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 Insects and Other Terrestrial
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Charlie B. Morris
Editor

Weevils
Biology, Behavior and Ecology
Copyright © 2024 by Nova Science Publishers, Inc.

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Contents

Preface .......................................................................................... vii

Chapter 1 Circular Economy in the Production of
Entomopathogenic Fungi for Enzyme
Production and Biological Control of
Insect Pests .........................................................................1
Emma O. Fuentes-Ramírez,
Rafael Uzárraga-Salazar,
Caliope Mendarte-Alquisira and
Gabriel R. Hernández-Martínez
Chapter 2 Reserve Mobilization During the
Embryogenesis of the Cowpea Weevil
Callosobruchus maculatus (F) .........................................37
Kayan E. Ventury, Sarah Rodrigues Ferreira,
Aline Gama Melila Licurgo, Leonardo F. R. De Sá,
Eduardo A. G. Oliveira, Andre T. S. Ferreira,
Jonas Perales, Olga L. T. Machado,
Kátia V. S. Fernandes, Thiago M. Venancio and
Antonia E. A. Oliveira
Chapter 3 The Use of Soil Microorganisms in the
Biological Control of Insects:
The Application of Microorganism Toxins and
Their Effects on Agrosystems .........................................69
Dulce Jazmín Hernández-Melchor,
Caliope Mendarte-Alquisira, Sandra Cortes-Pérez,
Claudia García-Sánchez and
Pablo Antonio López-Pérez
vi Contents

Chapter 4 A Generic Mathematical Model for Pest Control

with Time Delay Dynamics Based on
Silico Approaches ............................................................95
Pablo A. López Pérez, Eduardo Alvarado-Santos,
Dulce Jazmín Hernández Melchor,
Francisco Javier Martınez-Farıas and
Edith Jiménez Muñoz
Chapter 5 An Overview of the Rice Weevil ...................................129
Edith Jiménez Muñoz, Abraham Palacios Romero,
Justo Fabián Montiel Hernández,
Sergio Hernández León and
Pablo Antonio López Pérez
Index .........................................................................................149
Preface

This book contains five chapters that detail weevils. Chapter One discusses
the current state of knowledge regarding the use of agro-industrial waste to
produce the fungal biomass of entomopathogenic fungi, and its use for the
biological control of pests, the production of enzymes of industrial interest,
and various chemical compounds with high added value. Chapter Two
investigates the mobilization of reserves during the embryogenesis of
C.maculatus. Chapter Three considers the issue of biocontrol exerted by toxins
from various microorganisms on insect species considered important pests for
agriculture. Chapter Four conducts a review of pest-weevil growth models to
predict and analyze the pests’ behavior under different ecological sets of
conditions. Lastly, Chapter Five aims to show in a synthesised, clear and
precise way the relevant information on the species Sitophilus oryzae to help
researchers and decision-makers to better understand this pest.
Chapter 1

Circular Economy in the Production of

Entomopathogenic Fungi for Enzyme
Production and Biological Control of
Insect Pests

Emma O. Fuentes-Ramírez1, PhD

Rafael Uzárraga-Salazar2, PhD
Caliope Mendarte-Alquisira3, PhD
and Gabriel R. Hernández-Martínez2,∗, PhD
1Secretaríade Educación Pública. Subsecretaría de Educación Media Superior,
CDMX, México
2Universidad Veracruzana. Facultad de Ciencias Químicas, Orizaba, Veracruz, México
3Colegio de Postgraduados, Posgrado en Edafología, Microbiología de Suelos,

Campus Montecillo, Texcoco, Estado de México, México

Abstract
Agro-industrial waste has increased exponentially in recent years owing
to the growing demand for food and common-use products caused by the
increase in the world population. These wastes have the potential to be
used as a source of biomass for bioenergy generation; however, only a
small amount of this waste has been used for this purpose, and these
residues also represent a major source of pollution for the environment
and human health. Therefore, there is an urgent need to develop different
circular economy approaches to treat and convert agro-industrial waste
into value-added goods. This chapter discusses the current state of
knowledge regarding the use of agro-industrial waste to produce fungal

∗
Corresponding Author’s Email: [email protected]; [email protected].

In: Weevils
Editor: Charlie B. Morris
ISBN: 979-8-89113-292-4
© 2024 Nova Science Publishers, Inc.
2 E. O. Fuentes-Ramírez, R. Uzarraga-Salazar, C. Mendarte-Alquisira et al.

biomass of entomopathogenic fungi and its use for the biological control
of pests, the production of enzymes of industrial interest, and various
chemical compounds with high added value. Finally, we discuss the
challenges and opportunities of using fungal biomass as a platform to
manufacture different value-added products.

Keywords: insect pest, biocontrol, enzyme production, agro-industrial waste,

circular economy

Circular Economy of Agro-Industrial Waste: Current Status

The increasing world population has generated a growing demand for food for
both humans and livestock; therefore, the agroindustry has substantially grown
throughout the twentieth century (FAO 2009). That increment also generated
an excess of by-products, which later became agro-industrial waste. It is
estimated that approximately 1.3 billion metric tons of agriculture products
are generated for human consumption, and one-third of them remain as agro-
industrial waste, mainly consisting of bagasse, peels, and fruit pulp residues,
among others (Yafetto et al., 2023; Lima et al., 2018). Of these, a large amount
is composed of lignocellulosic biomass from wheat straw, corn stalks, and
other carbon-rich materials (Bajpai, 2016).
Research has been carried out to utilize and dispose of agro-industrial
waste, adopting a circular economy approach in which the reduction of waste
generated and the maximization of the value-added of materials extracted from
the waste are essential through recycling, reusing, and repurposing.
Biorefinery is one of the key examples of this, in which waste is transformed
into different valuable products such as biofuels, biochemicals, bioplastics,
and biofertilizers. This not only reduces the environmental impact of waste
disposal but also creates economic opportunities and promotes a more
sustainable and resource-efficient system (Policastro et al., 2022).
The key characteristic of agro-industrial waste is its biodegradability due
to its composition, mainly of lignocellulosic material. Lignocellulose makes
up the plant cell wall and is a complex mixture of lignin and carbohydrates,
with an average composition primarily consisting of cellulose (30–50%),
hemicellulose (15–35%), and lignin (10–30%). The high degree of structural
organization and interaction between these polymeric structures gives the
plant cell wall high resistance to chemical, physical, and biological
degradation (Chen et al., 2017; Delidovich et al., 2015). Cellulose, the most
abundant polymer in nature, is a linear polymer composed of D-glucose
 Circular Economy in the Production of Entomopathogenic Fungi … 3

