil structure. EPS act as a natural adhesive and (Miljaković et al., 2020). Moreover, the metabolites released by Bacillus
bind soil particles together to form stable aggregates, in turn enhancing spp. often serve as signaling molecules, promoting beneficial microbial
soil porosity, promoting better air circulation, and improving water symbiosis and microbial niche differentiation within the rhizosphere.
infiltration (O’Callaghan, 2016). Improved soil structure not only A crucial mechanism through which Bacillus spp. influence soil health
enhances root growth and plant vigor but also creates a less favorable is the decomposition of organic matter by secreting hydrolytic
environment for nematode movement and survival, as nematodes prefer enzymes, such as cellulases, proteases, and chitinases. These enzymes
compact, poorly aerated soils (Khan et al., 2022). accelerate the breakdown of complex organic materials into simpler
Overall, seed treatment with Bacillus strains represents a compounds, improving soil organic carbon content and nutrient
multifaceted approach for the management of nematodes by availability (Riseh et al., 2024). Bacillus spp. produce chitinases that
enhancing soil health, improving plant resilience, and directly degrade chitin-containing structures, such as nematode eggshells and
suppressing nematode populations. Thus, it is a more sustainable and fungal cell walls, thereby facilitating the recycling of essential elements,
effective method of nematode control (Zhang et al., 2009; O’Callaghan, such as nitrogen and carbon, within soil ecosystems. This degradation
2016; Hsiao et al., 2023; Hayat et al., 2023). process releases N-acetylglucosamine monomers, which serve as
nutrient sources for various soil microorganisms, thereby enhancing
nutrient cycling and soil fertility. The breakdown of these structures by
Foliar application Bacillus-derived chitinases also suppresses soilborne pathogens and
pests, contributing to a healthier soil microbiome (Gomaa, 2021).
Foliar application of Bacillus spp. is an effective biocontrol strategy Moreover, Bacillus spp. play a vital role in nutrient cycling, particularly
for managing phytopathogenic nematodes (Shafi et al., 2017). This in nitrogen fixation and phosphate solubilization. Certain strains, such
process involves culturing selected Bacillus strains and formulating as B. subtilis and B. megaterium, possess the genetic and enzymatic
them into a sprayable solution. Optimal timing is crucial for the machinery required for solubilizing insoluble phosphates in the soil.
success of this method, with applications typically performed during They produce organic acids (e.g., gluconic acid and citric acid) and
early plant growth stages under favorable environmental conditions phosphatases and convert insoluble phosphates into plant-accessible
to ensure effective colonization. Uniform application using sprayers forms, such as dihydrogen phosphate (Saeid et al., 2018). Several
ensures that the bacteria adhere well to plant surfaces, thereby Bacillus spp., including Paenibacillus polymyxa and P. macerans,
inducing systemic resistance and protecting against nematode damage contain nitrogenase enzymes that enable them to fix atmospheric
(Fu et al., 2020). This method has gained popularity in the U.S., China, nitrogen into ammonia, thereby enhancing soil fertility and providing
India, Brazil, Spain, and South Africa, particularly for high-value essential nutrients for plant growth. This biological nitrogen fixation
crops in areas with substantial nematode pressure (Chien and Huang, facilitates sustainable agricultural practices by reducing the need for
2020; Efthimiadou et al., 2020; Karačić et al., 2024). The effectiveness chemical nitrogen fertilizers. Studies have demonstrated the efficacy of
of foliar application is attributed to a combination of direct these bacteria in promoting plant growth through nitrogen fixation (Li
antagonism, ISR, and plant health enhancement, which collectively et al., 2022). Bacillus spp. can enhance soil structure by secreting EPS,
reduce nematode populations and improve crop growth and yield which facilitate the aggregation of soil particles. This aggregation
(Esitken et al., 2002; Ryu et al., 2011; El-Sawy et al., 2023). improves soil porosity, aeration, and water infiltration, thereby
However, the success of this approach hinges on optimizing the promoting plant root growth and nutrient uptake. Additionally, the
application techniques and timing and understanding the specific production of EPS facilitates moisture retention and reduces soil
interactions between Bacillus spp., the host plant, and the target erosion, thereby enhancing soil resilience under stress conditions.
nematode species (Shafi et al., 2017). Despite the advantages, including These benefits underscore the role of Bacillus spp. in sustainable soil
reduced environmental impacts and improved plant vigor, various management and plant health enhancement (Olagoke et al., 2022).
challenges need to be addressed; these include ensuring consistent Moreover, Bacillus spp. can induce systemic resistance in plants,
root protection and managing environmental variables (Abd-Elgawad indirectly influencing soil health by reducing pathogen pressure.
and Askary, 2020). Thus, continued research and field trials will Bacillus-treated plants exhibit enhanced production of antimicrobial
be crucial for refining this strategy and integrating it into sustainable compounds and defense-related enzymes through the activation of JA
nematode management programs. and SA pathways. This reduces the likelihood of pathogen colonization
and minimizes disease-mediated disruptions to soil microbial
dynamics (Kloepper et al., 2004). While Bacillus spp. offer numerous
Soil health status after the application of benefits as biocontrol agents, their application must be carefully
Bacillus strains managed to maintain ecological balance within the soil microbiome.
Overapplication or improper use can result in the overdominance of
The application of Bacillus spp. as biocontrol agents provides Bacillus strains, potentially suppressing other beneficial
multifaceted benefits beyond nematode suppression. Bacillus spp. microorganisms and disrupting microbial community structures. This

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imbalance may result in competition for resources, negatively as a seed treatment in combination with a vermicompost-enriched soil
impacting native microbial populations and overall soil health (Li et al., application significantly reduced nematode populations by 69.3% and
2022). Therefore, it is crucial to monitor and regulate the use of disease incidence by 70.2%, resulting in a 28.8% increase in carrot
Bacillus-based biocontrol agents in order to preserve the diversity and yield. This integrated approach outperformed chemical treatments,
functionality of soil microbial communities. Sustainable management highlighting the efficacy of B. subtilis IIHR BS-2 in managing the
practices, including the rotation of microbial inoculants, integrated use M. incognita–Pectobacterium carotovorum disease complex in carrots.
of organic amendments, and minimal use of chemical treatments, can Thus, the strategic incorporation of Bacillus strains into IPM
mitigate these risks and optimize the long-term benefits of programs has several advantages, including sustainable nematode
Bacillus applications. management, enhanced efficacy through synergistic effects, and
improved resistance management (Wepuhkhulu et al., 2011). Regular
monitoring of nematode populations and crop health is crucial for
IPM optimizing the timing and application of Bacillus treatments to ensure
the highest efficacy in conjunction with other control measures
Incorporating Bacillus strains into IPM strategies offers an (Chinheya et al., 2017). By integrating Bacillus strains into a
effective and sustainable approach for the management of comprehensive IPM strategy, farmers can achieve long-term nematode
phytopathogenic nematodes. Bacillus spp., such as B. subtilis and Bt, suppression, reduce reliance on chemical pesticides, and ultimately
employ multiple mechanisms to suppress nematodes (Gassmann improve crop productivity and sustainability in agricultural systems
et al., 2008; Jaiswal et al., 2022). These strains not only produce (Figure 7).
nematicidal compounds but also promote plant growth by producing
phytohormones and enhancing nutrient availability. This dual action
improves crop health and resilience, further mitigating the impact of Scalability and cost-effectiveness of
nematode infestations (Abd-Elgawad and Askary, 2018). Bacillus applications
Within an IPM framework, Bacillus strains are most effective
when used in combination with other biocontrol agents, chemical Bacillus spp. are recognized for their scalability as biocontrol
nematicides, and cultural practices. For instance, the application of agents, primarily because of their ability to form resilient spores that
B. firmus strain 1–1,582 in combination with chemical nematicides can be produced on a large scale through cost-effective industrial
and organic amendments significantly enhanced tomato yield and fermentation processes (Serrão et al., 2024). These spore-based
effectively suppressed M. incognita and P. lycopersici populations formulations exhibit extended shelf lives and require minimal storage
under greenhouse conditions, particularly when environmental conditions, thereby reducing logistical expenses for farmers,
conditions were less favorable for nematode development. These especially in resource-limited regions (Cho and Chung, 2020).
findings underscore the potential of B. firmus as a viable component Moreover, Bacillus formulations are compatible with existing
of IPM strategies during tomato cultivation (d'Errico et al., 2019). agricultural practices, including seed treatments, soil amendments,
A recent review by Paradva and Kalla (2023) highlighted the and foliar sprays, facilitating their integration into IPM systems.
potential of microbial biocontrol agents, particularly Bacillus-based Their synergistic interactions with organic amendments, such as
nanoparticles, as sustainable and eco-friendly alternatives to chemical compost, and microbial consortia further enhance their efficacy and
pesticides for plant disease and pest management. The synergistic use cost-effectiveness (Asif et al., 2024). Economic analyses have
of Bacillus strains with nematophagous fungi or predatory nematodes indicated that Bacillus-based products can significantly reduce
can confer multilevel protection by targeting different stages of the reliance on chemical nematicides and fertilizers, resulting in
nematode life cycle (Gassmann et al., 2008; d'Errico et al., 2019). substantial cost savings. For instance, the application of B. subtilis
Native Bacillus strains, such as B. marisflavi CRB2 and B. subtilis during tomato cultivation has been shown to reduce nematode-
CRB7, which harbor multiple antimicrobial peptide genes, have been induced losses by over 60%, resulting in notable yield improvements
proven to be effective against M. incognita in okra. Within an IPM and financial benefits (Pontes et al., 2024). Case studies from
framework, these strains have caused significant reductions in countries like Brazil and India have demonstrated the successful
nematode incidence and improvements in crop yields in laboratory, large-scale application of Bacillus spp. in soybean and rice production
pot, and field trials (Gurikar et al., 2022). When applied with reduced systems, respectively (Galbieri et al., 2023; Pandey et al., 2024).
doses of chemical nematicides, Bacillus strains can help lower the use Moreover, smallholder farmers in Africa have adopted these
of chemical treatments and maintain effective nematode control, formulations because of their affordability and effectiveness across
thereby minimizing the potential for resistance development and various crops, including maize and vegetables (Vasques et al., 2024).
environmental impacts (Ruiu, 2015). Moreover, cultural practices, Cost comparisons have revealed that Bacillus-based biopesticides are
such as crop rotation, cover cropping, and the use of organic soil approximately 30–50% less expensive than chemical alternatives,
amendments, enhance the efficacy of Bacillus applications by creating enhancing their appeal in low-income regions (Hezakiel et al., 2024).
less favorable conditions for nematode proliferation and supporting a In addition to economic advantages, these biopesticides offer
healthier soil microbiome (Singh et al., 2019). For instance, the significant environmental benefits by reducing pollution and health
integration of B. subtilis with cow manure resulted in a 54% reduction risks associated with chemical nematicides, thereby contributing to
in PPN populations in common beans and preserved nematode global sustainability goals (Köhl et al., 2019). They also promote
biodiversity, thereby serving as a sustainable and effective pest ecological balance by enhancing soil biodiversity and mitigating
management strategy (Wepuhkhulu et al., 2011). Furthermore, Rao secondary pest outbreaks, further reinforcing their role in sustainable
et al. (2017) demonstrated that the application of B. subtilis IIHR BS-2 agriculture (Abd-Elgawad, 2024).

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FIGURE 7
Graphical representation of integrated pest management strategies using Bacillus strains for nematode control.

Challenges and limitations The efficacy of Bacillus strains in nematode control is significantly
influenced by soil type, climatic conditions, and interactions with
The application of Bacillus strains as biocontrol agents for other soil microorganisms (Shafi et al., 2017; Singh et al., 2023).
managing nematodes in agricultural systems has several challenges Bacillus strains often perform more consistently in controlled
and limitations. Environmental factors, such as soil type and environments, such as greenhouses, where conditions are more
climate, play crucial roles in determining the efficacy of these predictable and manageable. However, translating the obtained results
bacteria. Soil characteristics, including pH, organic matter content, to field conditions can be challenging because of the variability in
and texture, can significantly influence the survival, colonization, environmental factors across different geographical locations and crop
and nematicidal activity of Bacillus strains. For instance, sandy systems (Ayaz et al., 2023).
soils may cause the bacteria to leach away, while heavy clay soils Despite the promising potential of Bacillus spp. in managing
could limit bacterial distribution (Gurikar et al., 2022). PPNs, several challenges need to be overcome to ensure consistent
Additionally, climatic conditions, particularly temperature and efficacy under field conditions. Environmental factors, such as soil
moisture levels, can significantly influence the efficacy of Bacillus type, temperature, moisture level, and pH, can significantly impact the
spp. (Ayaz et al., 2023). Extreme temperatures can inhibit bacterial survival, colonization, and biocontrol activity of Bacillus strains (Shafi
activity, while optimal moisture levels are necessary for the et al., 2017). Additionally, the presence of native soil microbiota can
germination and functioning of bacterial spores. Furthermore, necessitate competitive interactions that may suppress the
interactions with other soil microorganisms can limit the establishment and function of introduced Bacillus spp. Native
establishment of Bacillus strains because of competition for microorganisms compete with introduced Bacillus strains for essential
resources or antagonistic effects. nutrients and ecological niches. This competition can limit the growth
In addition to environmental factors, regulatory and safety and activity of the biocontrol agents, thereby reducing their
concerns pose substantial barriers to the widespread use of Bacillus effectiveness against PPNs. For instance, indigenous soil bacteria may
strains as biocontrol agents. The approval process for these biocontrol outcompete introduced Bacillus strains for carbon sources, thereby
agents involves rigorous testing to ensure their safety for humans, inhibiting their proliferation (Mawarda et al., 2022). Moreover, native
animals, and the environment. This process can be time-consuming microorganisms can form biofilms on root surfaces, creating physical
and expensive, particularly for smaller companies, thereby delaying barriers that can prevent Bacillus spp. from accessing plant roots and
the introduction of effective biocontrol products. exhibiting their biocontrol effects. These biofilms can effectively

