ACTBIO 3244 No.

of Pages 20, Model 5G

18 June 2014

Acta Biomaterialia xxx (2014) xxx–xxx

1

Contents lists available at ScienceDirect

Acta Biomaterialia
journal homepage: www.elsevier.com/locate/actabiomat

2 Review
5
4 Applications of biosynthesized metallic nanoparticles – A review
6

7 Q1 Adam Schröfel a,b,e,⇑, Gabriela Kratošová c, Ivo Šafařík a, Mirka Šafaříková a, Ivan Raška e, Leslie M. Shor b,d
8 a
Department of Nanobiotechnology, Institute of Nanobiology and Structural Biology of GCRC, Academy of Sciences, Ceske Budejovice, Czech Republic
9 b
Department of Chemical and Biomolecular Engineering, University of Connecticut, Storrs, CT, USA
10 c
Nanotechnology Centre, VSB-Technical University in Ostrava, Ostrava, Czech Republic
11 d
Center for Environmental Sciences & Engineering, University of Connecticut, Storrs, CT, USA
12 e
Charles University, Institute of Cellular Biology and Pathology, Prague, Czech Republic

13
14
a r t i c l e i n f o a b s t r a c t
1
2 6
9
17 Article history: We present a comprehensive review of the applications of biosynthesized metallic nanoparticles (NPs). 30
18 Received 16 January 2014 The biosynthesis of metallic NPs is the subject of a number of recent reviews, which focus on the various 31
19 Received in revised form 13 April 2014 ‘‘bottom-up’’ biofabrication methods and characterization of the final products. Numerous applications 32
20 Accepted 21 May 2014
exploit the advantages of biosynthesis over chemical or physical NP syntheses, including lower capital 33
21 Available online xxxx
and operating expenses, reduced environmental impacts, and superior biocompatibility and stability of 34
the NP products. The key applications reviewed here include biomedical applications, especially antimi- 35
22 Keywords:
crobial applications, but also imaging applications, catalytic applications such as reduction of environ- 36
23 Biosynthesis
24 Metallic nanoparticles
mental contaminants, and electrochemical applications including sensing. The discussion of each 37
25 Nanomedicine application is augmented with a critical review of the potential for continued development. 38
26 Bioimaging Ó 2014 Acta Materialia Inc. Published by Elsevier Ltd. All rights reserved. 39
27 Sensors 40
28
41
42

43 1. Introduction purchase and disposal of solvents and other consumable reagents. 64

Biosynthesis can be implemented in nearly any setting and at any 65
44 The unique properties of nanoscale materials have given rise to scale [3]. In addition, extensive investment in biotechnology 66
45 tremendous research activity directed towards nanoparticle (NP) know-how for optimized production of food, pharmaceuticals and 67
46 fabrication, characterization and applications. In order to reveal fuels also informs NP biosynthesis techniques. One important 68
47 ever more favorable NP functionality, some researchers look to drawback of NP biosynthesis methods is the requirement in some 69
48 nature for methods to produce NPs with novel properties or applications to purify the sample or to separate the NPs from the 70
49 enhanced function. Many organisms are known to form inorganic biological material used in their synthesis (See Figs. 1–6). Q3 71
50 materials either intra- or extracellularly. For example, iron-reduc- The properties of biosynthesized materials may differ from 72
51 ing bacteria have been known to reduce labile and/or toxic metals materials prepared by other methods. Biosynthesis can result in 73
52 into their zero-valent form [1]. The same or similar metal-reducing forms that are difficult to make using other techniques, such as 74
53 capability used as an NP production method is called biosynthesis alloys and wires. Biosynthesized NPs can also have enhanced 75
54 [2]. As reviewed recently, many different prokaryotic and eukary- stability and biocompatibility and reduced toxicity, mainly due to 76
55 otic organisms have been used to produce metallic NPs [3], and coating them with biogenic surfactants or capping agents. The 77
56 biosynthesis of NPs has attracted increasing attention in the past potential range of sizes, shapes and compositions of biosynthe- 78
57 10 years [4]. sized NPs translates into a broad domain of existing and new nano- 79
58 Among the key advantages that the biological approach has over material applications. 80
59 traditional chemical and physical NP synthesis methods is the bio- Applications of biosynthesized metal-based NPs range from 81
60 logical capacity to catalyze reactions in aqueous media at standard various biomedical purposes (e.g. antimicrobial coatings, medical 82
61 temperature and pressure. Production in aqueous media under imaging and drug delivery) to catalytic water treatment and envi- 83
62 standard conditions leads to many cost advantages, in terms of both ronmental sensors. We have organized this review according to the 84
63 capital equipment and operating expenses, especially in the applications that use biosynthesized NPs. The chemical composi- 85
tion, form and organism used for the biosynthesis are also 86
described. 87
⇑ Corresponding author at: Charles University, Institute of Cellular Biology and
Q2 Pathology, Prague, Czech Republic. Tel.: +420 777864404; fax: +420 224917418.
E-mail address: [email protected] (A. Schröfel).

http://dx.doi.org/10.1016/j.actbio.2014.05.022
1742-7061/Ó 2014 Acta Materialia Inc. Published by Elsevier Ltd. All rights reserved.

Please cite this article in press as: Schröfel A et al. Applications of biosynthesized metallic nanoparticles – A review. Acta Biomater (2014), http://
dx.doi.org/10.1016/j.actbio.2014.05.022
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titanium, copper, magnesium and particularly silver and gold, are 105
known for their antimicrobial, antiviral and antifungal capabilities 106
[10]. These metallic NPs are actively investigated as disinfectants, 107
in food processing, and for use as additives in clothing and in med- 108
ical devices [11]. 109
The following sections describe the key antibacterial, antiviral 110
and antifungal properties described in the literature for biosynthe- 111
sized NPs (Tables 1 and 2). However, due to the large number of 112
papers describing antimicrobial activity using slightly different 113
materials, endpoints or methods, in some cases only representative 114
examples are provided. 115

2.1.1. Antibacterial activity 116

AgNP exposure causes toxicity to bacteria, primarily from Ag 117
ions released into aqueous solution following partial oxidation 118

Fig. 1. Light microscopy of gold nanoparticle biosynthesis inside the moss leaf. The [5]. Ag ions and small NPs interact with the plasma membrane, dis- 119
purple color indicates the presence of gold nanoparticles inside the cells (picture turbing cellular functions, including permeability and respiration, 120
taken and kindly provided by Markéta Bohunická). and ultimately leading to lysis. AgNP exposure can prevent DNA 121
replication and protein synthesis by binding to DNA or by denatur- 122
izing ribosomes [5]. 123
88 2. Biomedical applications The detailed mechanisms of AuNP antibacterial functionality 124
against Escherichia coli is described by Cui et al. [12]. AuNPs were 125
89 Applications of metallic NPs in the biomedical fields are numer- shown to collapse membrane potential, strongly inhibiting ATPase 126
90 ous, and there is strong potential for continued growth in this area. activity and resulting in a decrease in cellular ATP levels. Another 127
91 Metallic NPs are widely used for their antimicrobial functionality; consequence of AuNP exposure was inhibited binding of tRNA to 128
92 for example, silver NPs (AgNPs) have been incorporated into the ribosome subunit. 129
93 wound dressings, bone cements and implants [5]. Gold NPs (AuN- Bacterial susceptibility to antimicrobial agents can depend on 130
94 Ps) have medically relevant optical and anticancer properties. For the cell wall structure. Bacteria are classified into two categories, 131
95 example, Alanazi et al. [6] describe how surface plasmon absorp- based on their cell wall structure: Gram-negative (G) bacteria 132
96 tion and surface plasmon light scattering can be used for diagnostic have a multi-layer cell wall and Gram-positive (G+) bacteria have 133
97 and therapeutic applications, and Patra et al. [7] describe the fab- a single-layer cell wall. Antibacterial activity of biosynthesized 134
98 rication and application of AuNPs for targeted cancer therapy. As NPs has been studied for both types of bacteria. 135
99 described by Pankhurst et al. [8,9], magnetic NPs appear promising A variety of biological materials have been used for the biosyn- 136
100 for targeted drug delivery and hyperthermia applications. thesis of NPs with demonstrable antibacterial effects. These mate- 137
rials include fungal, bacterial and algal biomass, as well as extracts 138
101 2.1. Antimicrobial applications of botanical materials, including leaves, bark, roots and tubers. One 139
of the first reports of antibacterial effects of biosynthesized NPs 140
102 The ongoing development of antimicrobial agents is important was published by Vigneshwaran et al. [13]. These authors used 141
103 Q4 due to the continuous selection of antibiotic resistance traits in the edible mushroom Pleurotus sajor-caju for the synthesis of 142
104 bacteria and other pathogens. Different metallic NPs, including AgNPs and performed successful antimicrobial testing against 143

Fig. 2. Antimicrobial activity of AgNPs synthesized by S. hygroscopicus. (a) Candida albicans; (b) Bacillus subtilis; (c) Escherichia coli; (d) Enterococcus faecalis; (e) Salmonella
typhimurium; (f) Saccharomyces cerevisiae. Each plate shows (A) culture supernatant; (B) AgNO3 control; (C, D) synthesized AgNPs, respectively. Reprinted from Ref. [15] with
permission from Elsevier.

Please cite this article in press as: Schröfel A et al. Applications of biosynthesized metallic nanoparticles – A review. Acta Biomater (2014), http://
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Fig. 3. Probable anti-proliferative mechanism of AuNP. Reprinted from Ref. [49] with kind permission from Springer Science and Business Media.