molecules linked by β-1,4 glycosidic bonds, forming microfibrils held

together by hydrogen bonds and van der Waals forces. In plants, cellulose
exists in two forms: a crystalline form (resistant to hydrolysis) and an
amorphous form (susceptible to enzymatic degradation) (Bajpai, 2016).
Hemicellulose is a short polymer consisting of pentoses such as D-xylose, L-
arabinose, and hexoses (D-glucose, D-mannose, and D-galactose). These
monosaccharides are linked by β-1,4 glucosidic bonds and occasionally by β-
1,3 bonds (Cuervo et al., 2009). The branched and amorphous nature of
hemicellulose allows it to be more easily hydrolyzed compared to cellulose
(Balat, 2011). Lignin is composed mainly of three structural units: p-
hydroxyphenyl, guaiacyl, and syringyl. Lignin is part of the plant cell wall,
providing resistance to microbial attack and oxidative stress due to its being
an amorphous phenolic polymer (Quílez-Bermejo et al., 2022).
Due to the lignocellulosic composition of many agro-industrial wastes,
such as those derived from sugarcane, corn, wheat, rice, soybeans, tomatoes,
and other crops, they can be used as an energy source. The estimated global
production of these residues in 2020 was approximately 189.1, 2324.8, 897.9,
756.7, 530.3, and 653.3 million metric tons, respectively (Oleszek et al.,
2023). By harnessing these waste materials through bioenergy production,
useful renewable energy can be generated while reducing reliance on fossil
fuels and mitigating greenhouse gas emissions, which is one of the positive
impacts of the circular economy.
Furthermore, agro-industrial waste can be used to obtain various
compounds of economic interest or be added to products for human
consumption, providing health benefits. For example, apple pomace is mainly
composed of carbohydrates, phenols, flavonoids, anthocyanins, and
triterpenoids, among others, and could potentially be used in bioprocesses for
enzyme production (cellulase, amylase) or obtaining compounds with
biological activity, such as prebiotics, antimicrobials, anti-inflammatory
agents, etc. Additionally, this waste could also be utilized in the production of
bakery products, meat products, or alcoholic beverages (Fernandes et al.
2019). Another example is rice bran, which contains carbohydrates, proteins,
fiber, lipids, and various compounds such as B-complex vitamins, caffeic acid,
cycloartenol ferulate, ferulic acid, and γ-oryzanol, which exhibit anticancer
activities, prevent chronic diseases, reduce cholesterol levels, help lower blood
pressure in humans, and reduce the risk of heart diseases. Rice bran can add
value to various bakery products by reducing fat content and increasing fiber
content (Sohail et al. 2017). It also serves as an energy source in bioprocesses
for producing enzymes such as glucoamylase, protease, and amylase (Naik et
4 E. O. Fuentes-Ramírez, R. Uzarraga-Salazar, C. Mendarte-Alquisira et al.

al., 2023). Incorporating these waste materials into the production processes
of different industries promotes the use of resources that would otherwise
become waste, reduces the reliance on virgin materials, and minimizes the
environmental footprint, which is one of the goals of the circular economy.
Agro-industrial wastes have great potential not only for obtaining
essential compounds for various productive sectors or as raw materials in
bioprocesses to obtain valuable bioproducts, but also for promoting a more
sustainable economy and making companies or industries more competitive
and environmentally friendly (Souza et al., 2022). Hence, by adopting circular
economy fundamentals and leveraging the value embedded in these waste
materials, we can create a more efficient and resilient agricultural system that
minimizes waste, reduces environmental impact, and fosters economic
growth.

Entomopathogenic Fungi Production from

Agro-Industrial Waste

One of the biggest concerns in agriculture is the extensive use of pesticides,

which have a series of disadvantages, such as the contamination of liquid,
gaseous, and solid media, with consequent effects on the ecosystems in which
they are disposed of, including damage to human health (Hassaan and El
Nemr, 2020). Owing to the need to reduce and/or substitute chemical
pesticides, it has been proposed to use entomopathogenic fungi, which have
been produced since their effectiveness against certain species of insects has
been proven (Lacey, 2017).
The production of entomopathogenic fungi depends on three important
factors: the efficacy of the pathogenicity of the cultured fungi, the production
of spores, and the reduction in costs generated during the bioprocess (Mishra
et al., 2016). Several authors have evaluated and optimized the production of
different species of entomopathogenic fungi using different agro-industrial
wastes as substrates under different types of fermentation: solid, liquid, or
biphasic (Sala et al., 2019; Pilafidis et al., 2022). One of the main reasons for
this is the reduction in production costs, but also because these wastes are a
source of carbon with a high composition of lignocellulosic material (Pilafidis
et al., 2022), which is easily metabolized by fungi (Dhiman et al., 2015;
Shirkavand et al., 2016).
 Circular Economy in the Production of Entomopathogenic Fungi … 5

Beauveria bassiana is one of the first entomopathogenic fungi to be

cultivated on a large scale in submerged fermentation (SmF) and later in
biphasic fermentation (Feng et al., 1994). Following this large-scale
production model, other species have been evaluated in SmF, mainly at the
laboratory scale (Abu-Laban and Saleh, 1992); however, since the 21st
century, solid-state fermentation (SSF) has been developed to cultivate
different species of entomopathogenic fungi (Dalla Santa et al., 2004; Tarocco
et al., 2005; Moslim et al., 2005; Ye et al., 2006; Cavalcante et al., 2007; Pham
et al., 2010; Omwango et al., 2013; Xie et al., 2012; Zhang and Yang, 2015).
Submerged fermentations have advantages mainly concerning mass transfer
and optimal mixing of nutrients in the culture medium, as well as precise
control of different parameters such as temperature (Pilafidis et al., 2022).
However, there are several disadvantages, particularly due to the nature of the
fungi, where mixing and agitation produce shear stress that negatively affects
mycelial growth. Furthermore, the use of large amounts of water and energy
implies higher process costs, which are not required in SSF (Pilafidis et al.,
2022).
Agro-industrial residues and their properties are diverse due to the
chemical composition of each residue as well as variations due to the
geographical location where they are obtained, the climate, and the seasons of
the year (Pilafidis et al., 2022). Therefore, it is necessary to carry out
pretreatments to confer homogeneous characteristics that favor fermentation
under optimal and standardized parameters for each fungal species.
Pretreatments seek to favor the increase of the substrate-mushroom contact
surface, the nutritional enrichment of the substrate, the level of acidity, the
percentage of humidity, and the elimination of substances that may be
contaminants in the substrate, among other properties that favor the easy
assimilation of the substrate and standardization of fermentation (Sala et al.,
2019). The cultivation of entomopathogenic fungi with agro-industrial
residues as a base substrate has provided good results, and some authors have
reported that compared with conventional culture media such as Potato
Dextrose Broth (PDB), it has increased fungal biomass production and spore
production (Leena et al., 2003). This may be due to the easy metabolization of
lignocellulosic material as well as the nutritional content of agro-industrial
residues, which are abundant in cellulose, hemicellulose, and lignin, as well
as proteins, mineral salts, and vitamins (Santa et al., 2005; Pilafidis et al.,
2022), making them nutritionally valuable substrates for fungal cultivation.
Agro-industrial wastes that have been used as substrates vary greatly,
including sugarcane industry wastes such as molasses and bagasse, coconut
6 E. O. Fuentes-Ramírez, R. Uzarraga-Salazar, C. Mendarte-Alquisira et al.