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exclude introduced bacteria from key interaction sites. For instance, including transcriptomics, RNA interference, and CRISPR/Cas9, are
biofilms formed by indigenous Pseudomonas spp. can inhibit the root increasing our understanding of plant–nematode interactions and
colonization of introduced Bacillus strains (Steinberg et al., 2020). boosting plant resistance to root-knot nematodes. Engineered Bacillus
Additionally, field variability significantly influences the efficacy of strains exhibit improved activity against nematodes, offering a broad-
Bacillus spp. as biocontrol agents, with the outcomes in controlled spectrum biocontrol solution that is highly specific to target pests
environments often differing from those in diverse agricultural (Danilova et al., 2023).
settings. Environmental factors, such as soil type, pH, moisture level, Although genetic engineering has significant potential for
temperature, and organic matter content, play crucial roles in the enhancing the nematicidal efficacy of Bacillus strains, its use is
survival, colonization, and activity of introduced Bacillus strains associated with several biosafety concerns. Unintended ecological
(Serrão et al., 2024). To overcome these challenges, comprehensive impacts, such as the disruption of native microbial communities or
field studies need to be conducted. Moreover, robust Bacillus off-target effects on nontarget organisms, must be carefully evaluated
formulations that can withstand environmental fluctuations and can (Samal et al., 2024). Horizontal gene transfer poses additional risks,
be effectively integrated into existing soil microbial communities need potentially resulting in the spread of engineered traits to unintended
to be developed. microbial populations. Regulatory hurdles, including stringent testing
For the commercialization and large-scale application of Bacillus for environmental and public health safety, also pose significant
strains, significant hurdles related to formulation, storage, and challenges. For example, the process of obtaining approval for
regulatory approval need to be overcome (Montesinos, 2003; Butu genetically modified Bacillus strains varies across jurisdictions, with
et al., 2022). The stability and shelf life of Bacillus products can extensive environmental impact assessments required to ensure
be affected by formulation methods, storage environments, and compliance with biosafety standards (Rozas et al., 2024).
shipment conditions. To ensure the success of Bacillus spp. as Formulation improvements have been a major focus in the
biocontrol agents, it is essential to enhance formulation technologies, advancement of Bacillus-based biocontrol products (Tong-Jian et al.,
extend product shelf life, and reduce production costs (Ortiz and 2013; Umamaheswari et al., 2020). Innovations in this area include the
Sansinenea, 2023). Ongoing efforts by researchers and industry development of more stable and effective formulations to maximize
partners are focused on optimizing microbial strains for large-scale the viability and efficacy of Bacillus derivatives (Chavarria-Quicaño
applications, in addition to ensuring that these products meet rigorous et al., 2023a,b). A significant advancement is microencapsulation. In
environmental and human health safety standards (Hossain this process, spores are enclosed within a protective matrix to shield
et al., 2023). them from environmental stressors while enabling controlled release
These challenges underscore the need for continued research and (Gao et al., 2024). This technique has been crucial for maintaining the
collaboration to effectively integrate Bacillus strains into sustainable viability of spores over extended periods, thereby enhancing the shelf
agricultural practices. Safety evaluations must also ensure that Bacillus life and effectiveness of the product (Khullar et al., 2024).
strains do not pose risks to nontarget organisms or the environment Researchers are also exploring synergistic combinations of
and do not have unintended ecological impacts, such as the disruption Bacillus strains with other biocontrol agents or biostimulants in order
of soil microbial communities or induction of resistance in pest to create multifunctional formulations that can confer comprehensive
populations (Ayaz et al., 2023). Public perception and acceptance of plant protection and promote plant growth. Advances in delivery
microbial biocontrol agents further complicate their application, systems and increases in shelf life have further revolutionized the
highlighting the need for better education and communication about application of Bacillus-based biocontrol agents (Karačić et al., 2024).
their safety and benefits. Addressing these challenges is essential to Novel delivery systems, such as nano-bioformulations and polymer-
fully harness the potential of Bacillus strains for sustainable nematode based carriers, are being developed to optimize the precision and
management (Hossain et al., 2023). efficacy of Bacillus applications (Behl et al., 2024). These systems are
designed to optimize the release of active agents at the site of infection,
thereby reducing the need for frequent applications and lowering the
Recent advances and innovations overall costs (Kumar et al., 2021). Moreover, improvements in storage
technology, including the development of temperature-stable
Targeted genome editing, particularly CRISPR/Cas9 technology, formulations and vacuum packaging techniques, have significantly
has revolutionized plant pathology by enabling precise genetic extended the shelf life of Bacillus products (Gotor-Vila et al., 2019).
modifications to enhance disease resistance in crops. This technology These innovations not only ensure the long-term viability of biocontrol
is preferred for its simplicity, cost-effectiveness, and adaptability, agents but also enhance their accessibility on a global scale, particularly
offering a promising approach for the development of pest- and in regions with challenging storage and transportation conditions.
disease-resistant plants (Das et al., 2023; Yin et al., 2024). These
genetic modifications often aim to increase the production of
antimicrobial compounds, such as lipopeptides, enzymes, and VOCs, Conclusion
which are crucial for suppressing various plant pathogens (Rocha and
Duggal, 2023; Maqsood et al., 2024). Additionally, genetic engineering Bacillus spp. have emerged as potent biocontrol agents against
has facilitated the introduction of novel traits, such as enhanced root PPNs, offering a promising and sustainable alternative to traditional
colonization and rhizosphere persistence, ensuring that engineered chemical treatments. Their effectiveness is attributed to their
Bacillus strains are more effective and resilient under diverse multifaceted mechanisms, including the production of nematicidal
environmental conditions (Ramírez-Pool et al., 2024). A recent review compounds, enhancement of plant resistance, and improvement of
by Khan et al. (2023) highlighted that advanced molecular strategies, soil health. Thus, they play invaluable roles in IPM strategies. Recent

Frontiers in Microbiology 22 frontiersin.org

Vasantha-Srinivasan et al. 10.3389/fmicb.2024.1510036

advances in genetic engineering and formulation technologies have supported by the Korea Institute of Planning and Evaluation for
significantly bolstered the efficacy and reliability of Bacillus strains for Technology in Food, Agriculture and Forestry (IPET) through the
agricultural applications. However, various challenges, such as Agricultural Machinery/Equipment Localization Technology
environmental variability, regulatory hurdles, and the need for Development Program funded by the Ministry of Agriculture, Food
optimized application methods, persist. Overcoming these challenges and Rural Affairs (MAFRA) (No. 122020–3) and the Basic Science
is essential for maximizing the efficacy of Bacillus spp. in sustainable Research Program through the National Research Foundation of
nematode management and ensuring global food security. Korea (NRF) funded by the Ministry of Science, ICT and Future
Planning (Grant No. 2022R1A2C1013108).

Author contributions
Conflict of interest
PV-S: Conceptualization, Investigation, Methodology, Writing –
original draft, Writing – review & editing. KP: Formal analysis, KP was the CEO of Invirustech Co., Inc.
Investigation, Writing – review & editing. KK: Conceptualization, The remaining authors declare that the research was conducted in
Formal analysis, Investigation, Writing – review & editing. W-JJ: the absence of any commercial or financial relationships that could be
Conceptualization, Investigation, Project administration, Resources, construed as a potential conflict of interest.
Supervision, Writing – review & editing. YH: Funding acquisition,
Investigation, Project administration, Resources, Writing – review &
editing. Publisher’s note
All claims expressed in this article are solely those of the authors
Funding and do not necessarily represent those of their affiliated organizations,
or those of the publisher, the editors and the reviewers. Any product
The author(s) declare that financial support was received for the that may be evaluated in this article, or claim that may be made by its
research, authorship, and/or publication of this article. This work was manufacturer, is not guaranteed or endorsed by the publisher.

References
Aballay, E., Prodan, S., Correa, P., and Allende, J. (2020). Assessment of rhizobacterial (Rhabditida: Meloidogynidae) and promote the growth of tomato plants. Rhizosphere
consortia to manage plant parasitic nematodes of grapevine. Crop Prot. 131:105103. doi: 31:100935. doi: 10.1016/j.rhisph.2024.100935
10.1016/j.cropro.2020.105103
Antil, S., Kumar, R., Pathak, D. V., Kumar, A., Panwar, A., and Kumari, A. (2022a).
Abd-Elgawad, M. M. (2024). Upgrading strategies for managing nematode pests on Plant growth-promoting rhizobacteria-Bacillus cereus KMT-5 and B. megaterium
profitable crops. Plan. Theory 13:1558. doi: 10.3390/plants13111558 KMT-8 effectively suppressed Meloidogyne javanica infection. Appl. Soil Ecol.
174:104419. doi: 10.1016/j.apsoil.2022.104419
Abd-Elgawad, M. M., and Askary, T. H. (2018). Fungal and bacterial nematicides in
integrated nematode management strategies. Egypt. J. Biol. Pest Control 28, 1–24. doi: Antil, S., Kumar, R., Pathak, D. V., Kumar, A., Panwar, A., Kumari, A., et al. (2021).
10.1186/s41938-018-0080-x On the potential of Bacillus aryabhattai KMT-4 against Meloidogyne javanica. Egypt. J.
Abd-Elgawad, M. M. M., and Askary, T. H. (2020). Factors affecting success of Biol. Pest Control 31, 1–9. doi: 10.1186/s41938-021-00417-2
biological agents used in controlling the plant-parasitic nematodes. Egypt. J. Biol. Pest Antil, S., Kumar, R., Pathak, D. V., Kumar, A., Panwar, A., Kumari, A., et al. (2022b).
Control 30:17. doi: 10.1186/s41938-020-00215-2 Potential of Bacillus altitudinis KMS-6 as a biocontrol agent of Meloidogyne javanica. J.
Abdellatif, A. A., Tahany, A. R., Sayed, M. A., Dina, I., and Elmaghraby, M. M. K. Pest. Sci. 95, 1443–1452. doi: 10.1007/s10340-021-01469-x
(2021). Activity of Serratia spp. and Bacillus spp. as biocontrol agents against Asaturova, A. M., Bugaeva, L. N., Homyak, A. I., Slobodyanyuk, G. A., Kashutina, E. V.,
Meloidogyne incognita infecting tomato. Pakist. J. Biotechnol. 18, 37–47. doi: 10.34016/ Yasyuk, L. V., et al. (2022). Bacillus velezensis strains for protecting cucumber plants
pjbt.2021.18.2/3.37 from root-knot nematode Meloidogyne incognita in a greenhouse. Plan. Theory 11:275.
Abdel-Salam, M. S., Ameen, H. H., Soliman, G. M., Elkelany, U. S., and Asar, A. M. doi: 10.3390/plants11030275
(2018). Improving the nematicidal potential of Bacillus amyloliquefaciens and Asif, K., Shabaan, M., Mahmood, W., Asghar, H. N., Zahir, Z. A., Zulfiqar, U., et al.
Lysinibacillus sphaericus against the root-knot nematode Meloidogyne incognita using (2024). Synergistic application of bacterial consortium and organic amendments
protoplast fusion technique. Egypt. J. Biol. Pest Control 28, 1–6. doi: 10.1186/ improves the growth and seed quality of mash bean (Vigna Mungo L.). Soil Sci. Plant
s41938-018-0034-3 Nutr. 24, 6893–6905. doi: 10.1007/s42729-024-02012-4
Adam, M., Heuer, H., and Hallmann, J. (2014). Bacterial antagonists of fungal Ayaz, M., Ali, Q., Farzand, A., Khan, A. R., Ling, H., and Gao, X. (2021). Nematicidal
pathogens also control root-knot nematodes by induced systemic resistance of tomato volatiles from Bacillus atrophaeus GBSC56 promote growth and stimulate induced
plants. PLoS One 9:e90402. doi: 10.1371/journal.pone.0090402 systemic resistance in tomato against Meloidogyne incognita. Int. J. Mol. Sci. 22:5049. doi:
Adiwena, M., Murtilaksono, A., Egra, S., Hoesain, M., Asyiah, I. N., Pradana, A. P., 10.3390/ijms22095049
et al. (2023). The effects of micronutrient-enriched media on the efficacy of Bacillus Ayaz, M., Li, C. H., Ali, Q., Zhao, W., Chi, Y. K., Shafiq, M., et al. (2023). Bacterial and
subtilis as biological control agent against Meloidogyne incognita. Biodiv. J. Biol. Divers. fungal biocontrol agents for plant disease protection: journey from lab to field, current
24, 33–39. doi: 10.13057/biodiv/d240105 status, challenges, and global perspectives. Molecules 28:6735. doi: 10.3390/
Ahmad, G., Khan, A., Khan, A. A., Ali, A., and Mohhamad, H. I. (2021). Biological molecules28186735
control: a novel strategy for the control of the plant parasitic nematodes. Antonie Van
Bacon, C. W., Hinton, D. M., and Hinton, A. Jr. (2006). Growth-inhibiting effects of
Leeuwenhoek 114, 885–912. doi: 10.1007/s10482-021-01577-9
concentrations of fusaric acid on the growth of Bacillus mojavensis and other biocontrol
Ahmed, S., Liu, Q., and Jian, H. (2019). Bacillus cereus a potential strain infested cereal Bacillus species. J. Appl. Microbiol. 100, 185–194. doi: 10.1111/j.1365-2672.2005.02770.x
cyst nematode (Heterodera avenae). Pak. J. Nematol. 37, 53–61. doi: 10.18681/pjn.v37.
Banihashemian, S. N., Jamali, S., Golmohammadi, M., and Ghasemnezhad, M.
i01.p53-61
(2023). Management of root-knot nematode in kiwifruit using resistance-inducing
Ali, Q., Yu, C., Wang, Y., Sheng, T., Zhao, X., Wu, X., et al. (2023). High killing rate of Bacillus altitudinis. Trop. Plant Pathol. 48, 443–451. doi: 10.1007/s40858-023-00573-w
nematode and promotion of rice growth by synthetic volatiles from Bacillus strains due
Baptista, J. P., Teixeira, G. M., Jesus, M. L. A., Bertê, R., Higashi, A., Mosella, M., et al.
to enhanced oxidative stress response. Physiol. Plant. 175:e13868. doi: 10.1111/ppl.13868
(2022). Antifungal activity and genomic characterization of the isolate Bacillus velezensis
Amorim, D. J., Tsujimoto, T. F., Baldo, F. B., Leite, L. G., Harakava, R., Wilcken, S. R. CMRP 4489, a biocontrol agent for plant-pathogenic fungi. Res. Sq. doi: 10.21203/
S., et al. (2024). Bacillus, Pseudomonas and Serratia control Meloidogyne incognita rs.3.rs-1619465/v1