144 Staphylococcus aureus (G+) and Klebsiella pneumoniae (G) bacteria. By far the most abundant studies on biosynthesized antibacterial 175
145 Raheman et al. [14] reported the extracellular synthesis of AgNPs NPs are those using plant tissues and extracts as reducing agents. As 176
146 by means of an endophytic fungus, Pestalotia sp., isolated from previously mentioned, biosynthesized NPs may require purification 177
147 leaves of Syzygium cumini and the antimicrobial properties of to remove pathogenic or poisonous compounds, particularly for 178
148 AgNPs against S. aureus (ATCC-25923) and Salmonella typhi materials intended for use in vivo. One approach to avoiding toxicity 179
149 (ATCC-51812). Synergistic effects were observed for combined concerns is to use only well-characterized and benign botanical 180
150 exposure to biosynthesized AgNPs and the commercially available extracts for biosynthesis [20]. For example, green tea extract (pre- 181
151 antibiotics gentamycin and sulphamethizole. pared from Camellia sinensis leaves) is a widely used reducing agent 182
152 Antimicrobial properties of bacteria-biosynthesized NPs were used in the biosynthesis of NPs. Vaseeharan et al. [21] used tea 183
153 illustrated in two studies by Sadhasivam et al. [15,16]. Streptomy- extract to prepare AgNPs with demonstrated antibacterial activity 184
154 ces hygroscopicus cells were used for biosynthesis of Ag- and AuNPs against Vibrio harveyi. Other botanical extracts have been used for 185
155 with antimicrobial properties against Bacillus subtilis, Enterococcus biosynthesis of antimicrobial AgNPs. Stem callus extract of bitter 186
156 faecalis, E. coli, Salmonella typhimurium, Staphylococcus epidermidis apple (Citrullus colocynthis) was used for AgNPs synthesis and dem- 187
157 and S. aureus. onstrated activity against biofilm-forming E. coli, Vibrio paraheamo- 188
158 An example of algae-based NP biosynthesis is described by Mer- lyticus, Pseudomonas aeruginosa, Proteus vulgaris and Listeria 189
159 in et al. [17], where AgNPs with antibacterial properties were syn- monocytogenes [22]. No activity was observed in the case of Proteus 190
160 thesized by the microalgal strains Chaetocerus calcitrans, Chlorella mirabilis, Salmonella enteritidis or Staphylococcus aureus. Kaviya 191
161 salina, Isochrysis galbana and Tetraselmis gracilis. These NPs showed et al. [23] studied biosynthesis of AgNPs using navel orange (Citrus 192
162 antimicrobial properties against K. pneumoniae, Proteus vulgaris, sinensis) peel extract and demonstrated antibacterial activity 193
163 Pseudomonas aeruginosa and E. coli, as measured using a clearing against E. coli, Pseudomonas. aeruginosa and S. aureus. Finally, Naga- 194
164 zone assay. Venkatpurwar and Pokharkar [18] introduced a jyothi and Lee [24] used Chinese yam (Dioscorea batatas) rhizome 195
165 method for synthesis of AgNPs using sulfated polysaccharides extract for the biosynthesis of antibacterial AgNPs. 196
166 isolated from the marine red alga Porphyra vietnamensis. The Several reports have described synergistic antimicrobial effects 197
167 dose-dependent effect of AgNPs synthesized in this study revealed of phytosynthesized nanoparticles used in combination with anti- 198
168 strong antibacterial activity against E. coli (G) and lesser effec- biotics. Ghosh et al. [25] synthesized AgNPs prepared with tuber 199
169 tiveness against S. aureus (G+). The synthesis of antibacterial extract of Dioscorea bulbifera, then measured synergistic antimicro- 200
170 AuNPs using powder or ethanolic extract from a marine alga bial potential using 22 types of commercially available antibiotics 201
171 Galaxaura elongata was demonstrated by Abdel-Raouf et al. [19]. and seven bacterial strains. For instance, they found an 11.8-fold 202
172 These authors also performed spectroscopy experiments in order inhibition efficiency increase when streptomycin and AgNPS are 203
173 to identify the algal compounds which may play a role as reducing used in combination against E. coli compared with the inhibition 204
174 agents or nanoparticle capping agents. efficiency using streptomycin only. 205

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Fig. 4. Optical images (right column) and reconstructed images from the intensity of Raman spectra with excitation at 514 nm (left column) and 633 nm (middle column), for
encapsulated cells before (top line) and after (second line) gold production and for free cells before (third line) and after (bottom line) gold production. Reproduced from Ref.
[61] by permission of The Royal Society of Chemistry.

206 Plant extracts have also been used for the biosynthesis of AuNPs
207 with antibacterial activity. Kumar et al. [26] used a deciduous tree
208 (Terminalia chebula) extract for the biosynthesis of AuNPs effective
209 against S. aureus and E. coli. MubarakAli et al. [27] used Mentha
210 piperita leaf extract for biosynthesis of AuNPs and AgNPs, and like-
211 wise demonstrated antimicrobial effects against S. aureus and
212 E. coli bacteria.
213 Biosynthesized metallic NPs that are immobilized on cotton
214 cloth have many important applications as material for wound
215 dressings. For example, Durán et al. [28] reported the extracellular
216 production of AgNPs mediated by the fungus Fusarium oxysporum.
217 Here, AgNPs were incorporated into cotton fabrics for inhibition of
218 S. aureus. However, one limitation of immobilized AgNPs in fabric
219 is the loss of the Ag ions, and sometimes the AgNPs, with washing.
220 El-Rafie et al. [29,30] demonstrated the use of immobilized
221 biogenic AgNPs on cotton fabric. In these studies, the AgNPs were
222 prepared with Fusarium solani and were applied to cotton fabrics
223 using an acrylate based binder. The cotton fabric showed a high
224 antimicrobial efficiency of approximately 90% against
225 S. aureus and E. coli after 20 washing cycles.
226 Tripathi et al. [31] examined biosynthesis of AgNPs using an
227 aqueous extract of Azadirachta indica leaves and their subsequent
228 immobilization on cotton cloth. These authors observed the bacteri-
229 cidal effect against E. coli and S. aureus with washing in distilled
230 water. Similarly, the biosynthesis of AgNPs in Eucalyptus citriodora Fig. 5. Electron micrograph of palladized cells of Shewanella oneidensis (kindly
231 and Ficus bengalensis leaf extracts and their loading into cotton fibers provided by Simon de Corte).

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232 was reported by Ravindra et al. [32]. Cotton fibers were immersed in 2.1.2. Antifungal activity 260
233 the leaf extract containing AgNPs, kept on a shaker for 24 h and then Several studies have described the bacteria Aspergillus niger 261
234 tested against E. coli using a modified disk diffusion method. antifungal activity of biosynthesized NPs. Gajbhiye et al. [38] 262
235 Antibacterial effect against E. coli was also tested in AgNPs that described the antifungal properties of biosynthesized NPs against 263
236 were prepared by means of the extract and powder of Curcuma Phoma glomerata, P. herbarum, Fusarium semitectum, Trichoderma 264
237 longa tubers [33], then immobilized on cotton cloth. AgNPs were sp. and Candida albicans in combination with fluconazol (a triazole 265
238 resuspended in water or in polyvinylidene fluoride (PVDF), then antifungal drug). AgNPs biosynthesized by another fungus, Q6 266
239 sprayed over pre-sterilized cotton cloth. Cloth treated with NPs Alternaria alternata, enhanced the antifungal activity of fluconazole 267
240 in PVDF exhibited lower antibacterial activity but much longer against all tested strains except P. herbarum and F. semitectum. In 268
241 reusability. Recently, antimicrobial applications for biosynthesized another study, mycelia-free water extracts of the fungal strain 269
242 AgNPs incorporated into nonwoven fabrics have been demon- Amylomyces rouxii were used for biosynthesis of AgNPs that were 270
243 strated. Yang and Li [34] prepared AgNPs using mango peel extract effective against the bacteria Shigella dysenteriae type I, 271
244 and demonstrated the antimicrobial effectiveness of these Staphylococcus aureus, Citrobacter sp., E. coli, Pseudomonas 272
245 nanoparticles immobilized on non-woven fabrics against E. coli, aeruginosa and Bacillus subtilis, and also against the fungi Candida 273
246 S. aureus and B. subtilis. albicans and Fusarium oxysporum [39]. 274
247 Sundaramoorthi et al. [35] described a wound-healing applica- Antifungal activity of biosynthesized AuNPs has also been 275
248 tion for biosynthesized AgNPs, prepared extracellularly using the described. Das et al. [40] synthesized AuNPs on the surface of the 276
249 Q5 fungus Aspergillus niger. The efficiency of the AgNPs was demon- fungus Rhizopus oryzae and demonstrated the growth inhibition 277
250 strated following excision in a rat model. The study supported both of G and G+ bacterial strains, as well as the fungi Saccharomyces 278
251 the antimicrobial effects of Ag and the ability of AgNPs to modulate cerevisiae and C. albicans. AuNPs that inhibit the growth of 279
252 cytokines involved in wound healing. Similarly, the medicinal C. albicans have also been obtained following biosynthesis using 280
253 plant Indigofera aspalathoides was used for biosynthesis of AgNPs a banana peel extract [41]. 281
254 tested in wound-healing applications following excision in animal
255 models [36]. 2.1.3. Antiviral activity 282
256 Finally, biogenic AgNPs derived from Chrysanthemum morifoli- Although viruses also represent serious problems in medicine or 283
257 um have been added to clinical ultrasound gel. In the study, the agriculture, there have been relatively few reports on the antiviral 284
258 gel was used on an ultrasound probe, and the bactericidal activity activity of biosynthesized NPs. Vijayakumar and Prasad [42] 285
259 and instrument sterility were evaluated [37]. described the antiviral activity of Ag NPs prepared intracellularly 286

Fig. 6. Electron micrographs of crystal morphologies and intracellular organization of magnetosomes found in various magnetotactic bacteria. The shapes of the magnetic
crystals include cubo-octahedral (a), elongated hexagonal prismatic (b, d, e, f) and bullet-shaped morphologies (c). The particles are arranged in one (a, b, c), two (e) or
multiple chains (d), or irregularly (f). The scale bar is equivalent to 100 nm. Reprinted from Schueler D, Frankel RB. Bacterial magnetosomes: microbiology, biomineralization
and biotechnological applications. Appl Microbiol Biotechnol 1999;52(4):464–473, with kind permission from Springer Science and Business Media.