oil cakes, cottonseed, coffee husks, rice, wheat, corn, sorghum, lentils,
cassava, pineapple residues, tea leaf residues, straw, barley, malt, and animal
products, such as whey and manure from cows, chickens, and sheep (Leena et
al., 2003; Santa et al., 2005; Cavalcante et al., 2007; Robl et al., 2009;
Machado et al., 2010; Omwango et al., 2013; Mishra and Sundari, 2017; Abu-
Laban and Saleh, 1992). Table 1 lists the different types of substrates that have
been used to grow different species of entomopathogenic fungi.

Table 1. Types of substrates that have been used to grow different species of
entomopathogenic fungi, and the different mode of fermentation

Entomopathogenic Agro-industrial wastes Fermentation References

fungus process
Paecilomyces lilacinus Chicken, cow, and sheep SSF (flask) Abu-Laban and
manures Saleh, (1992)
Paecilomyces farinosus Oil cakes: coconut, cotton SSF and SmF Leena,
seed, gingelly, groundnut, (conical flask) Easwaramoorthy
neem. and Nirmala,
(2003)
Paecilomyces farinosus Molasses, Spent wash, SSF (petri plate) Leena,
Bagasse from sugar and SmF (conical Easwaramoorthy
industry. flask) and Nirmala,
(2003)
Paecilomyces farinosus Tapioca rind from sago SSF (petri plate) Leena,
(Hotmskiold) industry, coconut water and SmF Easwaramoorthy
from copra industry, (conical flask) and Nirmala,
pressmud from sugar (2003)
industry
Paecilomyces lilacinus Refuse-potato, SSF (petri Robl et al. (2009)
cassava bagasse, rye, dishes)
barley, wheat, soy and
coffee husks
Beauveria bassiana Tea leaf waste, wheat SSF (Erlenmeyer Mishra et al.
bran, husk of rice, pigeon flasks) (2016)
pea and urad, seed cake
of jatropha and
pongamia.
Beauveria bassiana Rice SSF (tray Xie et al. (2012)
bioreactor)
Beauveria bassiana Cheese whey SSF and SmF Kassa et al. (2008)
Beauveria bassiana Refused potatoes and SSF (Erlenmeyer Dalla Santa et al.
sugar-cane bagasse (60– flasks) and SmF (2004)
40%) (column-type
bioreactor)
Beauveria bassiana Refused potatoes, coffee SSF (Erlenmeyer Santa et al. (2005)
husks, sugar cane bagasse flasks)
 Circular Economy in the Production of Entomopathogenic Fungi … 7

Entomopathogenic Agro-industrial wastes Fermentation References

fungus process
Beauveria bassiana A blend of refused SmF (column Santa et al. (2005)
potatoes and sugar-cane type bioreactor)
bagasse (60-40%)
Beauveria bassiana Rice, algaroba, malt SSF (Erlenmeyer Paiva-Guimarães
flasks) et al. (2020)
Entomopathogenic Agro-industrial wastes Fermentation References
fungus process
Beauveria bassiana Rice husk, beer draff SSF (packed-bed Sala et al., (2023)
bioreactors)
Trichoderma Rice, corn bran, wheat SSF (Erlenmeyer Cavalcante et al.
harzanium bran flasks) (2007)
Trichoderma viride. Rice, corn bran, wheat SSF (Erlenmeyer Cavalcante et al.
bran flasks) (2007)
Trichoderma Rice, corn bran, wheat SSF (Erlenmeyer Cavalcante et al.
koningii bran flasks) (2007)
Trichoderma Rice, corn bran, wheat SSF (Erlenmeyer Cavalcante et al.
polysporum bran flasks) (2007)
Trichoderma viride Pineapple waste SSF (beakers) Omwango et al.
(2013)
Trichoderma Straw and wheat bran SSF (bottles and Zhang and Yang
harzianum conical flasks) (2015)
Trichoderma Different combinations of SSF (jam bottels) Mishra and
harzianum wheat straw, wheat bran Sundari (2017)
and wheat grain
Lecanicillium lecanii Molasses, wheat, Biphasic culture. Machado et al.
sorghum, lentils, (2010)
milhocina, cheese whey,
cassava.
Lecanicillium lecanii Liquid media obtained Biphasic culture. Machado et al.
from agro‑industrial (2010)
residues and by‑products
Lecanicillium lecanii Solid media prepared Biphasic culture. Machado et al.
with mixtures of grains (2010)
and their derivatives
Fusarium oxysporum Chicken, cow, and sheep SSF (flask) Abu-Laban and
manures Saleh, (1992)
Fusarium solani Chicken, cow, and sheep SSF (flask) Abu-Laban and
manures Saleh, (1992)
Metarhizium anisopliae Cheese whey SSF, SmF and Kassa et al. (2008)
biphasic
production
system.
Aspergillun niger Pineapple waste SSF (beakers) Omwango et al.
(2013)
Microascus Chicken, cow, and sheep SSF (flask) Abu-Laban and
triganosporus manures Saleh, (1992)
Phoma leveillei Chicken, cow, and sheep SSF (flask) Abu-Laban and
manures Saleh, (1992)
8 E. O. Fuentes-Ramírez, R. Uzarraga-Salazar, C. Mendarte-Alquisira et al.

Table 1. (Continued)

Entomopathogenic Agro-industrial wastes Fermentation References

fungus process
Isaria javanica Barley, white rice, and SSF (baffled Xie et al. (2015)
brown rice. flasks)
Acremonium Chicken, cow, and sheep SSF (flask) Abu-Laban and
sclerotignum manures Saleh, (1992)

On the other hand, it is important to mention that solid substrates of plant

origin, which are not agro-industrial waste, have been effective in the
production of entomopathogenic fungi, such as rice, corn, sorghum, and wheat
grains (Tarocco et al., 2005; Moslim et al., 2005; Ye et al., 2006; Prakash et
al., 2008; Nuñez-Gaona et al., 2010; Pham et al., 2010). This gives them
several advantages, such as eliminating steps in the substrate pretreatment.
However, they are costlier to remove from the food chain and acquire the
prices at which they are sold in the grain market.