Frontiers in Microbiology 23 frontiersin.org

Vasantha-Srinivasan et al. 10.3389/fmicb.2024.1510036

Barnawal, D., Bharti, N., Pandey, S. S., Pandey, A., Chanotiya, C. S., and Kalra, A. Cetintas, R., Kusek, M., and Fateh, S. A. (2018). Effect of some plant growth-
(2017). Plant growth-promoting rhizobacteria enhance wheat salt and drought stress promoting rhizobacteria strains on root-knot nematode, Meloidogyne incognita, on
tolerance by altering endogenous phytohormone levels and TaCTR1/TaDREB2 tomatoes. Egypt. J. Biol. Pest Control 28, 1–5. doi: 10.1186/s41938-017-0008-x
expression. Physiol. Plant. 161, 502–514. doi: 10.1111/ppl.12614
Chavarria-Quicaño, E., Contreras-Jácquez, V., Carrillo-Fasio, A., De la
Basiouny, A. G., and Abo-Zaid, G. A. (2018). Biocontrol of the root-knot nematode, Torre-González, F., and Asaff-Torres, A. (2023a). Native Bacillus paralicheniformis isolate
Meloidogyne incognita, using an eco-friendly formulation from Bacillus subtilis, lab as a potential agent for phytopathogenic nematodes control. Front. Microbiol.
and greenhouse studies. Egypt. J. Biol. Pest Control 28:87. doi: 10.1186/ 14:1213306. doi: 10.3389/fmicb.2023.1213306
s41938-018-0094-4
Chavarria-Quicaño, E., De la Torre-González, F., González-Riojas, M.,
Bavaresco, L. G., Guaberto, L. M., and Araujo, F. F. (2021). Interaction of Bacillus Rodríguez-González, J., and Asaff-Torres, A. (2023b). Nematicidal lipopeptides from
subtilis with resistant and susceptible tomato (Solanum lycopersicum L.) in the control Bacillus paralicheniformis and Bacillus subtilis: a comparative study. Appl. Microbiol.
of Meloidogyne incognita. Arch. Phytopathol. Plant Protect. 54, 359–374. doi: Biotechnol. 107, 1537–1549. doi: 10.1007/s00253-023-12391-w
10.1080/03235408.2020.1833279
Chen, J., Abawi, G. S., and Zuckerman, B. M. (2000). Efficacy of Bacillus thuringiensis,
Behl, K., Jaiswal, P., and Pabbi, S. (2024). Recent advances in microbial and nano- Paecilomyces marquandii, and Streptomyces costaricanus with and without organic
formulations for effective delivery and agriculture sustainability. Biocatal. Agric. amendments against Meloidogyne hapla infecting lettuce. J. Nematol. 32, 70–77.
Biotechnol. 58:103180. doi: 10.1016/j.bcab.2024.103180 Available at: https://pubmed.ncbi.nlm.nih.gov/19270951/
Berlitz, D. L., Knaak, N., Cassal, M. C., and Fiuza, L. M. (2014). “Bacillus and Chen, L., Wang, Y., Zhu, L., Min, Y., Tian, Y., Gong, Y., et al. (2024). 3-(Methylthio)
biopesticides in control of phytonematodes” in Basic and applied aspects of biopesticides. propionic acid from Bacillus thuringiensis Berliner exhibits high Nematicidal activity
ed. K. Sahayaraj (New Delhi: Springer). against the root knot nematode Meloidogyne incognita (Kofoid and white) Chitwood.
Int. J. Mol. Sci. 25:1708. doi: 10.3390/ijms25031708
Bhat, A. A., Shakeel, A., Waqar, S., Handoo, Z. A., and Khan, A. A. (2023). Microbes
vs. nematodes: insights into biocontrol through antagonistic organisms to control root- Chernov, T. I., and Semenov, M. V. (2021). Management of soil microbial communities:
knot nematodes. Plan. Theory 12:451. doi: 10.3390/plants12030451 opportunities and prospects (a review). Eurasian Soil Sci. 54, 1888–1902. doi: 10.1134/
S1064229321120024
Blouin, M. S., Yowell, C. A., Courtney, C. H., and Dame, J. B. (1998). Substitution bias,
rapid saturation, and the use of mtDNA for nematode systematics. Mol. Biol. Evol. 15, Chien, Y. C., and Huang, C. H. (2020). Biocontrol of bacterial spot on tomato by foliar
1719–1727. doi: 10.1093/oxfordjournals.molbev.a025898 spray and growth medium application of Bacillus amyloliquefaciens and Trichoderma
asperellum. Eur. J. Plant Pathol. 156, 995–1003. doi: 10.1007/s10658-020-01947-5
Bo, T., Kong, C., Zou, S., Mo, M., and Liu, Y. (2022). Bacillus nematocida B16 enhanced
the rhizosphere colonization of Pochonia chlamydosporia ZK7 and controlled the Chinheya, C. C., Yobo, K. S., and Laing, M. D. (2017). Biological control of the
efficacy of the root-knot nematode Meloidogyne incognita. Microorganisms 10:218. doi: rootknot nematode, Meloidogyne javanica (Chitwood) using Bacillus isolates, on
10.3390/microorganisms10020218 soybean. Biol. Control 109, 37–41. doi: 10.1016/j.biocontrol.2017.03.009
Borriss, R., Wu, H., and Gao, X. (2019). “Secondary metabolites of the plant growth Cho, W. I., and Chung, M. S. (2020). Bacillus spores: A review of their properties and
promoting model rhizobacterium Bacillus velezensis FZB42 are involved in direct inactivation processing technologies. Food Sci. Biotechnol. 29, 1447–1461. doi: 10.1007/
suppression of plant pathogens and in stimulation of plant-induced systemic resistance” s10068-020-00809-4
in Secondary metabolites of plant growth promoting rhizomicroorganisms: discovery Choi, T. G., Maung, C. E. H., Lee, D. R., Henry, A. B., Lee, Y. S., and Kim, K. Y. (2020).
and applications. eds. H. Singh, C. Keswani, M. Reddy, E. Sansinenea and C. García- Role of bacterial antagonists of fungal pathogens, Bacillus thuringiensis KYC and Bacillus
Estrada. 147–168. velezensis CE 100 in control of root-knot neatode, Meloidogyne incognita and subsequent
Bravo, A., Gill, S. S., and Soberón, M. (2007). Mode of action of Bacillus thuringiensis growth promotion of tomato. Biocontrol Sci. Tech. 30, 685–700. doi:
cry and Cyt toxins and their potential for insect control. Toxicon 49, 423–435. doi: 10.1080/09583157.2020.1765980
10.1016/j.toxicon.2006.11.022 Choudhary, D. K., and Johri, B. N. (2009). Interactions of Bacillus spp. and plants–with
Brzezinska, M. S., Kalwasińska, A., Świątczak, J., Żero, K., and Jankiewicz, U. (2020). special reference to induced systemic resistance (ISR). Microbiol. Res. 164, 493–513. doi:
Exploring the properties of chitinolytic Bacillus isolates for the pathogens biological 10.1016/j.micres.2008.08.007
control. Microb. Pathog. 148:104462. doi: 10.1016/j.micpath.2020.104462 Chowdhury, S. P., Hartmann, A., Gao, X., and Borriss, R. (2015). Biocontrol
Bui, H. X., Hadi, B. A., Oliva, R., and Schroeder, N. E. (2020). Beneficial bacterial mechanism by root-associated Bacillus amyloliquefaciens FZB42–a review. Front.
volatile compounds for the control of root-knot nematode and bacterial leaf blight on Microbiol. 6:780. doi: 10.3389/fmicb.2015.00780
rice. Crop Prot. 135:104792. doi: 10.1016/j.cropro.2019.04.016 Cruz‐Magalhães, V., Guimarães, R. A., Da Silva, J. C., de Faria, A. F., Pedroso, M. P.,
Butu, M., Rodino, S., and Butu, A. (2022). Biopesticide formulations-current Campos, V. P., et al. (2022). The combination of two Bacillus strains suppresses
challenges and future perspectives. Biopesticides 2, 19–29. doi: 10.1016/ Meloidogyne incognita and fungal pathogens, but does not enhance plant growth. Pest
B978-0-12-823355-9.00010-9 Manag. Sci. 78, 722–732. doi: 10.1002/ps.6685

Calvo, P., Ormeño-Orrillo, E., Martínez-Romero, E., and Zúñiga, D. (2010). Dai, M. M., Liu, R., Jiang, H., Zhang, X. P., Song, W. W., Zhang, J., et al. (2023).
Characterization of Bacillus isolates of potato rhizosphere from Andean soils of Peru Volatile organic compounds of Bacillus pumilus strain S1-10 exhibit fumigant activity
and their potential PGPR characteristics. Braz. J. Microbiol. 41, 899–906. doi: 10.1590/ against Meloidogyne incognita. Plant Dis. 107, 3057–3063. doi: 10.1094/
S1517-83822010000400008 PDIS-10-22-2391-RE

Camacho, M., de Los Santos, B., Vela, M. D., and Talavera, M. (2023). Use of Danilova, I. V., Vasileva, I. A., Gilmutdinova, A. I., Dyadkina, I. V., Khusnullina, L. K.,
bacteria isolated from berry rhizospheres as biocontrol agents for charcoal rot and Khasanov, D. I., et al. (2023). Characterization of Bacillus pumilus strains with targeted
root-knot nematode strawberry diseases. Horticulturae 9:346. doi: 10.3390/ gene editing for antimicrobial peptides and sporulation factor. Microorganisms 11:1508.
horticulturae9030346 doi: 10.3390/microorganisms11061508

Camatti, G., dos Santos, F. M., Júnior, G. L. D. S. R., Camargo, D. P., Manfio, G. S., Das, K., Ayim, B. Y., Borodynko-Filas, N., Das, S. C., and Aminuzzaman, F. M. (2023).
Santos, J. R. P., et al. (2023). Bacillus-and Trichoderma-based products control the spiral Genome editing (CRISPR/Cas9) in plant disease management: challenges and future
nematode Helicotylenchus dihystera in soybean. Rhizosphere 27:100717. doi: 10.1016/j. prospects. J. Plant Protect. Res. 63, 159–172. doi: 10.24425/jppr.2023.145761
rhisph.2023.100717 Das, S., Wadud, M. A., and Khokon, M. A. R. (2021). Functional evaluation of culture
filtrates of Bacillus subtilis and Pseudomonas fluorescens on the mortality and hatching
Carmona-Hernandez, S., Reyes-Pérez, J. J., Chiquito-Contreras, R. G.,
of Meloidogyne javanica. Saudi J. Biol. Sci. 28, 1318–1323. doi: 10.1016/j.sjbs.2020.11.055
Rincon-Enriquez, G., Cerdan-Cabrera, C. R., and Hernandez-Montiel, L. G. (2019).
Biocontrol of postharvest fruit fungal diseases by bacterial antagonists: a review. Daulagala, P. W. H. K. P. (2021). Chitinolytic endophytic bacteria as biocontrol agents
Agronomy 9:121. doi: 10.3390/agronomy9030121 for phytopathogenic fungi and nematode pests: a review. Asian J. Res. Bot. 5, 14–24.
Carriel, C. B., and Soto, D. V. (2022). Persistence of Bacillus thuringiensis and de Paula, L. L., Campos, V. P., Terra, W. C., de Brum, D., Jacobs, D. C., Bui, H. X., et al.
Bacillus pumilus potential biological control agents of the coffee berry borer under (2024). The combination of Bacillus amyloliquefaciens and Purpureocillium lilacinum in
field conditions of Puerto Rico. Sci. Agric. 19, 43–56. doi: 10.19053/01228420.v19. the control of Meloidogyne enterolobii. Biol. Control 189:105438. doi: 10.1016/j.
n3.2022.14685 biocontrol.2023.105438
Castillo, H. F., Reyes, C. F., Morales, G. G., Herrera, R. R., and Aguilar, C. (2013). d'Errico, G., Marra, R., Crescenzi, A., Davino, S. W., Fanigliulo, A., Woo, S. L., et al.
“Biological control of root pathogens by plant growth promoting Bacillus spp” in Weed (2019). Integrated management strategies of Meloidogyne incognita and
and pest control - conventional and new challenges. eds. S. Soloneski and M. L. Pseudopyrenochaeta lycopersici on tomato using a Bacillus firmus-based product and two
Larramendy (Rijeka, Croatia: InTech), 79–103. synthetic nematicides in two consecutive crop cycles in greenhouse. Crop Prot. 122,
159–164. doi: 10.1016/j.cropro.2019.05.004
Cavalcanti, V. P., Terra, W. C., de Souza, J. T., Pacheco, P. V. M., de Sousa, L. F.,
Belizario, R. A., et al. (2024). A commercial formulation of Bacillus subtilis induces Devindrappa, M., Kamra, A., Singh, D., Gawade, B., and Sirohi, A. (2023). Plant
metabolomic changes in root exudates that invert the chemotactic responses of the growth promoting Bacillus species elicit defense against Meloidogyne incognita infecting
nematode Meloidogyne incognita to host and non-host plants. J. Plant Dis. Protect. 131, tomato in polyhouse. J. Basic Microbiol. 2023, 1–9. doi: 10.22541/
899–909. doi: 10.1007/s41348-024-00892-3 au.168001566.62776546/v1