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Table 1
Q13 Antibacterial activity.

NP Organism used Activity against References

Ag Pleurotus sajor-caju Staphylococcus aureus, Klebsiella pneumonia Vigneshwaran et al. [13]
Ag Pestalotia sp. S. aureus, Salmonella typhi Raheman et al. [14]
Ag Streptomyces hygroscopicus Bacillus subtilis, Enterococcus faecalis, Escherichia coli, Salmonella Sadhasivam et al. [15,16]
typhimurium
Au S. hygroscopicus B. subtilis, E. faecalis, E. coli, S. typhimurium, S. epidermidis, S. aureus Sadhasivam et al. [15,16]
Ag Chaetocerus calcitrans, Chlorella salina, K. pneumoniae, Proteus vulgaris, Pseudomonas aeruginosa, E. coli Merin et al. [17]
Isochrysis galbana, Tetraselmis gracilis
Ag Porphyra vietnamensis S. aureus, E. coli Venkatpurwar and Pokharkar [18]
Au Galaxaura elongata E. coli, K. pneumonia, S. aureus, P. aeruginosa Abdel-Raouf et al. [19]
Ag Camellia sinensis Vibrio harveyi Vaseeharan et al. [21]
Ag Citrullus colocynthis E. coli, Vibrio paraheamolyticus, P. aeruginosa, P. vulgaris, Listeria Satyavani et al. [56]
monocytogens
Ag Citrus sinensis E. coli, P. aeruginosa, S. aureus Kaviya et al. [23]
Ag Dioscorea batatas B. subtilis, S. aureus, E. coli Nagajyothi and Lee [24]
Ag Dioscorea bulbifera Acinetobacter baumannii, Enterobacter cloacae, E. coli, Haemophilus Ghosh et al. [25]
influenzae, K. pneumoniae, Neisseria mucosa, Proteus mirabilis
Au Terminalia chebula S. aureus, E. coli Kumar et al. [20,26]
Au, Ag Mentha piperita S. aureus, E. coli MubarakAli et al. [27]
Ag Fusarium oxysporum S. aureus on cotton fabrics Durán et al. [28]
Ag Fusarium solani S. aureus, E. coli on cotton fabrics El-Rafie et al. [29,30]
Ag Azadirachta indica S. aureus, E. coli on cotton fabrics Tripathi et al. [31]
Ag Eucalyptus citriodora, Ficus bengalensis E. coli on cotton fabrics Ravindra et al. [32]
Ag Curcuma longa E. coli on cotton fabrics Sathishkumar et al. [33]
Ag Mangifera indica E. coli, S. aureus, B. subtilis on non-woven fabrics - Yang and Li [34]
Ag Aspergillus niger Wound healing activity Sundaramoorthi et al. [35]
Ag Indigofera aspalathoides Wound healing activity Arunachalam et al. [36]
Ag Chrysanthemum morifolium Bactericidal ultrasound gel He et al. [37]

Table 2
Antifungal, antiviral and anti-parasite activity.

NP Organism used Activity against References

Ag Alternaria alternata Phoma glomerata, Phoma herbarum, Fusarium semitectum, Trichoderma sp., Gajbhiye et al. [38]
C. albicans – combination w/fluconazole
Ag Amylomyces rouxii Candida albicans, Fusarium oxysporum Musarrat et al. [39]
Au Rhizopus oryzae Saccharomyces cerevisiae, C. albicans Das et al. [40]
Au Musa sp. C. albicans Bankar et al. [41]
Ag Aspergillus ochraceus M13 phage virus Vijayakumar and Prasad [42]
Ce Leptothrix discophora, Pseudomonas putida Bacteriophage UZ1 De Gusseme et al. [43–45]
Ag Lactobacillus fermentum Bacteriophage UZ1, application to NanoCeram filter De Gusseme et al. [43–45]
Ag Lactobacillus fermentum Bacteriophage UZ1, application to PVDF membrane De Gusseme et al. [43–45]
Ag Nelumbo nucifera Larvae of Anopheles subpictus, Culex quinquefasciatus Santhoshkumar et al. [46]
Ag Rhizophora mucronata Larvae of Aedes aegypti, Culex quinquefasciatus Gnanadesigan et al. [47]
Ag Lawsonia inermis Pediculus humanus capitis, Bovicola ovis Marimuthu et al. [48]
Ag Manilkara zapota Rhipicephalus microplus Rajakumar and Rahuman [49]

287 in Aspergillus ochraceus. In the study, AgNPs embedded in a 2.1.4. Anti-parasite applications 307
288 carbonaceous matrix were obtained by heat treatment of the cells, Biosynthesized NPs are effective against various disease-caus- 308
289 and the effectiveness against M13 phage was determined using the ing insects or parasites. Santhoshkumar et al. [46] compared 309
290 plaque count method. larvicidal activity of AgNPs biosynthesized using different lotus 310
291 In another study, De Gusseme et al. [43] described virus inhibi- leaf (Nelumbo nucifera) extracts. In the study, antilarval activity 311
292 tion by zero-valent cerium produced by aqueous Ce(III) added to was measured for the fourth instar larvae of Anopheles subpictus 312
293 Leptothrix discophora and Pseudomonas putida cultures. The and Culex quinquefasciatus, both well-known vectors for malaria 313
294 as-prepared cerium exhibited efficient antivirus activity against and lymphatic filariasis. A similar study by Gnanadesigan et al. 314
295 bacteriophage UZ1. In another study by the same researchers [47] evaluated AgNPs biosynthesized with mangrove (Rhizophora 315
296 [44], Lactobacillus fermentum bacteria were used both as a reducing mucronata) leaf extract against Aedes aegypti and C. quinquefascia- 316
297 agent and as a scaffold for AgNPs. Their antiviral activity was deter- tus larva. 317
298 mined for murine norovirus 1 and bacteriophage UZ1. In another In another study, the larvicidal properties of AgNPs biosynthe- 318
299 study, the continuous antiviral capability of AgNPs embedded in sized with henna (Lawsonia inermis) leaf extract was determined 319
300 Lactobacillus cells was tested in an aqueous environment by for the human head louse Pediculus humanus capitis and the sheep 320
301 depositing the cells onto a NanoCeram electropositive filter. The body louse Bovicola ovis [48]. The study determined lousicidal 321
302 study demonstrated that the filter with cell-embedded NPs had activity using both a direct contact method (P. humanus) and an 322
303 remarkably higher antiviral activity compared with the original impregnated filter paper method (B. ovis). Finally, the acaricidal 323
304 filter. Similarly, De Gusseme et al. [45] demonstrated the activity of an evergreen tree (Manilkara zapota) aqueous extract 324
305 inactivation of UZ1 bacteriophages using a similar approach with and AgNPs synthesized by means of this extract were determined 325
306 cell-embedded NPs on a PVDF membrane. against the cattle tick (Rhipicephalus microplus) [49]. 326

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327 2.2. Drug delivery and cancer treatment present in grapes (Vitis vinifera). These AuNPs exhibited remark- 372
able affinity towards HBL-100 (human breast cancer cells), and 373
328 Biosynthesized NPs can interact with and alter the function of AuNP exposure resulted in HBL-100 apoptosis. Mishra et al. [53] 374
329 certain mammalian tissues. For example, metallic NPs can interfere described AuNP biosynthesis by the supernatant, live cell filtrate 375
330 with the antioxidant defense mechanism, leading to accumulation and biomass of the fungus Penicillium brevicompactum. In this 376
331 of reactive oxygen species, destruction of mitochondria and cell work, the cytotoxic properties of biosynthesized NPs were ana- 377
332 apoptosis [50]. This effect can be targeted, because the in vivo lyzed using mouse myoblast cancer C2C12 cells. In a different 378
333 effects of metal NP exposure strongly depend on the capping study, guava and clove extracts were used to reduce Au and Ag 379
334 agent: the same AgNPs with different capping agents have been salts [54]. Although biosynthesized AuNPs exhibited an anticancer 380
335 reported to be both cytotoxic [50] and non-cytotoxic [51]. The effect on HEK-293, HeLa and HT-29 cancer cell lines, AgNPs did not 381
336 use of stable noble metal NPs as carriers may minimize the side show any anticancer activity in this study. 382
337 effect of conventional chemotherapeutic agents by the selective In contrast, other reports have demonstrated anticancer effects 383
338 delivery of anticancer agents to malignant cells without affecting from AgNPs. Biosynthesis of anti-tumor AgNPs using Piper longum 384
339 the normal cells. For instance, gold can be readily modified due leaf as a reducing and capping agent was reported by Jacob et al. 385
340 to its ability to bind strongly to thiols (–SH) and amines (–NH2). [55]. These NPs showed an excellent cytotoxic effect on HEp-2 can- 386
341 Thus, covering the NP surface with biomolecules acting as chemo- cer cell lines. Similarly, callus extract of Citrullus colocynthis was 387
342 therapeutic and targeting agents is relatively straightforward [7]. use to form AgNPs which were effective against HEp-2 cells [56]. 388
343 With the selection of different capping agents, the cytotoxic activ- Similar efficiency against HeLa cells and a lymphoma mouse model 389
344 ity of metallic NPs can be used for both drug delivery and cancer was observed for AgNPs biosynthesized using Melia azedarach, a 390
345 cell targeting (Table 3). Whether the targeted delivery of NPs species of deciduous tree from the mahogany family [57]. A sophis- 391
346 themselves is therapeutic or the NPs act as carriers for some other ticated evaluation of AgNPs effect on cancerous cell lines was given 392
347 agent, biosynthesized NPs are becoming increasingly important in by Jeyaraj et al. [58]. The cytotoxicity effect of biogenic silver nano- 393
348 nanomedicine. particles against human breast cancer cells in vitro was studied by 394
means of the MTT, acridine orange/ethidium bromide and Hoechst 395
methods and the COMET assay. Extracellular synthesis of copper 396
349 2.2.1. Biocompatibility
NPs was performed using stem latex of Euphorbia nivulia [50]. This 397
350 Whenever NPs are used for in vivo applications, biocompatibil-
study concluded that copper NPs are toxic to A549 (human lung 398
351 ity with normal tissue is an important consideration. Moulton et al.
carcinoma) cells in a dose-dependent manner. 399
352 [51] described the biosynthesis of AgNPs using tea leaf extract as a
Recently, the anti-metastatic activity of biologically synthesized 400
353 reducing and capping agent. These authors exposed these NPs to
AuNPs was reported for the human fibrosarcoma cell line HT-1080 401
354 human keratinocytes and evaluated mitochondrial function to
[59]. Although the biosynthesized AuNPs had no toxic effects on 402
355 assess cell viability and membrane integrity. The results showed
HT-1080 cells in terms of cell viability, the study showed that AuN- 403
356 that AgNPs biosynthesized with tea leaf extract were nontoxic,
Ps inhibit cell migration of HT-1080 cells by interfering with the 404
357 suggesting this method may be promising for future in vivo
actin polymerization pathway. 405
358 applications. The biocompatibility of tea-extract-biosynthesized
359 AgNPs may be attributed to the antioxidant effect of polyphenol
360 and flavonoid surfactants.
2.2.3. NP drug carriers 406
361 Kumar et al. [20] described the blood compatibility of AuNPs
Magnetosomes are naturally occurring metallic nanoparticles 407
362 synthesized with ginger (Zingiber officionale) extract. Upon contact
found in some species of magnetotactic bacteria. These chains 408
363 with human blood, these AuNPs were shown to be non-platelet
are membranous prokaryotic structures, and are composed of 409
364 activating, and did not bring about the aggregation of other blood
approximately 20 magnetite crystals surrounded by a lipid bilayer. 410
365 cells. Moreover, they were highly stable under normal physiologi-
Sun et al. [60] demonstrated the use of bacterial magnetosomes as 411
366 cal conditions compared to chemically synthesized NPs (citrate
carriers for drug delivery applications. In the study, isolated and 412
367 capped), which tended to aggregate blood cells.
cleaned bacterial magnetosomes from the magnetotactic bacte- 413
rium Magnetospirillum gryphiswaldense were loaded with the 414
368 2.2.2. Anticancer NPs chemotherapy drug doxorubicin (DOX), attached via amino groups. 415
369 Cytotoxicology studies against various cancer cell lines have The anticancer effect of DOX-loaded bacterial magnetosomes was 416
370 been described for biosynthesized NPs. Amarnath et al. [52] pub- demonstrated using a cytotoxicity assay with HL60 and EMT-6 car- 417
371 lished experiments using AuNPs synthesized using phytochemicals cinoma cells. Inhibition of cancer cell proliferation and suppression 418