Integrative Utilization of Entomopathogenic Fungi

The use of entomopathogenic fungus to manufacture chemical compounds

with high added value could be a viable option for the sustainable use of
biomass from agro-industrial waste. Entomopathogenic fungi can produce a
wide range of industrially important enzymes, including proteases, chitinases,
xylanases, cellulases, and lipases, which can be employed in a variety of
industries, including bakery, paper, cattle, agrochemicals, and textiles, among
others. Entomopathogenic fungi also produce spores, toxins, or blastospores
that can be employed in agricultural pest management. Furthermore, these
fungi produce a vast array of secondary metabolites such as organic acids,
terpenes, cyclic depsipeptides, peptaibols, and polyketides, which can be
employed in the food, pharmaceutical, biomedical, and agrichemical
industries, among others.
Figure 1 shows a general outline of the use of entomopathogenic fungi to
produce value-added goods based on the integration of agro-industrial waste
as a substrate, which contributes to zero waste policy, one of the principles of
the circular economy (Chiaraluce, Bentivoglio, and Finco, 2021). Following,
it is described the production of value-added chemicals by entomopathogenic
fungi.
 Circular Economy in the Production of Entomopathogenic Fungi … 9

Figure 1. Agroindustrial waste management through circular economy for the

generation of value-added goods and biomass for biological pest control.

Biological Control of Insects by Entomopathogenic Fungi

The intensive use of agriculture has resulted in a constant need to control pests,
which have a direct impact on the yield and quality of production of all
agricultural crops. Today, many strategies are employed to meet this need,
such as the use of various chemical compounds and biological agents or a
combination of these (Mantzoukas and Eliopoulos, 2020). However, due to
the problems that chemical products cause for the environment and human
health, it is necessary to reduce them. In addition to the foregoing, pests
frequently develop resistance to chemical compounds, requiring the continual
search for new chemical compounds that allow pest management (Tudi et al.,
2021). Therefore, sustainable management of crop production is necessary.
One of the alternatives for pest control is the use of biological agents.
Biological control of insect pests is defined as the use of biological agents
that can cause severe damage or death to insects due to the persistent growth
of pathogenic microorganisms or the segregation of various chemical
substances that inhibit the growth of insects. Biological insect control agents
used to date include viruses, bacteria, protozoa, nematodes, and fungi.
However, today, entomopathogenic fungi are the most widely used
microorganisms for insect control due to the wide spectrum of insects on
which they can act, greater biomass production, and the ability to grow on
agro-industrial waste that they use as carbon and energy sources. (Samada and
10 E. O. Fuentes-Ramírez, R. Uzarraga-Salazar, C. Mendarte-Alquisira et al.

Tambunan, 2020). There is a difference in the capabilities to infect different

arthropods by fungi, that depends directly on the type of host-host interaction;
while some fungi are obligate pathogens, i.e., they completely depend on the
nutrients provided by the host, other fungi are facultative, i.e., their nutritional
requirements are determined by them (Lacey et al., 2015; Stenberg et al.,
2021). This difference in infection capabilities determines the specificity of
biological control by fungi.
The infection cycle of entomopathogenic fungi can occur through
different infectious stages of the fungus, such as spores, mycelia pellets, or
inert granules that contain the propagules of the fungus (Stenberg et al., 2021).
The first step is for the infectious agent to come into contact with the surface
of the insects. If the conditions are adequate, the fungus will germinate and
penetrate the insect cuticle. Subsequently, the fungus will go through its
exoskeleton due to the growth of the hyphae until it reaches a place rich in
nutrients called hemolymph. In the hemolymph, the fungus changes its cellular
reproduction from hyphal growth to the formation of yeast-like unicellular
structures called blastospores (sexual reproduction). The blastospores are able
to colonize all the tissues of the insects, taking advantage of the abundance of
nutrients, because they can evade the immune system of the insects and
produce toxins in the environment, which leads to a successful colonization of
the fungus and therefore to the death of the host. After the death of the insect,
the vegetative bodies of the fungus are formed, which gives rise to the
formation of new hyphae and the formation of new conidiophores. Finally, the
reproductive cycle of the fungus restarts with the formation of new conidia
that generate the spores of the fungus that are disseminated in the environment
(Mascarin and Jaronski, 2016; Valero-Jiménez et al., 2014).
The entomopathogenic fungi that are used for the biological control of
insect pests belong to the phylum Oomycota, Ascomycota,
Entomophthoromycota, and Zygomycota; among the best known are
Beauveria bassiana, Metarhizium, Isaria fumosorosea, Purpureocillium
lilacinum, Myrothecium verrucaria, and Paranosema locustae, among others.
Most of them have a saprophytic lifestyle, which allows them to grow in
various environments (different types of substrates) and have a high growth
rate of fungal biomass, which reduces the production costs of fungi. In
addition, entomopathogenic fungi are preferred for insect control compared to
chemical compounds because they are considered environmentally friendly,
biopersistent, do not generate resistance on the part of the hosts, do not
generate toxic by-products for the environment, are compatible with other pest
control strategies, and are considered natural enemies of insects (Lacey, 2017).
 Circular Economy in the Production of Entomopathogenic Fungi … 11

The main insect pests that entomopathogenic fungi can control are the orders
Diptera, Coleoptera, Hymenoptera, Lepidoptera, Diptera, Hymenoptera,
Homoptera, and others. In Table 2 are described some entomopathogenic
fungi tested for agriculture application.