Frontiers in Microbiology 24 frontiersin.org

Vasantha-Srinivasan et al. 10.3389/fmicb.2024.1510036

Díaz-Manzano, F. E., Amora, D. X., Martínez-Gómez, Á., Moelbak, L., and Escobar, C. and delay Cry5Ba-based nematode resistance. Appl. Environ. Microbiol. 83, e03505–
(2023). Biocontrol of Meloidogyne spp. in Solanum lycopersicum using a dual e03516. doi: 10.1128/AEM.03505-16
combination of Bacillus strains. Front. Plant Sci. 13:1077062. doi: 10.3389/
Ghahremani, Z., Escudero, N., Beltrán-Anadón, D., Saus, E., Cunquero, M., Andilla, J.,
fpls.2022.1077062
et al. (2020). Bacillus firmus strain I-1582, a nematode antagonist by itself and through
Diyapoglu, A., Oner, M., and Meng, M. (2022). Application potential of bacterial the plant. Front. Plant Sci. 11:796. doi: 10.3389/fpls.2020.00796
volatile organic compounds in the control of root-knot nematodes. Molecules 27:4355.
Gill, S. S., Cowles, E. A., and Pietrantonio, P. V. (1992). The mode of action of Bacillus
doi: 10.3390/molecules27144355
thuringiensis endotoxins. Annu. Rev. Entomol. 37, 615–634. doi: 10.1146/annurev.
Dobrzyński, J., Jakubowska, Z., Kulkova, I., Kowalczyk, P., and Kramkowski, K. (2023). en.37.010192.003151
Biocontrol of fungal phytopathogens by Bacillus pumilus. Front. Microbiol. 14:1194606.
Gomaa, E. Z. (2021). Microbial chitinases: properties, enhancement and potential
doi: 10.3389/fmicb.2023.1194606
applications. Protoplasma 258, 695–710. doi: 10.1007/s00709-021-01612-6
Du, J., Gao, Q., Ji, C., Song, X., Liu, Y., Li, H., et al. (2022). Bacillus licheniformis JF-22
Gotor-Vila, A., Usall, J., Torres, R., Solsona, C., and Teixidó, N. (2019). Enhanced
to control Meloidogyne incognita and its effect on tomato rhizosphere microbial
shelf-life of the formulated biocontrol agent Bacillus amyloliquefaciens CPA-8 combining
community. Front. Microbiol. 13:863341. doi: 10.3389/fmicb.2022.863341
diverse packaging strategies and storage conditions. Int. J. Food Microbiol. 290, 205–213.
Efthimiadou, A., Katsenios, N., Chanioti, S., Giannoglou, M., Djordjevic, N., and doi: 10.1016/j.ijfoodmicro.2018.10.013
Katsaros, G. (2020). Effect of foliar and soil application of plant growth promoting
Grage, K., McDermott, P., and Rehm, B. H. (2017). Engineering Bacillus megaterium
bacteria on growth, physiology, yield and seed quality of maize under Mediterranean
for production of functional intracellular materials. Microb. Cell Factories 16, 211–212.
conditions. Sci. Rep. 10:21060. doi: 10.1038/s41598-020-78034-6
doi: 10.1186/s12934-017-0823-5
El Aimani, A., Houari, A., Laasli, S. E., Mentag, R., Iraqi, D., Diria, G., et al. (2022).
Antagonistic potential of Moroccan entomopathogenic nematodes against root-knot Griffitts, J. S., Whitacre, J. L., Stevens, D. E., and Aroian, R. V. (2005). Bt toxin
nematodes, Meloidogyne javanica on tomato under greenhouse conditions. Sci. Rep. resistance from loss of a putative carbohydrate-modifying enzyme. Science 293, 860–864.
12:2915. doi: 10.1038/s41598-022-07039-0 doi: 10.1126/science.1062441

Elango, K., Sobhana, E., Sujithra, P., Bharath, D., and Ahuja, A. (2020). Traditional Grubišić, D., Uroić, G., Ivošević, A., and Grdiša, M. (2018). Nematode control by the
agricultural practices as a tool for management of insects and nematode pests of crops: use of antagonistic plants. Agric. Conspec. Sci. 83, 269–275.
an overview. J. Entomol. Zool. Stud. 8, 237–245. Available at: https://hrcak.srce.hr/207925

El-Saadony, M. T., Abuljadayel, D. A., Shafi, M. E., Albaqami, N. M., Desoky, E. S. M., Guo, S., Liu, M., Peng, D., Ji, S., Wang, P., Yu, Z., et al. (2008). New strategy for
El-Tahan, A. M., et al. (2021). Control of foliar phytoparasitic nematodes through isolating novel nematicidal crystal protein genes from Bacillus thuringiensis strain
sustainable natural materials: current progress and challenges. Saudi J. Biol. Sci. 28, YBT-1518. Appl. Environ. Microbiol. 74, 6997–7001. doi: 10.1128/AEM.01346-08
7314–7326. doi: 10.1016/j.sjbs.2021.08.035 Guo, Y., Weng, M., Sun, Y., Carballar-Lejarazú, R., Wu, S., and Lian, C. (2022). Bacillus
El-Sawy, S., El-Nagdi, W., Mohamed, S., Khalil, B., and Soliman, G. (2023). The thuringiensis toxins with nematocidal activity against the pinewood nematode
efficiency of biofertilizer and bio-control on root-knot nematode, using bacterial strains, Bursaphelenchus xylophilus. J. Invertebr. Pathol. 189:107726. doi: 10.1016/j.
and its effect on tomato plant protein patterns, and improving yield under field jip.2022.107726
conditions. Res. Sq., 2–37. doi: 10.21203/rs.3.rs-3475183/v1 Gupta, R., Mfarrej, M., Elnour, R., Hashem, M., and Ahmad, F. (2023). Defence
Engelbrecht, G., Claassens, S., Mienie, C. M., and Fourie, H. (2022). Filtrates of mixed response of host plants for cyst nematode: a review on parasitism and defence. Science
Bacillus spp inhibit second-stage juvenile motility of root-knot nematodes. Rhizosphere 35:102829:102829. doi: 10.1016/j.jksus.2023.102829
22:100528. doi: 10.1016/j.rhisph.2022.100528 Gurikar, C., Gowda, N. N., Hanumantharaju, K. N., and Netravati, B. P. (2022). “Role
Engelbrecht, G., van Rensburg, P. J. J., Fourie, H., and Claassens, S. (2020). In vitro of Bacillus species in soil fertility with reference to rhizosphere engineering” in
bioassays to determine the effect of Bacillus soli filtrates on the paralysis of Meloidogyne Rhizosphere engineering (Amsterdam, Netherlands: Elsevier), 65–76.
incognita second-stage juveniles. Nematology 22, 239–243. doi: 10.1163/15685411-00003345 Habazar, T., Yanti, Y., Dani, M. R., and Monica, D. (2021). “Biocontrol of Meloidogyne
Esitken, A. H. M. E. T., Karlidag, H. Ü. S. E. Y. İ. N., Ercisli, S. E. Z. A. İ., and Sahin, F. İ. sp. on tomato plants by selected Bacillus spp” in IOP Conference Series: Earth and
K. R. E. T. T. İ. N. (2002). Effects of foliar application of Bacillus subtilis Osu-142 on the Environmental Science (Bristol, United Kingdom: IOP Publishing). 757:012019.
yield, growth and control of shot-hole disease (Coryneum blight) of apricot. Hamze, R., and Ruiu, L. (2022). Brevibacillus laterosporus as a natural biological
Gartenbauwissenschaft 67, 139–142. control agent of soil-dwelling nematodes. Agronomy 12:2686. doi: 10.3390/
Etesami, H., Jeong, B. R., and Glick, B. R. (2023). Biocontrol of plant diseases by agronomy12112686
Bacillus Spp. Physiol. Mol. Plant Pathol. 126:102048. doi: 10.1016/j.pmpp.2023.102048 Hartz, P., Gehl, M., König, L., Bernhardt, R., and Hannemann, F. (2021). Development
Fabiyi, O. A. (2024). “Application of Bacillus species in the Management of and application of a highly efficient CRISPR-Cas9 system for genome engineering in
Meloidogyne incognita” in Sustainable Management of Nematodes in agriculture, role of Bacillus megaterium. J. Biotechnol. 329, 170–179. doi: 10.1016/j.jbiotec.2021.02.006
microbes-assisted strategies, vol. 19 (Cham: Springer International Publishing), Hayat, H. S., Rehman, A. U., Farooq, S., Naveed, M., Ali, H. M., and Hussain, M.
249–264. (2023). Boron seed coating combined with seed inoculation with boron tolerant bacteria
Fallahzadeh-Mamaghani, V., Shahbazi-Ezmareh, R., Shirzad, A., and Moslehi, S. (Bacillus sp. MN-54) and maize stalk biochar improved growth and productivity of
(2023). Possible mechanisms of action of Bacillus wiedmannii AzBw1, a biocontrol agent maize (Zea mays L.) on saline soil. Heliyon 9:e22075. doi: 10.1016/j.heliyon.2023.e22075
of the root-knot nematode, Meloidogyne arenaria. Egypt. J. Biol. Pest Control 33:28. doi: He, Y., Wang, R., Zhao, H., Ren, Y., Agarwal, M., Zheng, D., et al. (2022). Predicting
10.1186/s41938-023-00668-1 potential global distribution and risk regions for potato cyst nematodes (Globodera
Forghani, F., and Hajihassani, A. (2020). Recent advances in the development of rostochiensis and Globodera pallida). Sci. Rep. 12:21843. doi: 10.1038/s41598-022-26443-0
environmentally benign treatments to control root-knot nematodes. Front. Plant Sci. Heerklotz, H., and Seelig, J. (2007). Leakage and lysis of lipid membranes induced by
11:1125. doi: 10.3389/fpls.2020.01125 the lipopeptide surfactin. Eur. Biophys. J. 36, 305–314. doi: 10.1007/s00249-006-0091-5
Fu, H. Z., Marian, M., Enomoto, T., Hieno, A., Ina, H., Suga, H., et al. (2020). Biocontrol Henry, G., Deleu, M., Jourdan, E., Thonart, P., and Ongena, M. (2011). The bacterial
of tomato bacterial wilt by foliar spray application of a novel strain of endophytic Bacillus lipopeptide surfactin targets the lipid fraction of the plant plasma membrane to trigger
sp. Microbes Environ. 35:p.ME20078. doi: 10.1264/jsme2.ME20078 immune-related responses. Cell. Microbiol. 13, 1824–1837. doi:
Galbieri, R., Oliveira, J. A. D., Negri, B. F., Boldt, A. S., Rizzi, U. D. S., and Belot, J. L. 10.1111/j.1462-5822.2011.01664.x
(2023). Bacillus subtilis as growth-promoting rhizobacteria co-inoculated on Hezakiel, H. E., Thampi, M., Rebello, S., and Sheikhmoideen, J. M. (2024).
Bradyrhizobium-treated soybean seeds in the planting furrow. Rev. Ceres 70:e70601. doi: Biopesticides: a green approach towards agricultural pests. Appl. Biochem. Biotechnol.
10.1590/0034-737X202370060001 196, 5533–5562. doi: 10.1007/s12010-023-04765-7
Gamalero, E., and Glick, B. R. (2020). The use of plant growth-promoting bacteria to Hossain, M. A., Hossain, M. S., and Akter, M. (2023). Challenges faced by plant
prevent nematode damage to plants. Biology 9:381. doi: 10.3390/biology9110381 growth-promoting bacteria in field-level applications and suggestions to overcome the
Gao, A., Zheng, L., Wang, S., Pan, H., and Zhang, H. (2024). Preparation of barriers. Physiol. Mol. Plant Pathol. 126:102029. doi: 10.1016/j.pmpp.2023.102029
microcapsules and evaluation of their biocontrol efficacy. J. Biosci. Bioeng. 138, 328–337.
Hsiao, C. Y., Blanco, S. D., Peng, A. L., Fu, J. Y., Chen, B. W., Luo, M. C., et al. (2023).
doi: 10.1016/j.jbiosc.2024.05.007
Seed treatment with calcium carbonate containing Bacillus amyloliquefaciens PMB05
Gassmann, A. J., Stock, S. P., Sisterson, M. S., Carrière, Y., and Tabashnik, B. E. (2008). powder is an efficient way to control black rot disease of cabbage. Agriculture 13:926.
Synergism between entomopathogenic nematodes and Bacillus thuringiensis crops: doi: 10.3390/agriculture13050926
integrating biological control and resistance management. J. Appl. Ecol. 45, 957–966. doi:
Hu, H. J., Chen, Y. L., Wang, Y. F., Tang, Y. Y., Chen, S. L., and Yan, S. Z. (2017).
10.1111/j.1365-2664.2008.01457.x
Endophytic Bacillus cereus effectively controls Meloidogyne incognita on tomato plants
Gattoni, K. M., Park, S. W., and Lawrence, K. S. (2022). Evaluation of the mechanism through rapid rhizosphere occupation and repellent action. Plant Dis. 101, 448–455. doi:
of action of bacillus spp. to manage meloidogyne incognita with split root assay, RT-qPCR 10.1094/PDIS-06-16-0871-RE
and qPCR. Front. Plant Sci. 13:1079109. doi: 10.3389/fpls.2022.1079109
Hu, H., Gao, Y., Li, X., Chen, S., Yan, S., and Tian, X. (2020). Identification and
Geng, C., Liu, Y., Li, M., Tang, Z., Muhammad, S., Zheng, J., et al. (2017). Dissimilar nematicidal characterization of proteases secreted by endophytic bacteria Bacillus cereus
crystal proteins Cry5Ca1 and Cry5Da1 synergistically act against Meloidogyne incognita BCM2. Phytopathology 110, 336–344. doi: 10.1094/PHYTO-05-19-0164-R