Table 3
Drug delivery and cancer treatment applications.

NP Organism used Application References

Ag Camellia sinensis Biocompatible Moulton et al. [51]
Au Zingiber officinale Blood compatibility Kumar et al. [20]
Au Vites vinefera Cytotoxic activity against HBL-100 cells Amarnath et al. [52]
Au Penicillium brevicompactum Cytotoxic activity against mouse mayo blast cancer cells Mishra et al. [53]
Au Guava Cytotoxic activity against HEK-293, HeLa, and HT-29 cells Raghunandan et al. [54]
Ag Piper longum Cytotoxic activity against Hep-2 cells Jacob et al. [55]
Ag Citrullus colocynthis (L.) Schrad Cytotoxic activity against HEp-2 cells Satyavani et al. [56]
Ag Melia azedarach Cytotoxic activity against HeLa cell lines and lymphoma mice model Sukirtha et al. [57]
Cu Euphorbia nivulia Anticancer efficiency against human lung carcinoma cells Valodkar et al. [50]
Ag Sesbania grandiflora Anticancer efficiency against human breast cancer cells Jeyaraj et al. [58]
Au Dysomsa pleiantha Cell migration of HT-1080 cell line blocking Karuppaiya et al. [59]
Fe3O4 Magnetospirillum gryphiswaldense Carriers for drug delivery applications Sun et al. [60]
Fe3O4 Magnetospirillum gryphiswaldense Biocompatibility of BM Li et al. [61]
Au Porphyra vietnamensis Carrier for drug delivery Venkatpurwar et al. [62]

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419 of mRNA levels of the important oncogene c-myc suggest DOX- voltammetry studies confirmed that SeNPs enhanced the detection 455
420 loaded magnetosomes are promising for cancer therapy. Bacterial of H2O2 resulting in an 80 nM detection limit). This material can 456
421 magnetosomes are able to carry a large amount of drug, are easy therefore be used, for instance, for the detection of hydrogen 457
422 to prepare, and are more stable and more uniform compared with peroxide in the exhaled breath condensate of patients affected 458
423 artificial magnetic NPs. They are also biocompatible. Li et al. [61] with COPD (see Table 5). 459
424 demonstrated the biocompatibility of purified and sterilized mag- Other authors have also used a GCE modified with biosynthe- 460
425 netosomes surrounded by a lipid/protein membrane to mouse sized nanoparticles for electrochemical sensing. Zheng et al. [66] 461
426 fibroblasts in vitro. Another drug delivery study employed porphy- synthesized Au–Ag alloy NPs using yeast cells and demonstrated 462
427 ran from the marine alga Porphyra vietnamensis as a reducing and an enhanced electrochemical response for vanillin (from vanilla 463
428 capping agent for the biosynthesis of AuNPs [62]. These NPs were beans and vanilla tea). With a linear range of 0.2–50 lM and a 464
429 used as a carrier for DOX. The results demonstrated that AuNP- detection limit of 40 nM, this sensor can be a simple and cheap 465
430 bound DOX showed higher cytotoxicity to LN-229 (human glioma) alternative to analytical instruments involving gas or liquid chro- 466
431 cells than unbound DOX. Spectroscopy revealed that hydrogen matography, and can be used to check the quality of food products. 467
432 bonds are involved in the DOX–AuNP conjugation. Another possible medical application of biogenic AuNPs was 468
proposed and tested by MubarakAli et al. [67], who suggested that 469
433 2.3. Medical diagnostics and sensors the conjugation of DNA with biosynthesized nanoparticles can be 470
used for diagnosis of genetic disease. 471
434 Biosynthesized NPs are also making important contributions to
435 medicine in the sensing and diagnostics areas (Table 4). These 2.4. Medical imaging applications 472
436 materials have been successfully incorporated into chemical
437 sensors that can detect medically relevant compounds, including The optical properties of metallic nanocrystals have been of 473
438 peroxides and glucose. For example, eggshell membrane was used interest for centuries. The incorporation of biosynthesis methods 474
439 as a reducing agent and scaffold in the biosynthesis of AuNPs [63]. has made possible the preparation of metal NPs with a range of 475
440 The sensor showed a linear response to different glucose concen- sizes, shapes and dielectric properties. Optical properties associ- 476
441 trations, with a detection limit of 17 lM. The same material was ated with metallic NPs include a high- or low-refractive index, high 477
442 used to measure the glucose content of human blood serum transparency, novel photoluminescence properties, photonic 478
443 samples, and analysis showed agreement with a standard routine crystals and plasmon resonance [68]. Nanophotonics studies in 479
444 medical spectrophotometric test [64]. the field, where the light interacts with particles smaller than its 480
445 Hydrogen peroxide has been acknowledged as a diagnostic wavelength, lead to novel phenomena, such as localized surface 481
446 marker of oxidative stress, playing an important role in asthma plasmon resonance and a size-dependent semiconductor band 482
447 or chronic obstructive pulmonary disease (COPD). Wang et al. gap [69]. 483
448 [65] constructed a hydrogen peroxide sensor based on biosynthe- The biosynthesis AuNPs by silica-encapsulated Klebsormidium 484
449 sized selenium NPs (SeNPs) prepared using the bacterial strain flaccidum microalgae leads to the formation of a ‘‘living’’ biohybrid 485
450 Bacillus subtilis. The resulting SeNPs were spherical and could be material [70]. Researchers have used Raman spectroscopy for 486
451 converted into one-dimensional trigonal wires (proteins excreted in situ imaging of entrapped cells and have investigated the 487
452 from B. subtilis cells act as a template). A clean glassy carbon elec- influence of the AuNPs on the photosynthetic system of the algae. 488
453 trode (GCE) was amended with a drop of a colloidal suspension of The coupling of Raman imaging and sol–gel encapsulation might 489
454 SeNPs and a drop of the enzyme horseradish peroxidase. Cyclic allow for the development of photosynthesis-based biosensors. 490

Table 4
Medical diagnostics and sensors.

NP Organism used Application References

Au Eggshell membrane Glucose sensor Zheng et al. [63]
Au Eggshell membrane Glucose sensor in human blood serum Zheng et al. [64]
Se Bacillus subtilis H2O2 sensor Wang et al. [65]
Au–Ag Saccharomyces cerevisiae Vanillin sensor Zheng et al. [66]
Au Different microalgae DNA conjugation MubarakAli et al. [67]

Table 5
Imaging and other medical applications.