Table 2. Entomopathogenic fungi tested to control insect pests

Fungus species Target insect % mortality Number of References

spores/exposure
time.
Beauveria Dendrolimus ⁓90 1.58x106 conids/mL Kovač, Lacković
bassiana pini in 9.4 days of and Pernek,
exposure. (2020)
Beauveria Leptinotarsa 87.3 1.58x108 conids/mL Idrees et al.
bassiana decemlineata in 9.4 days of (2022)
exposure.
Beauveria Uvarovistia 57.7 1.58x106 conids/mL Mohammadbeigi
bassiana zebra in 2 days of and Port (2015)
exposure.
Beauveria Thaumatotibia 100 1x108 conids/mL in Mondaca et al.
bassiana leucotreta 7 days of exposure. (2020)
Metarhizium Uvarovistia 55.5 1.58x106 conids/mL Mohammadbeigi
anisopliae zebra in 2 days of and Port (2015)
exposure.
Metarhizium Tetranychus 70 1x107 conids/mL in Bugeme et al.
anisopliae urticae 10 days of exposure. (2008)
Metarhizium Curculio 100 2.0 x102 Ihara et al.
anisopliae sikkimensis conids/larva in 10 (2003)
weeks
Metarhizium Thaumatotibia 100 1x108 conids/mL in Mondaca et al.
brunneum leucotreta 14 days of exposure. (2020)
Metarhizium Anthonomus 90 7.70 x107 Nussenbaum and
anisopliae grandis conids/mL in 5 days Lecuona (2012)
of exposure.
Isaria Leptinotarsa 92 1.58x108 Hussein et al.
fumosorosea decemlineata blastospores/mL in (2016)
7 days of exposure.
Isaria Plutella 84.4 - 86.6 1x109 conids/mL in Nian et al.
fumosorosea & xylostella 14 days of exposure. (2015)
Bacillus
thuringiensis
Lecanicilliumes Aphis gossypii 100 1x108 conids/mL in Kim and Roberts
lecanii 4 days of exposure. (2012)
Lecanicilliumes Tuta absoluta 100 1x103 conids/mL in Abdel-Raheem et
lecanii 3 days of exposure. al. (2020)
Lecanicilliumes Bactrocera 90 1x103 hasta 1x108 Iqbal et al.
lecanii cucurbitae CFU/mL days of (2020)
exposure.
12 E. O. Fuentes-Ramírez, R. Uzarraga-Salazar, C. Mendarte-Alquisira et al.

Beauveria Genus
Beauveria is a genus of fungi that are facultative saprophytes with the ability
to infect a very wide range of arthropods, including insects, mites, and ticks.
These fungi can be found all over the world, and their natural habitat is the
soil, hence, Beauveria is the entomopathogenic fungus with the most isolated
strains around the world, and some of the most reported strains are Beauveria
amorpha, Beauveria caledonica, Beauveria bassiana, and Beauveria
brongniartii (Zimmermann, 2007).
B. bassiana is the entomopathogenic fungus with the widest spectrum for
controlling insect pests. It has been tested for controlling the pine-eared moth
(Dendrolimus pini) larvae, which have a 90% mortality rate with a B. bassiana
concentration of 1.58x106 conids/ml after 9.4 days of exposure (Kovač,
Lacković, and Pernek, 2020). Idrees et al. (2022) tested the control of
Spodoptera frugiperda, which is an important pest in maize, and found that a
concentration of 1x108 conidia/mL results in mortality percentages of insect
eggs of 87.3% after 7 days of exposure. Mondaca et al. (2020) reported that a
concentration of 1x108 conidia/ml in 7 days of exposure could achieve 100%
mortality of Thaumatotibia leucotreta, which is a moth that affects the tree
apple.

Isaria Genus
The genus Isaria, formerly known as Paecilomyces, is a genus that belongs to
the phylum Deuteromycota with two species of relevance in biological
control, Isaria fumosorosea and Paecilomyces lilacinus. It is widely
distributed in the world, including tropical and temperate zones, which makes
it ideal for use in biological control. The infectious agents of these fungi are
spores and blastospores. The morphology of these fungi is characterized by
presenting conidiophores that develop synnematous, septate and with
divergent branches, and filiated cells (Zimmermann, 2008).
Isaria can control economically important insect pests, for example,
Leptinotarsa decemlineata, which is an important pest of the Colorado potato,
can be controlled by Isaria fumosorosea at a concentration of ⁓1.58x108
blastospores/ml in 7 days, resulting in a beetle mortality rate of 92% (Hussein
et al., 2016). The cabbage moth (Plutella xylostella), which is a pest that
generates economic losses in crops of up to 1 billion dollars annually
worldwide, can be controlled by a combination of Isaria fumosorosea and
Bacillus thuringiensis, resulting in larval mortality between 84.4 and 86.6%
and a growth rate of adult moths between 7.0 and 8.7% (Nian et al., 2015).
 Circular Economy in the Production of Entomopathogenic Fungi … 13

Metarhizium Genus
The genus Metarhizium belongs to the phylum Ascomycota, with a worldwide
distribution usually in the soil. This genus has three important species that
have been used for biological control: Metarhizium album, Metarhizium
anisopliae, and Metarhizium flavoviride (Brunner-Mendoza et al., 2018). The
genus Metarhizium presents a morphology consisting of branched
conidiophores containing rounded apices with truncated or elongated
phialides.
Both spores and blastospores are used in different formulations as agents
against different insect pests. Mondaca et al. (2020) used Metarhizium
brunneum to control the codling moth (Thaumatotibia leucotreta), and with a
concentration of 1x108 conids/ml in 7 days of exposure, they achieved 100%
mortality of the moth. Bugeme et al. (2009) used different extracts of
Metarhizium anisopliae isolated from the soil against the two-spotted spider
(Tetranychus urticae), which is one of the most important pests of different
crops in the world. They reported that M. anisopliae was capable of infecting
T. urticae with a mortality greater than 70% in all treatments (different
temperatures and different isolated strains), after 10 days of exposure using a
concentration of 1 x107 conids/ mL. Ihara et al. (2003) tested M. anisopliae
against the weevil Curculio sikkimensis, which is an important pest of
chestnuts, and reported a mortality rate of 100% after 10 weeks of exposure
with a concentration of 2.0 x105 conidia/larva. M. anisopliae can control the
Anthonomus grandis weevil, which is the most important pest reported for the
cotton crop. It has been reported a mortality rate of 90% above an IC50 of 1.20
x107 conidia/ml and IC90 of 7.70 x107 conidia/ml, during 20 days of evaluation
(Nussenbaum and Lecuona, 2012).

Lecanicillium Genus
The genus Lecanicilliumes is an important group of entomopathogenic fungi
of the phylum Hyphomycetes that have been shown to infect different orders
of insects such as Lepidoptera, Homoptera, Diptera, and Hymenoptera. This
genus of fungi was previously known as Verticillium. They have two relevant
species for the biological control of pests: Lecanicilliumes lecanii and
Lecanicilliumes chlamydosporium. Like the previous genera, this group of
fungi can be found in a wide variety of climates and regions of the world,
including hot, humid, and tropical regions (AlAVO, 2015). This genus of
fungi is characterized by lacking sexual reproduction, and its form of
reproduction is through spores (asexual reproduction). In addition, it presents
the morphology of branched, whorl-type conidiophores (AlAVO, 2015).
14 E. O. Fuentes-Ramírez, R. Uzarraga-Salazar, C. Mendarte-Alquisira et al.