Frontiers in Microbiology 25 frontiersin.org

Vasantha-Srinivasan et al. 10.3389/fmicb.2024.1510036

Hu, L. B., Shi, Z. Q., Zhang, T., and Yang, Z. M. (2007). Fengycin antibiotics Khan, A. R., Mustafa, A., Hyder, S., Valipour, M., Rizvi, Z. F., Gondal, A. S., et al.
isolated from B-FS01 culture inhibit the growth of fusarium moniliforme Sheldon (2022). Bacillus spp. as bioagents: uses and application for sustainable agriculture.
ATCC 38932. FEMS Microbiol. Lett. 272, 91–98. doi: 10.1111/j.1574-6968.2007. Biology 11:1763. doi: 10.3390/biology11121763
00743.x
Khanh, T. L. V. (2020). Selection of Bacillus thuringiensis against pathogenic nematodes
Hu, Y., You, J., Wang, Y., Long, Y., Wang, S., Pan, F., et al. (2022). Biocontrol efficacy attacking pepper tree. Biotechnology 36, 57–62. doi: 10.21519/0234-2758-2020-36-3-57-62
of Bacillus velezensis strain YS-AT-DS1 against the root-knot nematode Meloidogyne
Khullar, G., Karami, Z., and Prakitchaiwattana, C. (2024). Development of
incognita in tomato plants. Front. Microbiol. 13:1035748. doi: 10.3389/
microencapsulated dried Bacillus sp. 63‐11 with enhanced shelf stability and bioactivity for
fmicb.2022.1035748
use as a food supplement. Int. J. Food Sci. Technol. 59, 1291–1298. doi: 10.1111/ijfs.16853
Huang, M., Bulut, A., Shrestha, B., Matera, C., Grundler, F. M., and Schleker, A. S. S.
Kloepper, J. W., Ryu, C. M., and Zhang, S. (2004). Induced systemic resistance and
(2021). Bacillus firmus I-1582 promotes plant growth and impairs infection and
promotion of plant growth by Bacillus spp. Phytopathology 94, 1259–1266. doi: 10.1094/
development of the cyst nematode Heterodera schachtii over two generations. Sci. Rep.
PHYTO.2004.94.11.1259
11:14114. doi: 10.1038/s41598-021-93567-0
Köhl, J., Kolnaar, R., and Ravensberg, W. J. (2019). Mode of action of microbial
Huang, X. W., Niu, Q. H., Zhou, W., and Zhang, K. Q. (2005). Bacillus nematocida
biological control agents against plant diseases: relevance beyond efficacy. Front. Plant
sp. nov., a novel bacterial strain with nematotoxic activity isolated from soil in
Sci. 10:845. doi: 10.3389/fpls.2019.00845
Yunnan, China. Syst. Appl. Microbiol. 28, 323–327. doi: 10.1016/j.syapm.2005.
01.008 Kulkova, I., Dobrzyński, J., Kowalczyk, P., Bełżecki, G., and Kramkowski, K. (2023).
Plant growth promotion using Bacillus cereus. Int. J. Mol. Sci. 24:9759. doi: 10.3390/
Huang, X., Wei, Z., Zhao, G., Gao, X., Yang, S., and Cui, Y. (2008). Optimization of ijms24119759
sterilization of Escherichia coli in milk by surfactin and fengycin using a response surface
method. Curr. Microbiol. 56, 376–381. doi: 10.1007/s00284-007-9066-8 Kumar, A., Kakrana, A., Sirohi, A., Subramaniam, K., Srinivasan, R., Abdin, M. Z.,
et al. (2017). Host-delivered RNAi-mediated root-knot nematode resistance in
Huang, Y., Xu, C., Ma, L., Zhang, K., Duan, C., and Mo, M. (2010). Characterisation Arabidopsis by targeting splicing factor and integrase genes. J. Gen. Plant Pathol. 83,
of volatiles produced from Bacillus megaterium YFM3. 25 and their nematicidal activity 91–97. doi: 10.1007/s10327-017-0701-3
against Meloidogyne incognita. Eur. J. Plant Pathol. 126, 417–422. doi: 10.1007/
s10658-009-9550-z Kumar, P., Pandhi, S., Mahato, D. K., Kamle, M., and Mishra, A. (2021). Bacillus-based
nano-bioformulations for phytopathogens and insect–pest management. Egypt. J. Biol.
Hui, F., Scheib, U., Hu, Y., Sommer, R. J., Aroian, R. V., and Ghosh, P. (2012). Structure Pest Control 31, 1–128. doi: 10.1186/s41938-021-00475-6
and glycolipid binding properties of the nematicidal protein Cry5B. Biochemistry 51,
9911–9921. doi: 10.1021/bi301386q Lee, Y. S., Cho, J. Y., Moon, J. H., and Kim, K. Y. (2016). Identification of
2-methylbutyric acid as a Nematicidal metabolite, and biocontrol and biofertilization
Iftikhar, Y., Sajid, A., Shakeel, Q., Ahmad, Z., and Ul Haq, Z. (2020). “Biological potentials of Bacillus pumilus L1. Korean J. Soil Sci. Fertil. 49, 401–408. doi: 10.7745/
antagonism: a safe and sustainable way to manage plant diseases” in Plant disease KJSSF.2016.49.4.401
management strategies for sustainable agriculture through traditional and modern
approaches: sustainability in plant and crop protection. eds. I. Ul Haq and S. Ijaz (Cham: Li, Q., Liu, S., Li, Y., Hao, T., and Chen, S. (2022). Nitrogen fixation by Paenibacillus
Springer). polymyxa WLY78 is responsible for cucumber growth promotion. Plant Soil 473,
507–516. doi: 10.1007/s11104-022-05307-6
Jaiswal, D. K., Gawande, S. J., Soumia, P. S., Krishna, R., Vaishnav, A., and Ade, A. B.
(2022). Biocontrol strategies: an eco-smart tool for integrated pest and diseases Li, L., Sun, Y., Chen, F., Hao, D., and Tan, J. (2023). An alkaline protease from Bacillus
management. BMC Microbiol. 22:324. doi: 10.1186/s12866-022-02744-2 cereus NJSZ-13 can act as a pathogenicity factor in infection of pinewood nematode.
BMC Microbiol. 23:10. doi: 10.1186/s12866-022-02752-2
Jamal, Q., Cho, J. Y., Moon, J. H., Munir, S., Anees, M., and Kim, K. Y. (2017).
Identification for the first time of Cyclo (d-pro-l-Leu) produced by Bacillus Li, L., Tan, J., and Chen, F. (2018). Bacillus pumilus strain LYMC-3 shows nematicidal
amyloliquefaciens Y1 as a Nematocide for control of Meloidogyne incognita. Molecules activity against Bursaphelenchus xylophilus via the production of a guanidine compound.
22:1839. doi: 10.3390/molecules22111839 Biocontrol Sci. Tech. 28, 1128–1139. doi: 10.1080/09583157.2018.1514587

Jang, S., Choi, S. K., Zhang, H., Zhang, S., Ryu, C. M., and Kloepper, J. W. (2023). Lilley, C. J., Kyndt, T., and Gheysen, G. (2011). “Nematode resistant GM crops in
History of a model plant growth-promoting rhizobacterium, Bacillus velezensis GB03: industrialised and developing countries” in Genomics and molecular genetics of plant-
from isolation to commercialization. Front. Plant Sci. 14:1279896. doi: 10.3389/ nematode interactions (Dordrecht: Springer), 17–541.
fpls.2023.1279896 Lin, L. Z., Zheng, Q. W., Wei, T., Zhang, Z. Q., Zhao, C. F., Zhong, H., et al. (2020).
Jeong, M. H., Yang, S. Y., Lee, Y. S., Ahn, Y. S., Park, Y. S., Han, H. R., et al. (2015). Isolation and characterization of fengycins produced by Bacillus amyloliquefaciens JFL21
Selection and characterization of Bacillus licheniformis MH48 for the biocontrol of pine and its broad-spectrum antimicrobial potential against multidrug-resistant foodborne
wood nematode (Bursaphelenchus xylophilus). J. Korean Soc. Forest Sci. 104, 512–518. pathogens. Front. Microbiol. 11:579621. doi: 10.3389/fmicb.2020.579621
doi: 10.14578/jkfs.2015.104.3.512 Liu, Z., Budiharjo, A., Wang, P., Shi, H., Fang, J., Borriss, R., et al. (2013). The highly
Jiang, H., Tian, L., Bu, F., Sun, Q., Zhao, X., and Han, Y. (2021). RNA-seq-based modified microcin peptide plantazolicin is associated with nematicidal activity of
identification of potential resistance genes against the soybean cyst nematode Bacillus amyloliquefaciens FZB42. Appl. Microbiol. Biotechnol. 97, 10081–10090. doi:
(Heterodera glycines) HG type 1.2.3.5.7 in ‘Dongnong L-10’. Physiol. Mol. Plant Pathol. 10.1007/s00253-013-5247-5
114:101627. doi: 10.1016/j.pmpp.2021.101627 Liu, G., Lin, X., Xu, S., Liu, G., Liu, F., and Mu, W. (2020). Screening, identification
Jouzani, G. S., Valijanian, E., and Sharafi, R. (2017). Bacillus thuringiensis: a successful and application of soil bacteria with nematicidal activity against root‐knot nematode
insecticide with new environmental features and tidings. Appl. Microbiol. Biotechnol. (Meloidogyne incognita) on tomato. Pest Manag. Sci. 76, 2217–2224. doi: 10.1002/ps.5759
101, 2691–2711. doi: 10.1007/s00253-017-8175-y Luo, L., Zhao, C., Wang, E., Raza, A., and Yin, C. (2022). Bacillus amyloliquefaciens as
Jung, W. J., Jung, S. J., An, K. N., Jin, Y. L., Park, R. D., Kim, K. Y., et al. (2002). Effect an excellent agent for biofertilizer and biocontrol in agriculture: an overview for its
of chitinase-producing Paenibacillus illinoisensis KJA-424 on egg hatching of root-knot mechanisms. Microbiol. Res. 259:127016. doi: 10.1016/j.micres.2022.127016
nematode (Meloidogyne incognita). J. Microbiol. Biotechnol. 12, 865–871. Available at: Mahapatra, S., Chakraborty, S., Samanta, M., Das, S., and Islam, T. (2022). “Current
https://koreascience.kr/ksci/search/article/articleView.ksci?articleBean. understanding and future directions of biocontrol of plant diseases by Bacillus spp., with
atclMgntNo=E1MBA4_2002_v12n6_865 special reference to induced systemic resistance” in Bacilli in agrobiotechnology: plant
Kahn, T. W., Duck, N. B., McCarville, M. T., Schouten, L. C., Schweri, K., stress tolerance, bioremediation, and bioprospecting (Cham: Springer International
Zaitseva, J., et al. (2021). A Bacillus thuringiensis cry protein controls soybean cyst Publishing), 127–150.
nematode in transgenic soybean plants. Nat. Commun. 12:3380. doi: 10.1038/ Mahmoud, W. M., Abdelmoneim, T. S., and Elazzazy, A. M. (2016). The impact of
s41467-021-23743-3 silver nanoparticles produced by Bacillus pumilus as antimicrobial and nematicide.
Kamalanathan, V., Sevugapperumal, N., and Nallusamy, S. (2023). Antagonistic Front. Microbiol. 7:1746. doi: 10.3389/fmicb.2016.01746
bacteria Bacillus velezensis VB7 possess nematicidal action and induce an immune Manivannan, A., Kumar, K. K., Varanavasiappan, S., Manimegalai, S., Poornima, K.,
response to suppress the infection of root-knot nematode (RKN) in tomato. Genes Devrajan, B. C., et al. (2019). Expression, purification and bioassay of Cry55Aa protein
14:1335. doi: 10.3390/genes14071335 against tomato root knot nematode, Meloidogyne incognita. Res. J. Pharmacogn.
Phytochem. 8, 570–573. doi: 10.5958/0975-4385.2020.00004.7
Kang, W. S., Chen, L. J., Wang, Y. Y., Zhu, X. F., Liu, X. Y., Fan, H. Y., et al. (2020).
Bacillus simplex treatment promotes soybean defence against soybean cyst nematodes: Manju, P., and Subramanian, S. (2017). Iturin and Surfactin families of Lipopeptides
a metabolomics study using GC-MS. PLoS One 15:e0237194. doi: 10.1371/journal. as key factors in antagonism of Bacillus subtilis towards Meloidogyne incognita on
pone.0237194 Gerbera jamesonii. Indian J. Nematol. 47, 31–38.
Karačić, V., Miljaković, D., Marinković, J., Ignjatov, M., Milošević, D., Tamindžić, G., Maqsood, A., Aslam, M. N., Khaliq, H., Shakeel, M. T., Wu, H., and Fahad, S. (2024).
et al. (2024). Bacillus species: excellent biocontrol agents against tomato diseases. Endophytic Bacillus spp. mediated plant growth promotion of tomato seedlings and
Microorganisms 12:457. doi: 10.3390/microorganisms12030457 suppression of Meloidogyne incognita and fusarium oxysporum disease complex. J. Plant
Growth Regul. 43, 2454–2469. doi: 10.1007/s00344-024-11279-x
Khan, A., Chen, S., Fatima, S., Ahamad, L., and Siddiqui, M. A. (2023).
Biotechnological tools to elucidate the mechanism of plant and nematode interactions. Marin-Bruzos, M., Grayston, S. J., Forge, T., and Nelson, L. M. (2021). Isolation and
Plan. Theory 12:2387. doi: 10.3390/plants12122387 characterization of streptomycetes and pseudomonad strains with antagonistic activity