NP Organism used Application References

Au Klebsormidium flaccidum Photosynthesis-based environmental biosensor Sicard et al. [70]
Ag Trichoderma viride NP photoluminescence Fayaz et al. [71]
Ag Parthenium hysterophorus NP photoluminescence Sarkar et al. [72]
Ag Coriandrum sativum leaf Optical limiting Sathyavathi et al. [74]
Te Bacillus selenitireducens Optical limiting Liao et al. [75]
Au Maduca longifolia Efficiency in absorbing infrared radiation Fayaz et al. [76]
Au Cymbopogon citratus Infrared absorbing optical coatings Shankar et al. [77]
CdTe Saccharomyces cerevisiae Biolabeling and bioimaging Bao et al. [78]
CdTe Escherichia coli Biolabeling and bioimaging Bao et al. [79]
CdS Brevibacterium casei Fluorescence emission Pandian et al. [80]
Au Psidium guajava Diabetes treatment –tyrosine phosphatase type PTP 1B inhibition Basha et al. [81]
Au, Ag Brevibacterium casei Anticoagulation activity Kalishwaralal et al. [82]
Au Solanum nigrum Free radical scavenging effect Muthuvel et al. [83]
Ag Trichoderma reesei HIV treatment Vahabi et al. [84]

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491 Blue orange light emission from biosynthesized AgNPs was blood plasma for 24 h did not show any significant reduction in the 554
492 reported by Fayaz et al. [71]. Fungal-mediated AgNPs were anticoagulation activity. 555
493 prepared using a Trichoderma viride filtrate. Photoluminescence Free radical scavenging activity was demonstrated by Muthuvel 556
494 measurements after laser excitation showed an emission in the et al. [83]. Au-NPs biosynthesized by means of Solanum nigrum 557
495 range of 320–520 nm, making such AgNPs promising for future were tested for the scavenging effect on 10 1-diphenyl-2-pic- 558
496 labeling and imaging applications. A similar study was introduced rylhydrazyl radical and hydroxyl radicals according to the method 559
497 by Sarkar et al. [72] using Parthenium hysterophorus leaf extract for of Blois and the deoxyribose method, respectively. The synthetic Q7 560
498 AgNP biosynthesis. antioxidant butyl hydroxyl toluene was used as a positive control, 561
499 An important problem of modern laser medicine is the exten- and biogenic nanoparticles showed up to 60% inhibition efficiency 562
500 sive exposure of vulnerable tissues outside of the operational field. for both radical types. Interestingly, Trichoderma reesei-produced 563
501 This problem can be solved by placing dyes that are capable of AgNPs prevent HIV-1 particles from binding to host cells [84]. 564
502 reversible darkening of the radiation onto the surface of irradiated Finally, Gopinath et al. [85] described enhanced mitotic cell 565
503 tissues. This phenomenon is called optical radiation limiting [73]. division and pollen germination activity caused by AuNPs 566
504 AgNPs biosynthesized using Coriandrum sativum leaf extract were synthesized using Terminalia arjuna leaf extract. These studies 567
505 found to exhibit strong reverse saturable absorption of laser irradi- demonstrate the wide range of biomedically relevent effects possi- 568
506 ation [74]. The authors measured nonlinear refraction and absorp- ble by exposure to biosynthesized NPs. Additional research will 569
507 tion coefficients using a Z-scan technique with laser pulses. These offer new discoveries and insights into the use of biosynthesized 570
508 results suggest AgNPs are capable of nonlinear optics. Similarly, NPs as promising treatments for human diseases. 571
509 microbiologically formed nanorods prepared using Bacilus seleniti-
510 reducens and composed of elemental tellurium Te(0) have been
511 described elsewhere [75]. These TeNPs form unusual nanocompos- 3. Environmental remediation applications 572
512 ites when combined with an organic chemical host and exhibit
513 excellent broadband optical limiting at 532 and 1064 nm. In this 3.1. Metal biosorption, bioremediation and biorecovery 573
514 regard, they significantly exceeded the best commercial optical
515 limiters currently available. Their relative ease of biomanufactur- Oxidation–reduction processes are universally used for cellular 574
516 ing combined with their unique properties makes these Te-based metabolism; therefore biomolecules with the ability to reduce or 575
517 nanocomposites particularly attractive for their immediate oxidize other chemical compounds are abundant in any living cell. 576
518 employment as coatings in medicine or industry (e.g. to protect Many microorganisms are able to bind and concentrate dissolved 577
519 eyes from damage caused by exposure to focused beams and metals as an active mechanism to detoxify their environment. 578
520 lasers). Other biological processes, and even dead biomass, simply couple 579
521 Fayaz et al. [76] biosynthesized AuNPs using Maduca longifolia metal reduction with oxidation of an electron donor. Since the 580
522 extract and showed strong near-infrared absorption. Although product of cellular metal reduction is usually nanostructured, bio- 581
523 some applications are not directly medical in nature, such as remediation of metals in solution and biosynthesis of metallic NPs 582
524 energy-saving window coatings, a similar technology can also be are in fact closely related processes [86]. In this section, we review 583
525 applied for cancer hyperthermia coatings [77]. studies that describe biological metal removal and NP formation 584
526 The same research team published two additional studies via biologically mediated processes (see Table 6). 585
527 describing cadmium telluride quantum dots (CdTeQDs) fabricated The biomass of algae, fungi, bacteria and yeasts, along with 586
528 via extracellular synthesis using Saccharomyces cerevisiae [78] and some biopolymers and biowaste materials, are known to bind 587
529 Escherichia coli [79]. The authors evaluated the NP’s size-dependent and concentrate precious metals [87]. This so-called biosorption 588
530 optical properties. CdTeQD were relatively small, capped with process can represent a cost-effective alternative to the common 589
531 protein and highly soluble in water. The optical properties were chemical methods for recovery of various dissolved metals from 590
532 studied in both cases using UV–visible spectroscopy and aqueous solution. The mechanisms involved in binding and 591
533 spectrofluorimetry with photoluminescence emission from 488 concentrating metals by microbes have been extensively studied 592
534 to 551 nm. CdTeQDs functionalized with folic acid were used for in natural environments [87]. 593
535 in vitro imaging of cancer cells, and were also found to be Chakraborty et al. [88] demonstrated the ability of cyanobacte- 594
536 biocompatible in a cytotoxicity assay [79]. This study clearly shows ria and algae to bind and concentrate Au and form AuNPs. The NP 595
537 the capacity of biosynthesized QDs to be used in bioimaging and formation process is specific to a particular genus, and they 596
538 biolabeling applications. described NP formation using the cyanobacterial strains Lyngbya 597
539 Finally, a study using Brevibacterium casei for the biosynthesis of majuscula and Spirulina subsalsa, and the freshwater green alga Rhi- 598
540 CdSNPs [80] showed that the NPs exhibited fluorescence emission zoclonium hieroglyphicum. AuNPs formation during biosorption by 599
541 even after immobilization within a polyhydroxybutyrate matrix. the seaweed Fucus vesiculosus was reported by Mata et al. [89]. 600
These authors described the pH dependence on NP formation and 601
discussed the stages of the bioreduction process. 602
542 2.5. Other medical applications Dead biomass of the macrofungus Pleurotus platypus was used 603
for biosorption of Ag in a study by Das et al. [90]. The fungal 604
543 Several studies have shown biosynthesized NPs to have poten- biomass exhibited the highest Ag uptake of 46.7 mg g1 at pH 6.0 605
544 tial applications for the treatment of other diseases, including in the presence of 200 mg l1 Ag(I) at 20 °C. These authors also 606
545 diabetes and bleeding disorders. Biosynthesized AuNPs have been offered detailed kinetic and thermodynamic analysis of the 607
546 shown to inhibit the enzyme tyrosine phosphatase type PTP 1B biosorption process. Zhang et al. [91] demonstrated the use of 608
547 in vitro [81]. Since PTP 1B has been found to dephosphorylate insu- the G facultative anaerobic bacteria Aeromonas SH10 to treat Ag 609
548 lin receptors, reducing its activity can enhance the activity of insu- in waste water. In this study, biomass was shown to accumulate 610
549 lin. AuNPs prepared by means of guavanoic acid from a leaf extract Ag+ and [Ag(NH3)2]+ ions as AgNPs. The maximum uptake of 611
550 of Psidium guajava showed a significant inhibitory effect, with an [Ag(NH3)2]+ was 0.23 g of Ag per g of cell dry weight. 612
551 IC50 of 1.14 lg ml1. Another study showed that biosynthesized An example of platinum recovery by polyethyleneimine (PEI)- 613
552 Au- and AgNPs produced and stabilized using Brevibacterium casei modified biomass was described by Won et al. [92]. In this study, 614
553 exhibited anticoagulation activity [82]. Exposure of the particles to PEI was attached to the surface of E. coli biomass and the resulting 615

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Table 6
Metal biosorption, bioremediation and biorecovery.

NP Organism used Application References

Au Lyngbya majuscula, Spirulina subsalsa, Rhizoclonium hieroglyphicum Bioaccumulation Chakraborty et al. [88]
Au Fucus vesiculosus Bioaccumulation, biorecovery Mata et al. [8]
Ag Pleurotus platypus Biosorption Das et al. [90]
Ag Aeromonas sp. SH10 Silver-containing waste water treatment Zhang et al. [91]
Pt Escherichia coli Biosorption, biorecovery by incineration Won et al. [92]
Au Sargassum sp. Biosorption, biorecovery by incineration Sathishkumar et al. [93]
Ag Saccharomyces cerevisiae As(V) bioaccumulation and removal Selvakumar et al. [94]
MnO2 Bacillus sp. (MTCC10650) Mn bioremediation Sinha et al. [95]