Lecanicilliumes lecanii has been tested to control the cotton aphid, Aphis
gossypii, which is one of the most important pests of cucumber, squash, and
tomato worldwide. Under a spore concentration of 1x108 conidia/ml, aphids
presented 100% mortality in 3rd instar nymphs and adults of the insect after 4
days of exposure to the fungus, while the first instar nymphs of the insect were
observed to have 100% mortality after 7 days. The median lethality time
(LT50) was 2.7, 2.9, and 5.4 days for the 1st instar, 3rd instar, and adults,
respectively (Kim and Roberts, 2012). Abdel-Raheem et al. (2020) reported a
mortality of Tuta absoluta (an insect pest of tomato leaves) of 100% when
applying 1x103 spores/mL in 3 days of exposure to Lecanicilliumes lecanii.
They reported an LC50 of 0.18 x101 and 0.22x102 spores/ml for the 1st and 3rd
instars of the Tuta absoluta nymph, respectively. L. lecanii can also control
the melon midge (Bactrocera cucurbitae) with a fungus concentration of
1x108 CFU/mL. The mortality rate observed was 90% after 10 days of
exposure. Authors reported an IC50 of 4.50 x102 to 7.64 x102 CFU/mL (Iqbal
et al., 2021).

Enzyme Production by Entomopathogenic Fungi

Entomopathogenic fungi have the capability to produce several extracellular

enzymes, which are associated with the fungus ability to degrade complex
polymers (sugars and proteins) and complex lipids (Chavan and Deshpande,
2013; Ulhoa and Peberdy, 1993). Entomopathogenic fungi can grow on low-
cost substrates like agro-industrial waste, have simple enzyme recovery, and
do not require additional supplements for optimal growth; therefore, they are
a promising source of enzyme production. Xylanases, lipases, proteases,
cellulases (endoglucanase and exoglucanase), and chitinases are among the
most important enzymes generated by entomopathogenic fungi (Butt et al.,
2016). The demand for enzymes worldwide has increased significantly due to
many industrial uses such as textile, paper, pharmaceutical, agro-industrial,
tanning, and livestock. According to BCC (2018), the global enzyme market
was valued at $5.5 billion in 2018 and is expected to reach $7.0 billion by the
end of 2023. These enzymes are produced by fungi such as Verticillium
lecanii, Beauveria bassiana, Metarhizium anisopliae, Trichoderma
harzianum, Isaria fumosorosea (formely Paecilomyces fumosoroseus),
Penicillium sp., and Lecanicillium sp. However, based on enzyme production,
B. bassiana and M. anisopliae are regarded as the two most well-known and
prominent entomopathogens (Moran-Aguilar et al., 2021; Mondal et al.,
 Circular Economy in the Production of Entomopathogenic Fungi … 15

2016). The production of enzymes from entomopathogenic fungi is carried out

by two methods: solid-state fermentation (SSF) and submerged fermentation
(SmF). While the SSF does not require significant energy investment or water
consumption, the SmF does. However, in both methods, agro-industrial waste
can be used to produce enzymes. (Chilakamarry et al., 2022). Different cases
of enzyme production from entomotopathogenic fungi are described below,
with emphasis on the use of agro-industrial residues.

Proteases
Proteases (EC 3.4) are a class of hydrolase proteins that break peptidic bonds
in proteins and regulate several physiological processes such as hormone
control, protein returnover, and differentiation, among others. Microbial
proteases are very active across a broad pH range (pH 4 to 10). Proteases are
classified into seven groups based on the presence of functional groups and
the position of peptide bonds: cysteine proteases (using a cysteine thiol), serine
proteases (using serine alcohol), glutamic proteases (using glutamate
carboxylic acid), metalloproteases (using a metal, typically zinc), aspartic
proteases (using an aspartate carboxylic acid), asparagine peptide lyases
(using asparagine), and threonine proteases (using threonine secondary
alcohol) (Harrison and Bonning 2010, Razzaq et al., 2019). Proteases are
possible natural pesticide options since they are harmful to insects when
expressed by microorganisms (Harrison and Bonning 2010). Microbial
proteases are the most commercially utilized enzymes in the world, and they
may be generated in great quantities in a short period of time by submerged
(SmF) and solid-state fermentation (SSF) with various carbon sources (Razzaq
et al., 2019). Regarding the above, Fernandes et al. (2012) assessed the ability
of Metarhizium anisopliae GC 312, Beauveria bassiana CG 470, and
Paecilomyces sp. CG 301 to produce proteases in SmF in a culture medium
supplemented with 4% and 1% of gelatin with or without 0.1% of glucose,
larval cuticles, and adults of Musca domestica. The highest amount of protease
produced was by M. anisopliae, followed by Paecilomyces sp. and B. bassiana
in a medium without glucose after 7 days of culture. On the other hand, using
10 g/L of various agro-industrial products (wheat bran, black gram peels,
green gram peels, horse gram peels, and gram peels), Trichoderma
longibrachiatum and Penicillium rubidurum were able to produce alkaline
proteases (233.78±7.12 U/mg and 228.61±11.13 U/mg, respectively) with
stability at 40°C and pH 9.0 and 8.0, in a period of 4 days (Behera et al., 2021).
Proteases of T. harzianum GIM 3.442 were produced using cloning of the E.
coli DH5α strain grown in the buffered minimum methanol-complex medium
16 E. O. Fuentes-Ramírez, R. Uzarraga-Salazar, C. Mendarte-Alquisira et al.

at 30 °C and 200 rpm for five days. The resulting protease (designated rP6281)
was characterized, the protease had high catalytic activity at pH 2.5 and 40 °C
as well as high relative activity in the presence of the metal ions Mn2+ and
Cu2+ (140.1 ± 2.6% and 151.2 ± 2.6%, respectively); this protease was not
metal ion-dependent, and its enzyme activity corresponded to an aspartic
protease (Deng et al., 2018). B. bassiana AAUEB-59 can produce high
enzymatic protease activity (enzyme index = 5.44) when cultured in SmF
containing olive oil at 2% and (NH4)2SO4 (Gebremariam et al., 2022). When
B. bassiana isolated are cultivated SmF in a medium containing 0.01% (w/v)
of yeast extract and 10 g of P. interpunctella larval cuticle, they produce a
high level of specific protease (0.654 U/mg protein) when cultured in SmF
(Reyhaneh et al., 2023). The genes that encode proteases respond to the
presence of the cuticle, are suppressed by readily catabolizable nitrogen and
carbon sources, and in some cases require inducers to develop in the medium
(Harrison and Bonning 2010). An approach for producing these enzymes is
genetic modification to overexpress proteases.