Frontiers in Microbiology 26 frontiersin.org

Vasantha-Srinivasan et al. 10.3389/fmicb.2024.1510036

against the plant parasitic nematode Pratylenchus penetrans and fungi associated with root-knot nematode, Meloidogyne incognita, with Cinnamomum cassia crude extracts.
replant disease. Biol. Control 158:104599. doi: 10.1016/j.biocontrol.2021.104599 J. Korean Soc. Appl. Biol. Chem. 54, 507–514. doi: 10.3839/jksabc.2011.078
Mathew, R., and Opperman, C. H. (2019). The genome of the migratory nematode, Nicol, J. M., Turner, S. J., Coyne, D. L., Nijs, L. D., Hockland, S., and Maafi, Z. T.
Radopholus similis, reveals signatures of close association to the sedentary cyst (2011). “Current nematode threats to world agriculture” in Genomics and molecular
nematodes. PLoS One 14:e0224391. doi: 10.1371/journal.pone.0224391 genetics of plant-nematode interactions (Dordrecht: Springer), 21–43.
Mawarda, P. C., Mallon, C. A., Le Roux, X., Van Elsas, J. D., and Salles, J. F. (2022). Niu, Q., Huang, X., Zhang, L., Li, Y., Li, J., Yang, J., et al. (2006). A neutral protease
Interactions between bacterial inoculants and native soil bacterial community: the case from Bacillus nematocida, another potential virulence factor in the infection against
of spore-forming Bacillus spp. FEMS Microbiol. Ecol. 98:fiac127. doi: 10.1093/ nematodes. Arch. Microbiol. 185, 439–448. doi: 10.1007/s00203-006-0112-x
femsec/fiac127
Niu, Q., Tian, Y., Zhang, L., Xu, X. E., Niu, X., Xia, Z., et al. (2011). Overexpression of
Mazzuchelli, R. D. C. L., Mazzuchelli, E. H. L., and de Araujo, F. F. (2020). Efficiency the key virulence proteases Bace16 and Bae16 in Bacillus nematocida B16 to improve its
of Bacillus subtilis for root-knot and lesion nematodes management in sugarcane. Biol. nematocidal activity. J. Mol. Microbiol. Biotechnol. 21, 130–137. doi: 10.1159/000332805
Control 143:104185. doi: 10.1016/j.biocontrol.2020.104185
Niu, Q., Zhang, L., Zhang, K., Huang, X., Hui, F., Kan, Y., et al. (2016). Changes in
Mesa-Valle, C. M., Garrido-Cardenas, J. A., Cebrian-Carmona, J., Talavera, M., and intestinal microflora of Caenorhabditis elegans following Bacillus nematocida B16
Manzano-Agugliaro, F. (2020). Global research on plant nematodes. Agronomy 10:1148. infection. Sci. Rep. 6:20178. doi: 10.1038/srep20178
doi: 10.3390/agronomy10081148
O’Callaghan, M. (2016). Microbial inoculation of seed for improved crop performance:
Messa, V., Nunes, J., and Mattei, D. (2019). Seed treatment with Bacillus issues and opportunities. Appl. Microbiol. Biotechnol. 100, 5729–5746. doi: 10.1007/
amyloliquefaciens for the control of Meloidogyne javanica" in vivo" bean culture and its s00253-016-7590-9
direct effect on the motility, mortality and hatching of M. javanica "in vitro". Agron. Sci.
Oh, I. J., Ju, W. T., Kim, Y. J., Jung, W. J., Kim, K. Y., and Park, R. D. (2014a).
Biotechnol. 5:59. doi: 10.33158/ASB.2019v5i2p59
Nematicidal activity of Auxarthron reticulatum DY-2 against the pine wood nematode
Mian, S., Machado, A. C. Z., Hoshino, R. T., Mosela, M., Higashi, A. Y., Shimizu, G. D., Bursaphelenchus mucronatus. Nematology 16, 427–436. doi: 10.1163/15685411-00002775
et al. (2024). Complete genome sequence of Bacillus velezensis strain Ag109, a biocontrol
Oh, I. J., Kim, Y. J., and Kim, K. Y. (2014b). Nematicidal activity of Verticillium
agent against plant-parasitic nematodes and Sclerotinia sclerotiorum. BMC Microbiol.
saksenae A-1 against the pine wood nematode Bursaphelenchus mucronatus. J. Chitin
24:194. doi: 10.1186/s12866-024-03282-9
Chitos. 19, 81–86.
Migunova, V. D., and Sasanelli, N. (2021). Bacteria as biocontrol tool against
Oka, Y. (2010). Mechanisms of nematode suppression by organic soil amendments—a
phytoparasitic nematodes. Plan. Theory 10:389. doi: 10.3390/plants10020389
review. Appl. Soil Ecol. 44, 101–115. doi: 10.1016/j.apsoil.2009.11.003
Migunova, V. D., Tomashevich, N. S., Konrat, A. N., Lychagina, S. V., Dubyaga, V. M.,
Olagoke, F. K., Bettermann, A., Nguyen, P. T. B., Redmile-Gordon, M., Babin, D.,
D’Addabbo, T., et al. (2021). Selection of bacterial strains for control of root-knot disease
Smalla, K., et al. (2022). Importance of substrate quality and clay content on microbial
caused by Meloidogyne incognita. Microorganisms 9:1698. doi: 10.3390/
extracellular polymeric substances production and aggregate stability in soils. Biol. Fertil.
microorganisms9081698
Soils 58, 435–457. doi: 10.1007/s00374-022-01632-1
Miljaković, D., Marinković, J., and Balešević-Tubić, S. (2020). The significance of
Oliveira, D. F., Santos, H. M. D., Nunes, A. S., Campos, V. P., Pinho, R. S. D., and
Bacillus spp. in disease suppression and growth promotion of field and vegetable crops.
Gajo, G. C. (2014). Purification and identification of metabolites produced by Bacillus
Microorganisms 8:1037. doi: 10.3390/microorganisms8071037
cereus and B. subtilis active against Meloidogyne exigua, and their in silico interaction
Moens, M., Perry, R. N., and Jones, J. T. (2018). “Cyst nematodes - life cycle and with a putative phosphoribosyltransferase from M. incognita. An. Acad. Bras. Cienc. 86,
economic importance” in Cyst nematodes (Wallingford: CABI), 1–26. 525–538. doi: 10.1590/0001-3765201402412
Mohamed, S. A., El-Sayed, G. M., Elkelany, U. S., Youssef, M. M., El-Nagdi, W. M., and Ortiz, A., and Sansinenea, E. (2023). “Microbial-based biopesticides:
Soliman, G. M. (2021). A local Bacillus spp.: isolation, genetic improvement, nematode commercialization and regulatory perspectives” in Development and commercialization
biocontrol, and nitrogen fixation. Egyptian. Pharm. J. 20, 352–363. doi: 10.4103/epj. of biopesticides (Cambridge, Massachusetts, USA: Academic Press), 103–118.
epj_30_21
Osman, H. A., Ameen, H. H., Mohamed, M., and Elkelany, U. S. (2020). Efficacy of
Montesinos, E. (2003). Development, registration and commercialization of microbial integrated microorganisms in controlling root-knot nematode Meloidogyne javanica
pesticides for plant protection. Int. Microbiol. 6, 245–252. doi: 10.1007/ infecting peanut plants under field conditions. Bull. Natl. Res. Cent. 44, 1–10. doi:
s10123-003-0144-x 10.1186/s42269-020-00366-0
Moslehi, S., Pourmehr, S., Shirzad, A., and Khakvar, R. (2021). Potential of some Pacifico, M. G., Eckstein, B., and Bettiol, W. (2021). Screening of Bacillus for the
endophytic bacteria in biological control of root-knot nematode Meloidogyne incognita. development of bioprotectants for the control of Fusarium oxysporum f. sp. vasinfectum
Egypt. J. Biol. Pest Control 31, 1–11. doi: 10.1186/s41938-021-00396-4 and Meloidogye incognita. Biol. Control 164:104764. doi: 10.1016/j.
Mostafa, F. A., Khalil, A. E., Nour, A., and Ibrahim, D. S. (2018). The role of Bacillus biocontrol.2021.104764
megaterium and other bio-agents in controlling root-knot nematodes infecting sugar Padgham, J. L., and Sikora, R. A. (2007). Biological control potential and modes of
beet under field conditions. Egypt. J. Biol. Pest Control 28, 1–6. doi: 10.1186/ action of Bacillus megaterium against Meloidogyne graminicola on rice. Crop Prot. 26,
s41938-018-0068-6 971–977. doi: 10.1016/j.cropro.2006.09.004
Nadeem, H., Niazi, P., Asif, M., Kaskavalci, G., and Ahmad, F. (2021). Bacterial strains Palomares-Rius, J. E., Clavero-Camacho, I., Archidona-Yuste, A.,
integrated with surfactin molecules of Bacillus subtilis MTCC441 enrich nematocidal Cantalapiedra-Navarrete, C., León-Ropero, G., Braun Miyara, S., et al. (2020). Global
activity against Meloidogyne incognita. Plant Biol. 23, 1027–1036. doi: 10.1111/plb.13301 distribution of the reniform nematode genus Rotylenchulus with the synonymy of
Ngalimat, M. S., Yahaya, R. S. R., Baharudin, M. M. A. A., Yaminudin, S. M., Rotylenchulus macrosoma with Rotylenchulus borealis. Plan. Theory 10:7. doi: 10.3390/
Karim, M., Ahmad, S. A., et al. (2021). A review on the biotechnological applications of plants10010007
the operational group Bacillus amyloliquefaciens. Microorganisms 9:614. doi: 10.3390/ Pandey, N., Vaishnav, R., Rajavat, A. S., Singh, A. N., Kumar, S., Tripathi, R. M., et al.
microorganisms9030614 (2024). Exploring the potential of Bacillus for crop productivity and sustainable solution
Nguyen, V. N., Ju, W. T., Kim, Y. J., Jung, W. J., Kim, K. Y., and Park, R. D. (2014). for combating rice false smut disease. Front. Microbiol. 15:1405090. doi: 10.3389/
Suppression of cucumber root-knot nematode Meloidogyne incognita by chitinolytic fmicb.2024.1405090
fungi Lecanicillium pasalliotae A-1 and Lecanicillium antillanum B-3. J. Chitin Chitos. Paradva, K. C., and Kalla, S. (2023). Nanopesticides: a review on current research and
19, 93–99. future perspective. Chem. Select 8:e202300756. doi: 10.1002/slct.202300756
Nguyen, D. M. C., and Jung, W. J. (2014). Nematicidal properties of crude extracts Park, M. R., Oh, S., Son, S. J., Park, D. J., Oh, S., Kim, S. H., et al. (2015). Bacillus
obtained from medicinal plants against root-lesion nematode Pratylenchus coffeae. J. licheniformis isolated from traditional Korean food resources enhances the longevity of
Viet. Environ. 6, 264–269. doi: 10.13141/jve.vol6.no3.pp264-269 Caenorhabditis elegans through serotonin signaling. J. Agric. Food Chem. 63,
Nguyen, X. H., Naing, K. W., Lee, Y. S., Jung, W. J., Anees, M., and Kim, K. Y. (2013). 10227–10233. doi: 10.1021/acs.jafc.5b03730
Antagonistic potential of Paenibacillus elgii HOA73 against the root-knot nematode, Patil, G. B., Lakhssassi, N., Wan, J., Song, L., Zhou, Z., Klepadlo, M., et al. (2019).
Meloidogyne incognita. Nematology 15, 991–1000. doi: 10.1163/15685411-00002737 Whole‐genome re‐sequencing reveals the impact of the interaction of copy number
Nguyen, D. M. C., Seo, D. J., Kim, K. Y., Kim, T. H., and Jung, W. J. (2012). variants of the rhg1 and Rhg4 genes on broad‐based resistance to soybean cyst
Nematode-antagonistic effects of Cinnamomum aromaticum extracts and a purified nematode. Plant Biotechnol. J. 17, 1595–1611. doi: 10.1111/pbi.13086
compound against Meloidogyne incognita. Nematology 14, 913–924. doi: Pontes, K. B., Machado, A. C. Z., Nogueira, A. F., Fagundes, D. F. V., de Lima
10.1163/156854112X634987 Filho, R. B., Mosela, M., et al. (2024). Efficacy of microbiological nematicides in
Nguyen, V. N., Seo, D. J., Park, R. D., and Jung, W. J. (2009). Nematicidal activity of controlling root-knot nematodes in tomato. Front. Agron. 6:1462323. doi: 10.3389/
compounds extracted from medicinal plants against the pine wood nematode fagro.2024.1462323
Bursaphelenchus xylophilus. Nematology 11, 835–845. doi: 10.1163/156854109X424353 Pradhan, P., Naresh, P., Barik, S., Acharya, G. C., and Bastia, R. (2023). Adamala
Nguyen, D. M. C., Seo, D. J., Park, R. D., Lee, B. R., and Jung, W. J. (2011). Changes in breeding for root-knot nematode resistance in fruiting Solanaceous vegetable crops: a
antioxidative enzyme activities in cucumber plants with regard to biological control of review. Euphytica 219:71. doi: 10.1007/s10681-023-03204-2