616 material was used to accumulate platinum from waste water. Sub- The following sections describe catalytic treatment of organic com- 651
617 sequent incineration of the modified biomass resulted in 98.7% pounds and metals using biosynthesized metallic NPs. 652
618 recovery of platinum from the ash. A similar study employed the
619 brown macroalga Sargassum sp. [93] for Au recovery and reported
3.3. Catalytic degradation of organic pollutants 653
620 an efficiency of greater than 90%.
621 Toxic concentrations of naturally occurring arsenic in drinking
3.3.1. Catalytic dehalogenation 654
622 water are a major public health problem in Southeast Asia. Sel-
Palladium-based catalysts are able to dehalogenate aromatic 655
623 vakumar et al. [94] described a promising solution to this problem
compounds. This reaction is very important for organic synthesis 656
624 through their development of an AgNP sorbent for As(V) removal.
in research and industry, and also for contaminant remediation. 657
625 In the study, the reducing capabilities of a novel yeast strain of
Halogenated organic compounds dominate the priority list of per- 658
626 Saccharomyces cerevisiae was used to sequester the metal. Finally,
sistent, bioaccumulative and toxic (PBT) pollutants as designated 659
627 Sinha et al. [95] showed that a heavy-metal-resistant strain of
by the US Environmental Protection Agency. By definition, PBT 660
628 Bacillus sp. formed MnO2 NPs simultaneously with the remediation
compounds do not break down naturally in the environment, so 661
629 of manganese.
enhanced processes to dehalogenate these compounds are of great 662
630 Hexavalent chromium compounds are dangerous toxins, while
interest. Halogenated organic PBTs include several banned pesti- 663
631 Cr(III) ions and compounds are relatively non-toxic. Bare living
cides, including chlordane, dichlorodiphenyltrichloroethane 664
632 cells of Shewanella algae, Pseudomonas putida and Desulfovibrio
(DDT), dieldrin and hexachlorobenzene, as well as polychlorinated 665
633 vulgaris have been shown to reduce Cr(VI) to Cr(III) [96]. Many
biphenyls (PCBs), compounds formerly used in electronic devices 666
634 other studies rely on biosynthesized PdNPs to catalytically reduce
and as coolants, lubricants and plasticizers. 667
635 chromium. (See Section 3.4 on catalytic Cr(VI) reduction.)
Baxter-Plant et al. [99,100] described the dehalogenation of 668
chlorophenol (CP) and selected PCB congeners, including 4-chloro- 669
636 3.2. Coupling biosorption with catalytic contaminant degradation biphenyl, 2,4,6-trichlorobiphenyl, 2,3,4,5-tetrachlorobiphenyl and 670
2,20 ,4,40 ,6,60 -hexachlorobiphenyl, via palladized cells of G Desulf- 671
637 Due to their large surface area per weight, metallic NPs are ovibrio bacteria. Biosynthesized PdNPs were obtained by the reduc- 672
638 widely used for catalysis, and in particular for heterogeneous catal- tion of the palladium precursor in the presence of Desulfovibrio 673
639 ysis. Metallic NPs offer selectivity, high activity and stability. The desulfuricans, Desulfovibrio vulgaris and Desulfovibrio sp. Oz-7. As 674
640 major drawback of metallic NP catalysis is cost: the constituent described by Bunge et al. [101], reduction in the absence of cells 675
641 metals, including gold, platinum and palladium, are very expen- does not lead to the formation of PdNPs; rather, this process 676
642 sive, and their fabrication into nanoparticles is energy intensive. requires an electron donor, such as formate (see Tables 8 and 9). 677
643 Coupled biosynthetic approaches can generate catalytically active Shewanella oneidensis is another strain of bacteria that has been 678
644 NPs through biosorption of waste streams containing precious used to biosynthesize PdNPs for dehalogenation of PCB and other 679
645 metals. The coupling of biological metal removal with catalyst for- chlorinated organic compounds. De Windt et al. [102] described 680
646 mation has been described in recent reviews by De Corte et al. [97] PdNPs precipitated on the cell wall and inside the periplasmic 681
647 and Hennebel et al. [98]. These biosynthesized metallic NPs can space of S. oneidensis and demonstrated the effective dehalogen- 682
648 then be used for catalytic dehalogenation, organic oxidation or ation of PCBs in water and sediment. Their study described in 683
649 metal reduction. Most environmental remediation applications of detail bioreduction with different electron donors and varying 684
650 biosynthesized catalyst employ palladium (Pd) NPs (see Table 7). fractions of PdNPs associated with the biomass. They showed that 685

Table 7
Catalytic dehalogenation.

NP Organism used Application References

Pd Desulfovibrio vulgaris, D. desulfuricans Dechlorination of CP and PCBs Baxter-Plant et al. [99]
Pd D. desulfuricans Dechlorination of CP and PCBs Baxter-Plant et al. [100]
Pd Shewanella oneidensis Dechlorination of chlorophenol and PCBs De Windt et al. [102]
Pd S. oneidensis Dechlorination of perchlorate and PCBs De Windt et al. [103]
Macaskie et al. [104]
Pd D. desulfuricans, Rhodobacter sphaeroides Dechlorination of (PCBs) and penta-CP Redwood et al. [105]
Pd S. oneidensis Dechlorination of lindane Mertens et al. [106]
Pd S. oneidensis Dechlorination of TCE, membrane reactor Hennebel et al. [107]
Pd S. oneidensis Dechlorination of TCE, fixed bed reactor Hennebel et al. [108]
Fe/Pd Camellia sinensis Dechlorination of TCE Smuleac et al. [109]
Pd D. desulfuricans Dehalogenation PCBs and polybrominated diphenyl ether Harrad et al. [110]
Pd D. desulfuricans Dehalogenation of flame retardant materials Deplanche et al. [111]
Pd S. oneidensis Deiodination of diatrizoate Hennebel et al. [112]
Pd S. oneidensis Dehalogenation of diatrizoate in microbial electrolysis cells De Gusseme et al. [113]

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686 the catalytic activity of biosynthesized PdNPs was 100 higher Fe/PdNPs. The biosynthesized NPs exhibited a lower reaction rate 720
687 than commercial palladium catalyst powder. than chemically synthesized FeNPs, though the reactivity of chem- 721
688 In a follow-on report, De Windt et al. [103] performed a detailed ically synthesized FeNPs diminished to less than 20% within four 722
689 assessment of the bioreduction process and its conditions. In par- cycles. By contrast, the reactivity of the green tea extract-synthe- 723
690 ticular, they investigated the factors influencing the particle size sized NPs was preserved throughout 3 months of repeated use 724
691 and catalytic properties of PdNPs formed from a soluble palladium under conditions simulating a real water treatment system, possi- 725
692 precursor by S. oneidensis. Interestingly, the relatively large palla- bly due to a number of polyphenols that can act as capping agents. 726
693 dium crystals formed on non-viable biomass exhibited high cata- Biosynthesized PdNPs can also catalytically dehalogenate bro- 727
694 lytic efficiency towards hydrophobic molecules such as PCBs, minated organic compounds. Harrad et al. [110] demonstrated that 728
695 while the smaller PdNPs created on living bacterial cells showed palladized D. desulfuricans is able to catalytically dehalogenate 729
696 high catalytic activity towards perchlorate. polybrominated diphenyl ether (PBDE). Hydrophobic brominated 730
697 Macaskie et al. [104] extensively studied the catalytic dechlori- compounds such as PBDE are used as flame retardants in building 731
698 nation of 2-chlorophenol, pentachlorophenol and various PCB materials, textiles and plastics. Deplanche et al. [111] also used 732
699 congeners by palladized cells of Desulfovibrio and Escherichia coli. palladized cells of D. desulfuricans for the catalytic dehalogenation 733
700 Redwood et al. [105] compared the efficiency of palladized D. of flame retardants, including PBDE and tris-(chloroisopropyl)- 734
701 desulfuricans with Rhodobacter sphaeroides for catalytic dechlorina- phosphate (TCPP), and compared their performance with 735
702 tion of PCBs and pentachlorophenol. Mertens et al. [106] chemically reduced palladium powder. The chemically reduced 736
703 demostrated the efficiency of palladized S. oneidensis for the cata- Pd was more effective in debrominating PBDE, but the biosynthe- 737
704 lytic decomposition of the pesticide lindane. These authors also sized PdNPs were five times more effective in TCPP dechlorination. 738
705 incorporated the catalytic material into a membrane bioreactor Two studies have demonstrated that biosynthesized NPs can 739
706 for the continuous treatment of lindane-contaminated water. remediate diatrizoic acid (or diatrizoate), a radiocontrast agent. 740
707 Other studies have demonstrated the use of palladized cells for Hennebel et al. [112] demonstrated that PdNPs encapsulated on 741
708 dechlorination of the common groundwater contaminant trichlor- PVDF membranes effectively deiodinate diatrizoate in water. Sim- 742
709 ethylene (TCE). Hennebel et al. described two reactor geometries ilarly, De Gusseme et al. [113] showed that biosynthesized PdNPs 743
710 for catalytic dechlorination of TCE by biosynthesized PdNPs: a contributed to higher dehalogenation rates of TCE and higher 744
711 pilot-scale membrane reactor [107] and a fixed bed reactor with deiodination rates of diatrizoate when applied on the surface of a 745
712 PdNPs embedded in a polyurethane foam [108]. These authors graphite cathode. The presence of PdNPs on the cathode enhanced 746
713 described the cumulative removal of 98% of TCE after 22 h, with the rate of diatrizoate removal by both direct electrochemical 747
714 ethane as the predominant product, and a maximum removal rate reduction and catalytic reduction using the hydrogen produced 748
715 of 1.059 mg of TCE per g of biosynthesized PdNPs per day. at the cathode of the microbial electrolysis cell. 749
716 Other authors used Fe and Fe/Pd NPs biosynthesized with tea
717 extract (Camellia sinensis) then immobilized in polymer mem- 3.3.2. Catalytic 4-nitrophenol degradation 750
718 branes for the catalytic degradation of TCE [109]. These authors The rapid development and use of synthetic pesticides, dyes, 751
719 found that the reaction rate constant was higher for the bimetallic explosives and pharmaceuticals in the middle of the last century 752

Table 8
Catalytic 4-nitrophenol degradation and catalytic treatment of other aqueous organic compounds.

NP Organism used Application References

Au Sesbania drummondii Reduction of 4-nitrophenol Sharma et al. [114]
Au Cacumen platycladi Reduction of 4-nitrophenol Huang et al. [115]
Ag Sepia esculenta Reduction of 4-nitrophenol Jia et al. [118]
Ag Breynia rhamnoides Reduction of 4-nitrophenol Gangula et al. [116]
Au B. rhamnoides Reduction of 4-nitrophenol Gangula et al. [116]
Pd/Au Cupriavidus necator Reduction of 4-nitrophenol Hosseinkhani et al. [117]
Ag Rhizopus oryzae Reduction of 4-nitrophenol Das et al. [119]
Fe C. sinensis Degradation of aqueous cationic and anionic dyes Shahwan et al. [120]
Au C. sinensis Reduction of methylene blue Gupta et al. [121]
ZnS Streptococcus thermophiles, Photocatalytic degradation of fuchsine Zhou et al. [122]
Lactobacillus bulgaricus,
Lactobacillus acidophilus
Ag Coccinia grandis Photocatalytic degradation of Coomassie Brilliant Blue G-250 Arunachalam et al. [123]
Pd Pseudomonas putida Removal of micropollutants (e.g. ibuprofen, diclofenac, mecoprop) Forrez et al. [124]

Table 9
Catalytic Cr(VI) reduction.