Lipases
Lipases (EC 3.1.1.3) are hydrolases that catalyze the transformation of long-
chain triglycerides to release carboxyl ester and glycerol as well as other
biotechnological applications such as detergent manufacturing, bakery flavor
enhancement, and the production of chemicals linked to it (Chandra et al.,
2020 After proteases and amylases, lipases are the third most significant
enzymes used (Yao et al., 2021). Lipases are classified into three types based
on their substrate specificity and location: 1) non-specific lipases, 2) 1,3-
specific lipases, and 3) fatty acid-specific lipases (Yao et al., 2021). Lipases,
like cellulases and chitinases, are involved in the destruction of phytopathogen
insect cuticles (Singh and Arya 2019). Lipase production was valued at USD
340 million in 2020 and is expected to reach USD 494.7 million in 2026
(Szymczak et al., 2021). The production of lipases has been done in SSF using
agro-industrial waste as support (rice hulls, corn cob, banana stalk, Wodyetia
bifurcata A. K., Irvine leaves, coconut husks, and Salacca wallichiana stem,
among others) or substrate (cassava peel, wheat bran, barley spent grain, citrus
pulp, sugarcane bagasse, and so on). For example, the Acinetobacter baylyi
strain produces high lipase activity (3.32 U/g) with high immobilization
efficiency of lipases (96.49%) using Salacca wallichiana stem as support
(Ittrat et al., 2014). In SSF, Trichoderma asperellum TF1 produces a high level
of lipase (30.6 ± 0.3 U/g) from a mixture of vine shoots, potato flour, jatropha,
olive pomace, and olive oil as carbon sources (Hamrouni et al., 2020).
 Circular Economy in the Production of Entomopathogenic Fungi … 17

Candida viswanathii was used to produce lipases in SSF using a variety of

agro-industrial wastes (cassava peel, wheat bran, barley spent grain, citrus
pulp, and sugarcane bagasse) and different nitrogen sources (yeast extract,
corn steep liquor, whey powder, soybean meal, soy protein, or cotton seed
protein). The highest lipase production was obtained using wheat bran plus
spent barley grain 1:1 (w/w) and supplemented with yeast extract. The
resulting lipase showed optimal activity at 50 °C and pH 5.0 (de Almeida et
al., 2016). Lima et al. (2021) reported that C. viswanathii strain was fermented
in SSF with agro-industrial residues such as soybean husk, corn straw, barley
bagasse, corn cob, and soybean husk added as well as an external nitrogen
source (casein, ammonium chloride, urea, and yeast extract) and olive oil
(40% m/v) as an inductor of lipases. The cultures were incubated at 30°C for
5 days, and the addition of the nitrogen source resulted in the maximum lipase
activity (17.88 U/g) (Lima et al., 2021). Yarrowia lipolytica, formerly known
as Candida lipolytica, is another lipase-producing strain that has been widely
employed in research. In solid fermentation, this strain may create large
volumes of lipases from a variety of carbon sources, including agro-industrial
waste. Its lipase activities have ideal pH and temperature ranges of 6–10 and
37–55 °C (Nascimento et al., 2022).

Xylanases
Xylanases (endo-β-1,4-xylanase, EC 3.2.1.8) are hemicellulases that break β-
1,4 bound present in the xylan backbone of hemicelluloses for successive
transformation to xylose fractions (Chadha et al., 2019). Most of the xylanases
produced by fungi can be grouped into the GH11 family. Xylanases are
involved in many biotechnology applications, including the paper and pulp
industry, digestibility improvement in animal feed, biofuel production, and the
bakery industry (Chadha et al., 2019). Microorganisms such as Trichoderma
harzianum PBLA can produce xylanases in SSF using pine sawdust as a solid
support impregnated with a culture medium added with glucose (50 g/L) as a
carbon source, with a maximum xylanase production of 107 ± 0.3 U/g dm
(Lopez-Ramirez et al., 2018). Paenibacillus campinasensis NTUS-11 can
produce thermostable xylanase in SmF with a specific activity of 2750 U/mg
and an optimal activity at 60°C and pH 7.0 (Wang et al., 2022).
Myveliophthora thermophila, Thermomyces lanuginosus, Malbranchea sp.,
Thermoascus aurantiacus, Scytalidium thermophilium, Geobacillus sp.,
Thermopolyspora flexuosa, and Caldicellulosiruptor are some more xylanase-
producing fungus. These microorganisms produce thermophilic xylanases
with a high specific activity ranging from 5.79 to 1923 U/mL min, with
18 E. O. Fuentes-Ramírez, R. Uzarraga-Salazar, C. Mendarte-Alquisira et al.

optimal activity at pH between 4.0 and 9.0 and a temperature range of 60–85
°C (Chadha et al., 2019). Aspergillus niger ITV-01, A. niger CECT 2700, and
A. niger CECT 2915 were used to produce xylanases in SSF from sugarcane
bagasse and brewery spent grain; the highest xylanase activity (1400.80 U/g)
was obtained using brewery spent grain with the A. niger CECT 2700 strain
(Moran-Aguilar et al., 2021). In SmF, B. bassiana SAN01 produced xylanase
with a specific activity of 324.2 U/mg and stability at pH 6.0 and 45°C
(Amobonye et al., 2020).

Cellulases
Cellulases are glycosyl hydrolases that degrade cellulose. In fungi, they are
divided into three main types: 1) endoglucanase (1,4-β-D-glucan
glucanhydrolase, EC 3.2.1.4); 2) exoglucanase (exo-β-glucanase, that include
1-4-β-D-glucan-glucohydrolases (EC 3.2.1.74) and 1,4-β-D-glucan-
cellobiohydrolases (EC 3.2.1.91); and 3) β-glucosidase or β-1,6-glucosidase
(EC 3.2.1.21). Endoglucanases (EGs) are globally marketed from fungi such
as Aspergillus, Trichoderma, and B. bassiana. These enzymes have a wide
range of biotechnological uses, including pulp and paper, laundry, textiles,
beer and wine, food, and animal feed (Bhat, 2000). EGs are the most important
cellulases, contributing to cellulase hydrolysis by randomly targeting internal
O-glucosidic bonds of cellulose, resulting in new reducing and non-reducing
ends of glucans (Bhat, 2000; Zou et al., 2021). EGs appear to be focused on
the most polymerized soluble cellulose, such as carboxymethylcellulose
(CMC), which yields glucose, cellobiose (disaccharide), and cellotriose
(trisaccharide), all of which are substrates for exoglucanases (Bhat, 2000).
Exoglucanases, conversely, are enzymes that gradually attack molecules that
are terminally non-reducing in cellulose, releasing cellobiose subunits.
Exoglucanases are not very active against crystalline cellulase but exhibit
highly cooperative synergistic action in the presence of endoglucanases.
Exoglucanases have limited action on cellulose substitutes such as CMC and
hydroxymethyl cellulose. In another way, β-glucosidase or β-1,6-glucosidase
is a glucosidase enzyme that attacks β-1-4 bonds in low molecular weight like
cellobiose and cellodextrines (cellotrioses and cellotetroses) to produce
glucose and catalyzes the hydrolysis of non-reducing terminal residues in β-
glucosides producing glucose (Jeng et al., 2011). Lopez-Ramirez et al. (2018)
obtained cellulases in SSF using T. harzianum. This study used agro-industrial
pine sawdust as a solid support and glucose as a carbon source, with a
maximum cellulase activity of 9.11 ± 0.13 U/g dm (Lopez-Ramirez et al.,
2018). Metarhizium anisopliae IBCB 348 was cultivated in SSF to produce
 Circular Economy in the Production of Entomopathogenic Fungi … 19