Frontiers in Microbiology 27 frontiersin.org

Vasantha-Srinivasan et al. 10.3389/fmicb.2024.1510036

Pueyo, M. T., Bloch, C., Carmona-Ribeiro, A. M., and Di Mascio, P. (2009). Sanahuja, G., Banakar, R., Twyman, R. M., Capell, T., and Christou, P. (2011). Bacillus
Lipopeptides produced by a soil Bacillus megaterium strain. Microb. Ecol. 57, 367–378. thuringiensis: a century of research, development and commercial applications. Plant
doi: 10.1007/s00248-008-9464-x Biotechnol. J. 9, 283–300. doi: 10.1111/j.1467-7652.2011.00595.x
Rabbee, M. F., Ali, M. S., Choi, J., Hwang, B. S., Jeong, S. C., and Baek, K. H. (2019). Santos, J., Silva, A., Queiroz, P., Eckstein, B., and Monnerat, R. (2022). Selection of
Bacillus velezensis: a valuable member of bioactive molecules within plant microbiomes. Bacillus thuringiensis strains toxic to Meloidogyne incognita. Anais Escol. Agron. Veter.
Molecules 24:1046. doi: 10.3390/molecules24061046 52:e73070. doi: 10.1590/1983-40632022v5273070
Rabbee, M. F., Hwang, B. S., and Baek, K. H. (2023). Bacillus velezensis: a beneficial Saxena, A. K., Kumar, M., Chakdar, H., Anuroopa, N., and Bagyaraj, D. J. (2020).
biocontrol agent or facultative phytopathogen for sustainable agriculture. Agronomy Bacillus species in soil as a natural resource for plant health and nutrition. J. Appl.
13:840. doi: 10.3390/agronomy13030840 Microbiol. 128, 1583–1594. doi: 10.1111/jam.14506
Radwan, M. A. (2007). Efficacy of Bacillus thuringiensis integrated with other non- Schnepf, E., Crickmore, N., Van Rie, J., Lereclus, D., Baum, J., Feitelson, J., et al. (1998).
chemical materials to control Meloidogyne incognita in tomato. Nematol. Mediterr. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 62,
35, 69–73. 775–806. doi: 10.1128/mmbr.62.3.775-806.1998
Ramalakshmi, A., Sharmila, R., Iniyakumar, M., and Gomathi, V. (2020). Nematicidal Seo, D. J., Nguyen, V. N., Kim, K. Y., Park, R. D., and Jung, W. J. (2013). Nematicidal
activity of native Bacillus thuringiensis against the root knot nematode, Meloidogyne activity of gallic acid purified from Terminalia nigrovenulosa bark against the root-knot
incognita (Kofoid and white). Egypt. J. Biol. Pest Control 30, 1–9. doi: 10.1186/ nematode Meloidogyne incognita. Nematology 15, 507–518. doi:
s41938-020-00293-2 10.1163/15685411-00002696
Ramezani Moghaddam, M., Mahdikhani Moghaddam, E., Baghaee Ravari, S., and Serrão, C. P., Ortega, J. C. G., Rodrigues, P. C., and de Souza, C. R. B. (2024). Bacillus
Rouhani, H. (2014). The first report of Bacillus pumilus influence against Meloidogyne species as tools for biocontrol of plant diseases: a meta-analysis of twenty-two years of
javanica in Iran. J. Crop Protect. 3, 105–112. research, 2000–2021. World J. Microbiol. Biotechnol. 40:110. doi: 10.1007/
s11274-024-03935-x
Ramírez-Pool, J. A., Calderón-Pérez, B., Ruiz-Medrano, R., Ortiz-Castro, R., and
Xoconostle-Cazares, B. (2024). Bacillus strains as effective biocontrol agents against Settu, V., Annaiyan, S., and Mannu, J. (2024). Revealing the genetic arsenal of Bacillus
Phytopathogenic Bacteria and promoters of plant growth. Microb. Ecol. 87:76. doi: firmus TNAU1: unleashing nematicidal and plant growth promotion traits. Physiol. Mol.
10.1007/s00248-024-02384-1 Plant Pathol. 129:102177. doi: 10.1016/j.pmpp.2023.102177
Ramyabharathi, S. A., Meena, K. S., Rajendran, L., Raguchander, T., and Shafi, J., Tian, H., and Ji, M. (2017). Bacillus species as versatile weapons for plant
Jonathan, E. I. (2020). Potential of a rhizobacterium Bacillus subtilis (Bbv 57) on pathogens: a review. Biotechnol. Biotechnol. Equip. 31, 446–459. doi:
fusarium oxysporum f. sp. gerberae and Meloidogyne incognita infecting Gerbera grown 10.1080/13102818.2017.1286950
in protected cultivation. Eur. J. Plant Pathol. 158, 615–632. doi: 10.1007/
Shi, J., Peng, D., Zhang, F., Ruan, L., and Sun, M. (2020). The Caenorhabditis elegans
s10658-020-02087-6
CUB-like-domain containing protein RBT-1 functions as a receptor for Bacillus
Rao, M. S., Kamalnath, M., Umamaheswari, R., Rajinikanth, R., Prabu, P., Priti, K., thuringiensis Cry6Aa toxin. PLoS Pathog. 16:e1008501. doi: 10.1371/journal.
et al. (2017). Bacillus subtilis IIHR BS-2 enriched vermicompost controls root knot ppat.1008501
nematode and soft rot disease complex in carrot. Sci. Hortic. 218, 56–62. doi: 10.1016/j.
Shu, J., Zhang, R. J., Liang, Y. C., Chen, Y. Q., Zhang, J., Guo, J., et al. (2021). Control
scienta.2017.01.051
of root-knot nematode disease by compounding biological agents from plant and
Raymond, B., and Federici, B. A. (2017). In defence of Bacillus thuringiensis, the safest microorganisms. Biotechnol. Bull. 37, 164–174. doi: 10.13560/j.cnki.biotech.
and most successful microbial insecticide available to humanity - a response to EFSA. bull.1985.2021-0408
FEMS Microbiol. Ecol. 93. doi: 10.1093/femsec/fix084
Sikora, R. A., and Roberts, P. A. (2018). “Management practices: an overview of
Raza, A., Hassan, A., Akram, W., Anjum, T., and Ali, B. (2024). Seed coating with the integrated nematode management technologies,” Plant Parasit. Nemat. Subtrop. Trop.
synthetic consortium of beneficial Bacillus microbes improves seedling growth and Agric. eds. R. A. Sikora, D. Coyne, J. Hallmann and P. Timper (Wallingford, UK: CABI),
manages fusarium wilt disease. Sci. Hortic. 325:112645. doi: 10.1016/j. 2nd Edition. 795–838.
scienta.2023.112645
Singh, S., Balodi, R., Meena, P. N., and Singhal, S. (2021). Biocontrol activity of
Riascos-Ortiz, D., Mosquera-Espinosa, A. T., Varón de Agudelo, F., Oliveira, C. M. G., Trichoderma harzianum, Bacillus subtilis and Pseudomonas fluorescens against
and Muñoz Flórez, J. E. (2022). “Non-conventional management of plant-parasitic Meloidogyne incognita, fusarium oxysporum and Rhizoctonia solani. Indian Phytopathol.
nematodes in musaceas crops” in Sustainable management of nematodes in agriculture, 74, 703–714. doi: 10.1007/s42360-021-00368-6
Vol. 1: organic management (Cham: Springer International Publishing), 381–422.
Singh, B. K., Delgado-Baquerizo, M., Egidi, E., Guirado, E., Leach, J. E., Liu, H., et al.
Riseh, R. S., Vatankhah, M., Hassanisaadi, M., and Barka, E. A. (2024). Unveiling the (2023). Climate change impacts on plant pathogens, food security and paths forward.
role of hydrolytic enzymes from soil biocontrol Bacteria in sustainable Phytopathogen Nat. Rev. Microbiol. 21, 640–656. doi: 10.1038/s41579-023-00900-7
management. Front. Biosci. 29:105. doi: 10.31083/j.fbl2903105
Singh, A., Sharma, P., Kumari, A., Kumar, R., and Pathak, D. V. (2019). “Management
Rocha, L. F., and Duggal, P. (2023). “Management of Cyst-Forming Nematodes in of Root-Knot Nematode in different crops using microorganisms” in Plant biotic
agricultural crops through novel biological and genetic engineering technologies” in interactions. eds. A. Varma, S. Tripathi and R. Prasad (Cham: Springer), 85–99.
Novel biological and biotechnological applications in plant nematode management
(Singapore: Springer Nature), 313–339. Sohrabi, F., Sheikholeslami, M., Heydari, R., Rezaee, S., and Sharifi, R. (2020).
Investigating the effect of Glomus mosseae, Bacillus subtilis and Trichoderma harzianum
Rostami, M., Karegar, A., and Taghavi, S. M. (2021). Biocontrol potential of bacterial
on plant growth and controlling Meloidogyne javanica in tomato. Indian Phytopathol.
isolates from vermicompost and earthworm against the root-knot nematode
73, 293–300. doi: 10.1007/s42360-020-00227-w
Meloidogyne javanica infecting tomato plants. Egypt. J. Biol. Pest Control 31:36. doi:
10.1186/s41938-021-00383-9 Steinberg, N., Keren-Paz, A., Hou, Q., Doron, S., Yanuka-Golub, K., Olender, T., et al.
(2020). The extracellular matrix protein TasA is a developmental cue that maintains a
Rostami, M., Shahbazi, S., Soleimani, R., and Ghorbani, A. (2024). Optimizing
motile subpopulation within Bacillus subtilis biofilms. Sci. Signal. 13:eaaw8905. doi:
sustainable control of Meloidogyne javanica in tomato plants through gamma radiation-
10.1126/scisignal.aaw8905
induced mutants of Trichoderma harzianum and Bacillus velezensis. Sci. Rep. 14:17774.
doi: 10.1038/s41598-024-68365-z Stoica, R. M., Moscovici, M. I. Ș. U., Tomulescu, C. A. T. E. R. I. N. A., Cășărică, A. N.
Rozas, E. E., Dias, M., Acosta, A. M. L., Custódio, M. R., do, C., and Mendes, M. G. E. L. A., Băbeanu, N. A. R. C. I. S. A., Popa, O. V. I. D. I. U., et al. (2019). Antimicrobial
(2024). Proteomic characterization of metal recovery process realized by marine bacteria compounds of the genus Bacillus: a review. Rom. Biotechnol. Lett. 24, 1111–1119. doi:
bacillus subtilis Hyhel1expossed to bioleaching liquor. Braz. J. Chem. Eng. 41, 865–874. 10.25083/rbl/24.6/1111.1119
doi: 10.1007/s43153-023-00350-x Sturhan, D. I. E. T. E. R., and Brzeski, M. W. (2020). “Stem and bulb nematodes,
Ruiu, L. (2015). Insect pathogenic bacteria in integrated pest management. Insects 6, Ditylenchus spp” in Manual of agricultural nematology (Boca Raton, Florida, USA: CRC
352–367. doi: 10.3390/insects6020352 Press), 423–464.