NP Organism used Application References

Pd E. coli mutant strains Reduction of Cr(VI) to Cr(III) Deplanche et al. [125]
Pd D. desulfuricans Reduction of Cr(VI) to Cr(III) Mabbett and Macaskie [126]
Pd Desulfovibrio vulgaris, Desulfovibrio desulfuricans Reduction of Cr(VI) to Cr(III) Humphries et al. [127]
Pd D. desulfuricans Reduction of Cr(VI) to Cr(III) Mabbett et al. [128]
Pd/MM* D. desulfuricans, Escherichia coli Reduction of Cr(VI) to Cr(III) Mabbett et al. [129]
Pd Serratia sp. (NCIMB) Reduction of Cr(VI) to Cr(III) Beauregard et al. [130]
Pd Clostridium pasteurianum Reduction of Cr(VI) to Cr(III) in aquifer environment Chidambaram et al. [131]
Pd E. coli, Desulfovibrio spp. Reduction of Cr(VI) to Cr(III) Macaskie et al. [146]
*
Mixed precious metals.

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753 has resulted in a legacy of toxic nitro-aromatic contamination in magenta dye fuchsine using PbS and ZnS hollow nanostructures 818
754 soil and water. Technologies for catalytic removal of compounds formed on two species of bacteria. Photocatalytic degradation of 819
755 such a 4-nitrophenol (also known as p-nitrophenol or PNP) can the dye Coomassie Brilliant Blue G-250 in the presence of UV light 820
756 help restore impacted environments. Furthermore, the degradation has also been shown by AgNPs prepared from the aqueous extract 821
757 of PNP can be measured easily using widely available and inexpen- of Coccinia grandis leaves [123]. 822
758 sive optical methods such as UV–visible spectrophotometry. The Finally, Forrez et al. [124] used biosynthesized PdNPs in a mem- 823
759 catalytic degradation of PNP has thus become a common test brane reactor to remove micropollutants such as ibuprofen (>95%), 824
760 system to evaluate the catalytic reduction capabilities of biosyn- diclofenac (86%), mecoprop (81%) and triclosan (>78%) from the 825
761 thesized NPs. secondary effluent of a sewage treatment plant. The authors 826
762 The first report of PNP reduction employing biosynthesized NPs suggested that the removal mechanisms could include chemical 827
763 was published by Sharma et al. [114]. Seedlings of the plant Sesba- oxidation by PdNPs and/or biological removal by Pseudomonas 828
764 nia drummondii were grown in a hydrogen tetrachloroaurate solu- putida bacteria. 829
765 tion and stable AuNPs were subsequently formed in plant tissues.
766 This AuNP-rich plant tissue was used as an efficient catalyst for 3.4. Catalytic Cr(VI) reduction 830
767 PNP reduction in the presence of sodium borohydride.
768 Subsequently, others have used plant materials to biosynthesize Another important environmental application for biosynthe- 831
769 noble metal NPs for catalytic PNP reduction. Huang et al. [115] car- sized NPs is the catalytic reduction of the powerful oxidant Cr(VI) 832
770 ried out an extensive study using 21 species of traditional Chinese to the relatively non-toxic valence state Cr(III). Several recent stud- 833
771 herbs and medicinal plants. These plants were divided into four ies have shown that PdNPs biosynthesized by various species of 834
772 Q8 groups, and their leaves, flowers, fruits or grasses were used for bacteria, including E. coli, Desulfovibrio, Serratia and Clostridium, 835
773 NP biosynthesis by 30 min incubation in aqueous HAuCl4. Due to can effectively catalyze the reduction of Cr(VI) to Cr(III) under both 836
774 their monodispersity and small size, AuNPs prepared using Cacu- batch and continuous flow conditions. For example, Deplanche 837
775 men platycladi leaves were used to demonstrate catalytic PNP et al. [125] evaluated how three types of hydrogenases encoded 838
776 reduction. Gangula et al. [116] used the stem extract of a medicinal by E. coli influence the activity of biosynthesized catalyst for 839
777 plant Breynia rhamnoides for fast (7 min) biosynthesis of AgNPs Cr(VI)/Cr(III) reduction. This study also described the hydrogenase 840
778 and AuNPs. These authors found the conversion efficiency to be involvement in Pd(II) reduction. Macaskie et al. [104] compared 841
779 dependent on the NP size, which is possibly controlled by the stem E. coli and Desulfovibrio spp. for the biosynthesis of PdNPs for cat- 842
780 extract concentration used for biosynthesis. alytic Cr(VI)/Cr(III) reduction. Mabbett and Macaskie [126] used 843
781 Bacteria have also been used for biosynthesis of bimetallic Pd/ Desulfovibrio desulfuricans for the biosynthesis of PdNPs for 844
782 AuNPs for PNP reduction. Hosseinkhani et al. [117] formed biosup- Cr(VI)/Cr(III) reduction in waste water. These authors found that 845
783 ported Pd(0) and Au(0) NPs on the surface of Cupriavidus necator the biosynthesized PdNPs were more efficient reduction catalysts 846
784 cells. Bimetallic particles were subsequently formed following than either bare living D. desulfuricans biomass or chemically 847
785 the addition of either Au(III) or Pd(II) salt to the biosupported reduced palladium. They proposed that the palladium catalyzes 848
786 NPs. Although the bimetallic NPs did not have a core–shell struc- the hemolytic cleavage of H2 and that the H⁄ radicals then donate 849
787 ture, they exhibited superior catalytic efficiency in PNP conversion their electrons to reduce the Cr(VI). 850
788 compared with monometallic NPs. Unlike the previous experiments, all of which were carried out 851
789 Catalytic PNP reduction has also been done using animal-derived under batch conditions, Humphries et al. [127] reported a 852
790 materials for the biosynthesis of NPs. Jia et al. [118] described AgNP continuous flow system for Cr(VI)/Cr(III) reduction. In this study, 853
791 biosynthesis and immobilization using a cuttlebone-derived organic biosupported PdNPs formed by Desulfovibrio vulgaris were 854
792 matrix from the cuttlefish Sepia esculenta. The calcareous matrix of immobilized in agar and the effects of Pd concentration, Cr(VI) con- 855
793 the cuttlebone functioned as both a reducer and a scaffold for AgNP centration and process flow rate were investigated. This work built 856
794 formation. These researchers also described the reusability of the on a study by Mabbett et al. [128], who had previously demon- 857
795 composite material and the potential for separation of NPs from strated a continuous flow system for Cr(VI)/Cr(III) reduction by 858
796 the matrix. Das et al. [119] showed that the immobilization of the PdNPs biosynthesized by D. desulfuricans. Mabett et al. [129] 859
797 biogenic AgNPs on the nanostructured silica leads to their excellent subsequently described the formation of a mixed metal catalyst 860
798 hydrogenation catalytic efficiency. Protein extract from Rhizopus biosynthesized with D. desulfuricans and E. coli from a metal waste 861
799 oryzae was applied on the nanosilica and used for AgNP biosynthesis. stream for Cr(VI)/Cr(III) reduction. 862
800 The resulting material was subsequently used for catalytic hydroge- Beauregard et al. [130] used a biofilm-forming bacterial species 863
801 nation of 4-nitrophenol. Serratia sp. to mediate the adherence of bio-PdNPs to porous poly- 864
urethane foam. The foam was used as a scaffold for the catalyst and 865
802 3.3.3. Catalytic treatment of other aqueous organic compounds supported the growth of the bacterium. Magnetic resonance imag- 866
803 Other organic compounds have been effectively reduced using ing was used to directly monitor Cr(VI)/Cr(III) reduction since 867
804 biosynthesized NPs. Iron and gold NPs have been used to catalyti- Cr(VI)aq is non-paramagnetic and Cr(III)aq is paramagnetic. Finally, 868
805 cally remove dyes from aqueous solutions. In one study, FeNPs Chidambaram et al. [131] demonstrated successful Cr(VI) reduc- 869
806 biosynthesized by means of green tea extract were used as a Fen- tion experiments using PdNs biosynthesized by the bacterium 870
807 ton-like catalyst for the decolorization of aqueous solutions of Clostridium pasteurianum. This study is unique because, unlike 871
808 methylene blue and methyl orange dyes [120]. Compared with iron the previous studies, the C. pasteurianum communities were grown 872
809 NPs produced by the reduction of sodium borohydride, the biosyn- on aquifer material and catalytic reduction experiments were 873
810 thesized iron NPs exhibited faster dye removal and a greater extent performed in a natural aquifer environment. This study opens up 874
811 of dye removal. Gupta et al. [121] used green tea extract to biosyn- the potential for in situ Cr(VI) remediation via Pd(II) injection into 875
812 thesize AuNPs for catalytic reduction of the dye methylene blue in the aquifer. 876
813 the presence of Sn(II) in both aqueous solution and micelles. The
814 authors showed that a small quantity of AuNPs decreases the acti- 3.5. Biosynthesized NPs to enhance membrane treatment processes 877
815 vation energy for reduction of methylene blue, and complete
816 removal of dye could be achieved even at low temperature. Zhou Technologies to reduce biofouling can greatly enhance the 878
817 et al. [122] described the photocatalytic degradation of the performance of membrane-based water treatment processes. 879