cellulases using different agro-industrial residues as substrates (malt bagasse,

corn steep liquor, sugarcane bagasse, and white rice), where sugarcane
bagasse was the most suitable substrate to produce endoglucanase and
exoglucanase with 20.87 ± 0.43 U/g and 22.30 ± 0.41 U/g, respectively. (Aita
et al., 2019). T. asperellum TV104 produces cellulase activity (34.3 ± 0.4 U/g)
in SSF with a mixture of vine shoots, potato flour, jatropha, olive pomace, and
olive oil as carbon sources (Hamrouni et al., 2020). A. niger CECT 2700
produced cellulase with high activity (6.23 U/g) in SSF using brewery spent
grain as a carbon source (Moran-Aguilar et al., 2021). A novel endophytic
fungus denominated Penicillium oxycum R4 cellulase using waste of stems
Hibiseu manihot L. waste stems (2 g/L) as a carbon source and different
nitrogen supplies (beef extracts, peptone, yeast extracts, (NH4)2SO4, NaNO3);
the highest cellulase activity (5.27 U/mL) was found in the culture added with
(NH4)2SO4 as a nitrogen source (Li et al., 2021).

Chitinases
Chitinases are glycosyl hydrolases with an important role in the transformation
of chitin and can be classified into two major types; 1) endochitinases (EC.
3.2.1.14) that make the first cleavage to form low molecular weight
chitooligomers (recognize o-glycosyl bonds between chito-saccharide
residues); and 2) exochitinases, which include chitobiosidases (EC 3.2.1.29)
(catalyze the progressive release of diacetylchitobiose starting at the
nonreducing end of chitin microfibril) and β-(1-4) N-acetylglucosaminidases
(EC 3.2.1.132) (hydrolyze diacetylchitobiose to N-acetyl-glucosamine).
Chitinases have a wider range of biotechnological applications, including the
bioconversion of chitin wastes, the biocontrol of fungal phytopathogens,
harmful insects, and biopesticides, among others (Singh and Arya, 2019).
Chitinases help preserve the balance of carbon and nitrogen ratios in
ecosystems (Okongo et al., 2019; Ray et al., 2019). Regarding chitinolytic
producers, the most important are Trichoderma, Aspergillus, Metarhizium,
and Beauveria. Trichoderma viride AUMC 13021 can produce chitinase
(38.33 U/mg protein) in SmF using maltose (1%) and yeast extract (1%) as
carbon and nitrogen sources, respectively, after 96 h at 35°C, pH 6.5, and 125
rpm (Abu-Tahon and Isaac, 2019). T. harzianum produces high chitinase
activity (261.5 mU/L per day) in SmF supplemented with mushroom
(Agaricus bisporus) chitin after 14 days of growing at 28 ± 1°C, 150 rpm, and
an initial pH of 6.0 (Urbina-Salazar et al., 2018). On the other hand, when
Aspergillus niveus is cultured under SmF using crab shells as a carbon source,
it can produce thermostable and denaturation-resistant chitinase (9.68 U/mg
20 E. O. Fuentes-Ramírez, R. Uzarraga-Salazar, C. Mendarte-Alquisira et al.

of protein) (Alves et al., 2018). Aspergillus flavus (AUMC 13576), on the

other hand, may produce thermostable chitinase (620.54 U/l) using shrimp as
substrate (Beltagy et al., 2018). Trichoderma koningiopsis UFSMQ40 may
produce significant levels of chitinase activity (10.76 U/g) in 72 hours at 30°C
using SSF and agro-industrial substrates (wheat bran substrate, colloidal
chitin, corn steep liquor) (Baldoni et al., 2020). B. bassiana AAUMB-29 can
produce high enzymatic chitinase activity (enzyme index = 3.41) when
cultured in SmF containing olive oil at 2% and (NH4)2SO4 (Gebremariam et
al., 2022). Isolates of B. bassiana produce a high level of specific exochitinase
(0.148 U/mg protein) when cultured SmF in a medium added with 0.01%
(w/v) of yeast extract, and 10 g of P. interpunctella larval cuticle (Reyhaneh
et al., 2023).
According to prior research, the production of these enzymes can vary
depending on the microorganism, type of culture, temperature, pH, and source
of carbon and nitrogen combined, and the microorganism can produce more
than one lytic enzyme. The industrial production of enzymes from
entomopathogenic microorganisms can be expensive at first, but using agro-
industrial waste in solid-state fermentation and submerged fermentation can
be an excellent strategy for scaling up the production of lipases, xylanases,
proteases, cellulases, and chitinases at a low cost. This concept would enable
alternate uses of agro-industrial waste to achieve a circular economy.

Other Value-Compounds from Entomopathogenic Fungi

Entomopathogenic fungi secrete a variety of secondary metabolites into the

environment. Organic molecules of low molecular weight are found among
these chemicals, including cyclic depsipeptides, terpenoids, derived amino
acids, peptides and their derivatives, and polyketides (Molnár et al., 2010;
Wang et al., 2018). All these products are thought to have a high added value
due to the various properties they possess, such as antibacterial, antiviral,
antitumor, cytotoxic, phytotoxic, and specific inhibitors of enzymatic
activities, which can be used in a variety of fields, including medicine, food,
agrochemicals, and pharmaceuticals. Some instances of these chemicals being
produced by entomopathogenic fungi are shown below.
Cyclic depsipeptides are cyclic peptide-linked compounds that have
hydroxylated carboxylic acid and amino acid residues linked by amide and
ester bonds, giving them a wide variety of chemical structures such as
destruxins, enniatins, isariins, beauvericins, beauvenniatins, and isaridins
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