Ryu, C. M., Shin, J. N., Qi, W., Ruhong, M., Kim, E. J., and Pan, J. G. (2011). Potential Subbotin, S. A., Rius, J. E. P., and Castillo, P. (2021). Systematics of root-knot nematodes
for augmentation of fruit quality by foliar application of bacilli spores on apple tree. (Nematoda: Meloidogynidae): Brill Available at: https://Iccn.loc.gov/2021030916.
Plant Pathol. J. 27, 164–169. doi: 10.5423/PPJ.2011.27.2.164 Sun, M., Liang, C., Fu, X., Liu, G., Zhong, Y., Wang, T., et al. (2024). Nematocidal
Saeid, A., Prochownik, E., and Dobrowolska-Iwanek, J. (2018). Phosphorus activity and biocontrol efficacy of endophytic Bacillus velezensis Pt-RP9 from Pinus
solubilization by Bacillus species. Molecules 23:2897. doi: 10.3390/molecules23112897 tabuliformis against pine wilt disease caused by Bursaphelenchus xylophilus. Biol. Control
196:105579. doi: 10.1016/j.biocontrol.2024.105579
Saikai, K., and MacGuidwin, A. E. (2022). Impact of Pratylenchus penetrans on
soybean grown in Wisconsin, USA. Plant Dis. 106, 2904–2910. doi: 10.1094/ Sun, X. L., Yang, Y. H., Zhu, L., Liu, F. Y., Xu, J. P., Huang, X. W., et al. (2018). The
PDIS-09-21-1888-RE lysine acetylome of the nematocidal bacterium Bacillus nematocida and impact of
nematode on the acetylome. J. Proteome 177, 31–39. doi: 10.1016/j.jprot.2018.02.005
Samal, I., Bhoi, T. K., Mahanta, D. K., Komal, J., and Singh, S. (2024). Chapter 3
biorational pest management: potentials, unintended consequences, and future Tian, B., Yang, J., and Zhang, K. Q. (2007). Bacteria used in the biological control of
concerns. In: R. Kumar, OliveiraM. de, Aguiar AndradeE. de, D. Suyal and R. Soni, eds. plant-parasitic nematodes: populations, mechanisms of action, and future prospects.
Biorationals and biopesticides: pest management, Berlin, Boston: De Gruyter 47–76. FEMS Microbiol. Ecol. 61, 197–213. doi: 10.1111/j.1574-6941.2007.00349.x

Frontiers in Microbiology 28 frontiersin.org

Vasantha-Srinivasan et al. 10.3389/fmicb.2024.1510036

Tian, X. L., Zhao, X. M., Zhao, S. Y., Zhao, J. L., and Mao, Z. C. (2022). The biocontrol Xing, Z., Wu, X., Zhao, J., Zhao, X., Zhu, X., Wang, Y., et al. (2020). Isolation and
functions of Bacillus velezensis strain Bv-25 against Meloidogyne incognita. Front. identification of induced systemic resistance determinants from Bacillus simplex
Microbiol. 13:843041. doi: 10.3389/fmicb.2022.843041 Sneb545 against Heterodera glycines. Sci. Rep. 10:11586. doi: 10.1038/s41598-020-68548-4
Timper, P. (2014). Conserving and enhancing biological control of nematodes. J. Xiong, J., Zhou, Q., Luo, H., Xia, L., Li, L., Sun, M., et al. (2015). Systemic nematicidal
Nematol. 46, 75–89. activity and biocontrol efficacy of Bacillus firmus against the root-knot nematode
Meloidogyne incognita. World J. Microbiol. Biotechnol. 31, 661–667. doi: 10.1007/
Tong-Jian, X. I. A. O., Fang, C. H. E. N., Chao, G. A. O., Qing-Yun, Z. H. A. O.,
s11274-015-1820-7
Qi-Rong, S. H. E. N., and Wei, R. A. N. (2013). Bacillus cereus X5 enhanced bio-organic
fertilizers effectively control root-knot nematodes (Meloidogyne sp.). Pedosphere 23, Yang, J., Liang, L., Li, J., and Zhang, K. (2013). Nematicidal enzymes from
160–168. doi: 10.1016/S1002-0160(13)60003-X microorganisms and their applications. Appl. Microbiol. Biotechnol. 97, 7081–7095. doi:
10.1007/s00253-013-5045-0
Tran, T. P. H., Wang, S. L., Nguyen, V. B., Tran, D. M., Nguyen, D. S., and Nguyen, A. D.
(2019). Study of novel endophytic bacteria for biocontrol of black pepper root-knot Yang, T., Xin, Y., Liu, T., Li, Z., Liu, X., Wu, Y., et al. (2022). Bacterial volatile-mediated
nematodes in the central highlands of Vietnam. Agronomy 9:714. doi: 10.3390/ suppression of root-knot nematode (Meloidogyne incognita). Plant Dis. 106, 1358–1365.
agronomy9110714 doi: 10.1094/PDIS-06-21-1139-RE
Umamaheswari, R., Rao, M. S., Chaya, M. K., Sowmyavani, M., Navyashree, R. K., Ye, L., Wang, J. Y., Liu, X. F., Guan, Q., Dou, N. X., Li, J., et al. (2022). Nematicidal activity
and Kavya, B. M. (2020). Bio-efficacy of liquid formulations of Bacillus subtilis IIHR of volatile organic compounds produced by Bacillus altitudinis AMCC 1040 against
Bs-2 (1% AS) and Bacillus amyloliquefaciens IIHR Ba-2 (1% AS) in the management Meloidogyne incognita. Arch. Microbiol. 204:521. doi: 10.1007/s00203-022-03024-3
of Meloidogyne incognita infecting tomato. Pest Manag. Horticul. Ecosyst. 26, 262–268.
Yin, N., Liu, R., Zhao, J. L., Khan, R. A. A., Li, Y., Ling, J., et al. (2021a). Volatile organic
Van Frankenhuyzen, K. (2009). Insecticidal activity of Bacillus thuringiensis crystal compounds of Bacillus cereus strain Bc-cm103 exhibit fumigation activity against
proteins. J. Invertebr. Pathol. 101, 1–16. doi: 10.1016/j.jip.2009.02.009 Meloidogyne incognita. Plant Dis. 105, 904–911. doi: 10.1094/PDIS-04-20-0783-RE
Van Frankenhuyzen, K. (2013). Cross-order and cross-phylum activity of Bacillus Yin, Y., Wang, P., Wang, X., and Wen, J. (2024). Construction of Bacillus subtilis for
thuringiensis pesticidal proteins. J. Invertebr. Pathol. 114, 76–85. doi: 10.1016/j. efficient production of fengycin from xylose through CRISPR-Cas9. Front. Microbiol.
jip.2013.05.010 14:1342199. doi: 10.3389/fmicb.2023.1342199
Vasques, N. C., Nogueira, M. A., and Hungria, M. (2024). Increasing application of Yin, N., Zhao, J. L., Liu, R., Li, Y., Ling, J., Yang, Y. H., et al. (2021b). Biocontrol efficacy
multifunctional Bacillus for biocontrol of pests and diseases and plant growth of Bacillus cereus strain Bc-cm103 against Meloidogyne incognita. Plant Dis. 105,
promotion: lessons from Brazil. Agronomy 14:1654. doi: 10.3390/agronomy14081654 2061–2070. doi: 10.1094/PDIS-03-20-0648-RE
Verduzco-Rosas, L. A., García-Suárez, R., López-Tlacomulco, J. J., and Ibarra, J. E. Yu, Z., Xiong, J., Zhou, Q., Luo, H., Hu, S., Xia, L., et al. (2015). The diverse nematicidal
(2021). Selection and characterization of two Bacillus thuringiensis strains showing properties and biocontrol efficacy of Bacillus thuringiensis Cry6A against the root-knot
nematicidal activity against Caenorhabditis elegans and Meloidogyne incognita. FEMS nematode Meloidogyne hapla. J. Invertebr. Pathol. 125, 73–80. doi: 10.1016/j.
Microbiol. Lett. 368:fnaa186. doi: 10.1093/femsle/fnaa186 jip.2014.12.011
Waller, P. J., and Thamsborg, S. M. (2004). Nematode control in ‘green’ ruminant Yuan, Y., Yan, Z., Chen, Y., Ye, J., and Tan, J. (2023). Effects of Bacillus cereus on
production systems. Trends Parasitol. 20:493. doi: 10.1016/j.pt.2004.07.012 survival, fecundity, and host adaptability of pine wood nematode. Diversity 15:566. doi:
10.3390/d15040566
Wang, J. Y., Guo, C., Zhao, P., Yu, F. Y., Su, Y., Qu, J. P., et al. (2021a). Biocontrol
potential of Bacillus altitudinis AMCC1040 against root-knot nematode disease of ginger Yun, H. S., Heo, J. H., Son, S. J., Park, M. R., Oh, S., Song, M. H., et al. (2014). Bacillus
and its impact on rhizosphere microbial community. Biol. Control 158:104598:104598. licheniformis isolated from Korean traditional food sources enhances the resistance of
doi: 10.1016/j.biocontrol.2021.104598 Caenorhabditis elegans to infection by Staphylococcus aureus. J. Microbiol. Biotechnol. 24,
1105–1108. doi: 10.4014/jmb.1406.06008
Wang, J. Y., Zhang, X. C., Guo, C., Li, P. G., Yu, F. Y., Zhao, P., et al. (2021b).
Diversity and nematocidal activity of culturable bacteria from suppressive soils in Zhang, L. N., Jiang, C. H., Si, F., Song, N., Yang, W., Zhu, Y., et al. (2024). Long-term
Shandong Province, China. Biocontrol Sci. Tech. 31, 387–399. doi: 10.1080/09583157. field application of a plant growth-promoting rhizobacterial consortium suppressed
2020.1854176 root-knot disease by shaping the rhizosphere microbiota. Plant Dis. 108, 94–103. doi:
10.1094/PDIS-09-22-2196-RE
Wei, J. Z., Hale, K., Carta, L., Platzer, E., Wong, C., Fang, S. C., et al. (2003). Bacillus
Zhang, J., Li, Y., Yuan, H., Sun, B., and Li, H. (2016). Biological control of the cereal
thuringiensis crystal proteins that target nematodes. Proc. Natl. Acad. Sci. 100,
cyst nematode (Heterodera filipjevi) by Achromobacter xylosoxidans isolate 09X01 and
2760–2765. doi: 10.1073/pnas.0538072100
Bacillus cereus isolate 09B18. Biol. Control 92, 1–6. doi: 10.1016/j.biocontrol.2015.08.004
Wepuhkhulu, M., Kimenju, J., Anyango, B., Wachira, P., and Kyallo, G. (2011). Effect Zhang, F., Peng, D., Ye, X., Yu, Z., Hu, Z., Ruan, L., et al. (2012). In vitro uptake of 140
of soil fertility management practices and Bacillus subtilis on plant parasitic nematodes kDa Bacillus thuringiensis nematicidal crystal proteins by the second stage juvenile of
associated with common bean, Phaseolus vulgaris. Trop. Subtrop. Agroecosyst. Meloidogyne hapla. PLoS One 7:e38534. doi: 10.1371/journal.pone.0038534
13, 27–34.
Zhang, J. X., Xue, A. G., and Tambong, J. T. (2009). Evaluation of seed and soil treatments
Widianto, D., Pramita, A. D., Kurniasari, I., Arofatullah, N. A., Prijambada, I. D., with novel Bacillus subtilis strains for control of soybean root rot caused by fusarium
Widada, J., et al. (2021). Bacillus is one of the most potential genus as a biocontrol agent oxysporum and F. Graminearum. Plant Dis. 93, 1317–1323. doi: 10.1094/PDIS-93-12-1317
of golden cyst nematode (Globodera rostochiensis). Arch. Phytopathol. Plant Protect. 54,
2191–2205. doi: 10.1080/03235408.2021.1925501 Zhaojian, G., Qiufen, W., Feihong, D., Xiang, X., Yifeng, Z., Wei, J., et al. (2021).
Screening and mutagenesis of broad-spectrum antagonistic Bacillus licheniformis and
Won, S. J., Choub, V., Kwon, J. H., Kim, D. H., and Ahn, Y. S. (2018). The control of purification and identification of antimicrobial substances produced by its mutant. Food
fusarium root rot and development of coastal pine (Pinus thunbergii Parl.) seedlings in a Sci. 42, 143–150. doi: 10.7506/spkx1002-6630-20191112-161
container nursery by use of Bacillus licheniformis MH48. Forests 10:6. doi: 10.3390/f10010006
Zhou, Y., Chen, J., Zhu, X., Wang, Y., Liu, X., Fan, H., et al. (2021). Efficacy of Bacillus
Wu, W., Zeng, Y., Yan, X., Wang, Z., Guo, L., Zhu, Y., et al. (2023). Volatile organic megaterium strain Sneb207 against soybean cyst nematode (Heterodera glycines) in
compounds of Bacillus velezensis GJ-7 against Meloidogyne hapla through multiple soybean. Pest Manag. Sci. 77, 568–576. doi: 10.1002/ps.6057
prevention and control modes. Molecules 28:3182. doi: 10.3390/molecules28073182
Zhu, M., Xu, X. E., Li, Y., Wang, P., Niu, S., Zhang, K., et al. (2019). Biosynthesis of the
Xia, Y., Xie, S., Ma, X., Wu, H., Wang, X., and Gao, X. (2011). The purL gene of Bacillus nematode attractant 2-Heptanone and its co-evolution between the pathogenic
subtilis is associated with nematicidal activity. FEMS Microbiol. Lett. 322, 99–107. doi: bacterium Bacillus nematocida and non-pathogenic bacterium Bacillus subtilis. Front.
10.1111/j.1574-6968.2011.02336.x Microbiol. 10:1489. doi: 10.3389/fmicb.2019.01489
Xiao, F., Zhang, Y., Zhang, L., Li, S., Chen, W., Shi, G., et al. (2024). Advancing Bacillus Zuckerman, B. M., Dicklow, M. B., and Acosta, N. (1993). A strain Ofbacillus
licheniformis as a superior expression platform through promoter engineering. thuringiensis for the control of plant‐parasitic nematodes. Biocontrol Sci. Tech. 3, 41–46.
Microorganisms 12:1693. doi: 10.3390/microorganisms12081693 doi: 10.1080/09583159309355257

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