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880 Zhang et al. [132] showed that different amounts of biogenic Reusability studies demonstrated that the catalyst retained its 925
881 AgNPs formed by Lactobacillus fermentum prevented biofouling activity over five cycles. 926
882 on polyethersulfone membranes. The membranes were used to Biosynthesized NPs have been used to catalyze cross-coupling 927
883 remove organophosphate pesticides and E. coli cells from a waste reactions (i.e. C–C bond formation). Søbjerg et al. [138] showed 928
884 water model. The authors measured the structure and performance that palladized bacteria Cupriavidus necator, Pseudomonas putida 929
885 of the membrane and assessed biofouling using E. coli and P. aeru- and Staphylococcus sciuri were effective catalysts for both the 930
886 ginosa bacteria both individually and in mixed culture. The nano- Suzuki–Miyaura and Mizoroki–Heck reactions. In a follow-on 931
887 functionalized membrane coating exhibited good antibacterial report, these authors described how biomass/Pd ratio and NPs 932
888 activity and prevented biofilm formation on the membrane surface sizes influenced the hydrogenation of (E)-3-(4-methoxyphenyl)- 933
889 during the 9 week test. N-methylacrylamide and the reduction of 4-chloro-nitrobenzene 934
[139]. Finally, Gauthier et al. [140] demonstrated the formation 935
of catalyst for C–C bond formation was coupled to the recovery 936
of Pd from a waste stream using Cupriavidus necator cells. 937
890 4. Industrially important applications
In addition to palladium, biosynthesized gold and platinum NPs 938
have been used to catalyze other organic synthesis reactions. Du 939
891 4.1. Catalytic organic synthesis
et al. [141] used biosynthesized AuNPs to catalyze propylene epox- 940
idation. Negatively charged AuNPs were immobilized on a titanium 941
892 Cheap specific catalysts for commercially important organic
silicalite support using electrostatic attractive interactions in an 942
893 synthesis reactions, including hydrogenation, cross-coupling reac-
extract of Cacumen platycladi. These authors achieved a propylene 943
894 tions and epoxidation, are extremely important in industry.
epoxide formation rate higher than previously described in other 944
895 Biosynthesized palladium, gold and platinum catalysts have been
reports. The authors proposed that the efficiency and selectivity 945
896 used successfully in several different organic synthesis pathways
of biosynthesized catalysts could be influenced by residual biomol- 946
897 (see Table 10).
ecules. A more detailed investigation of the same catalyst by Zhan 947
898 Creamer et al. [133] used palladized cells of bacterial strains
et al. [142] described the optimum reaction parameters, including 948
899 Desulfovibrio desulfuricans (G) and Bacillus sphaericus (G+) for cat-
the Si/Ti molar ratio, Au loading, immobilization pH and reaction 949
900 alytic hydrogenation of itaconic (or methylenesuccinic) acid. Com-
temperature, together with possible reaction mechanisms. Simi- 950
901 parisons performed in a stirred autoclave between biosynthesized
larly, AuNPs immobilized on a titanium silicalite support were 951
902 PdNPs and commercial graphite-supported catalysts displayed
calcined and used for industrially important epoxidation of styrene 952
903 similar activity. Bennett et al. [134] investigated the hydrogenation
to styrene oxide [143]. This experimental setup enables a styrene 953
904 and isomerization of 2-pentane using palladized D. desulfuricans in
conversion of 92.7% and a styrene oxide selectivity of 90.4% under 954
905 a stainless steel Büchi reactor. They found that, although the rate of
optimal conditions. 955
906 2-pentane hydrogenation was lower for the biosynthesized Pd cat-
Finally, biosynthesized PtNPs have been used to catalyze the 956
907 alyst than for the commercial Pd/Al2O3 catalyst, the selectivity was
synthesis of the organic dye antipyrilquinoneimine from aniline 957
908 similar. Wood et al. [135] used palladized Rhodobacter capsulatas
and 4-aminoantipyrine in acidic aqueous solution [144]. In this 958
909 and Arthrobacter oxidans for the hydrogenation of 2-butyne-1,
report, honey-mediated platinum nanostructures were found to 959
910 4-diol. The biosynthesized PdNPs exhibited high selectivity during
be stable in water for more than 4 months. 960
911 partial hydrogenation to 2-butene-1,4-diol.
912 Creamer et al. [136] demonstrated the use of biosynthesized
913 PdNPs to catalyze non-aqueous hydrogenation. Desulfovibrio desul- 4.2. Energy-related applications 961
914 furicans and B. sphaericus produced palladium catalyst, which
915 catalyzed the hydrogenation of 4-azidoaniline hydrochloride to The ability of different organisms to reduce and absorb precious 962
916 1,4-phenylenediamine and 3-nitrostyrene to 1-ethyl-3-nitroben- metal salts and form NPs has been used to enhance several aspects 963
917 zene in methanol. of fuel cell performance. Biogenic NPs have been used to produce 964
918 Unlike the aforementioned studies, Jia et al. [137] published a H2 fuel, to catalyze chemical oxidation of the fuel and to improve 965
919 method for PdNPs biosynthesis that does not require the H2 donor. power recovery (Table 11). 966
920 Biosynthetic PdNPs were formed by the reduction of palladium Several investigators have used biosynthesized PdNPs for H2 967
921 chloride in a crude extract of Gardenia jasminoides. The authors production. Bunge et al. [101] used three species of bacteria (Cupri- 968
922 measured catalytic hydrogenation of p-nitrotoluene and demon- avidus necator, Pseudomonas putida and Paracoccus denitrificans) to 969
923 strated a conversion of 100% at 5 MPa and 150 °C for 2 h, with a biosynthesize PdNPs for catalytic H2 production from hypophosph- 970
924 selectivity of 26.3% for the product p-methyl-cyclohexylamine. ite. Wu et al. [145] biosynthesized PdNPs with gardenia extract on 971

Table 10
Catalytic organic synthesis.

NP Organism used Application References

Pd D. desulfuricans, Bacillus sphaericus Hydrogenation of itaconic acid Creamer et al. [133]
Pd D. desulfuricans Hydrogenation of 2-pentane Bennett et al. [134]
Pd Rhodobacter capsulatus, Arthrobacter oxidans Hydrogenation of 2-butyne-1,4-diol Wood et al. [135]
Pd D. desulfuricans, B. sphaericus Hydrogenation, reduction and selective dehalogenation in non-aqueous solvents Creamer et al. [136]
Pd Gardenia jasminoides Hydrogenation of p-nitrotoluene Jia et al. [137]
Pd Cupriavidus necator, Pseudomonas putida Suzuki–Miyaura and Mizoroki–Heck reactions Søbjerg et al. [138]
Pd C. necator, Staphylococcus sciuri Suzuki–Miyaura, hydrogenation of (E)-3-(4-methoxyphenyl)-N-methylacrylamide Søbjerg et al. [139]
Pd C. necator, Staphylococcus sciuri 4-chloronitrobenzene reduction Søbjerg et al. [139]
Pd C. necator Catalysis of C–C bond formation Gauthier et al. [140]
Au Cacumen platycladi Propylene epoxidation Du et al. [141]
Au C. platycladi Propylene epoxidation Zhan et al. [142]
Au C. platycladi Styrene epoxidation Huang et al. [143]
Pt Honey Preparation of organic dye Venu et al. [144]

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972 TiO2 supports to enhance photocatalytic H2 evolution from pure Several studies have examined the electrical transmission prop- 1024
973 water. Macaskie et al. [146] provided a brief overview of bacterial erties of biosynthesized NPs incorporated into electrodes. In one 1025
974 hydrogenase activity for several applications, including waste study, dried whole plant extract from Scutellaria barbata was used 1026
975 decontamination, production of precious metal nanocatalyst and for the biosynthesis of AuNPs [153]. These AuNPs were applied to 1027
976 biohydrogen production. These authors also described how E. coli a glassy carbon electrode (GCE), and the authors found enhanced 1028
977 with modified hydrogenase and dehydrogenase regulation could electrical transmission between the modified electrode and PNP. 1029
978 be used to further enhance performance. Another study also demonstrated enhanced electrical transmission 1030
979 Biosynthesized NPs have been incorporated into fuel cells to using a GCE modified with AuNPs prepared from the flower extract 1031
980 catalyze chemical reactions and have been used in electrode con- of Rosa damascene [154]. This study employed cyclic voltammetry 1032
981 struction. Yong et al. [147] bioaccumulated Pt and Pd as NPs using in a solution of 0.1 M KCl and 5.0 mM [Fe(CN)6]3-/4- to demonstrate 1033
982 Desulfovibrio desulfuricans and mixed the dried biomaterial with an increase in the electronic transmission rate for the modified 1034
983 activated carbon powder to create carbon paper used in a commer- electrode. Sadhasivam et al. [16] performed cyclic voltammetry 1035
984 cial fuel cell system. Dimitriadis et al. [148] used yeast biomass studies using a three-electrode configuration employing AuNPs 1036
985 immobilized in polyvinyl alcohol (PVA) cryogels for the biorecov- biosynthesized by Streptomyces hygroscopicus. Platinum and Ag/ 1037
986 ery of platinum from aqueous solution, then directly incorporated AgCl were used as counter and reference electrodes, respectively, 1038
987 this PtNP–biomass–PVA material into a fuel cell. Another study and electrochemically coated Cu2O on a Pt substrate (Cu2O–Pt) 1039
988 described four different concentrations of biomass-supported pal- with an AuNPs–methylene blue monolayer was employed as the 1040
989 ladium NPs using Shewanella oneidensis as an electrode catalyst in a working electrode. 1041
990 polymer exchange membrane fuel cell [149]. Various electrochemical sensing applications can make use of 1042
991 Orozco et al. [150] studied the ability of PdNPs biosynthesized the unique properties of biosynthesized NPs. Jha and Prasad 1043
992 by two different strains of E. coli to both produce hydrogen via fer- [155] introduced a biosynthetic method to prepare ferroelectric 1044
993 mentation and convert the H2 into energy in a fuel cell. Both the BaTiO3 NPs using the bacterium Lactobacillus sp. The resulting 1045
994 parent strain MC4100 and the mutant strain IC007 were coated NPs were mixed with a PVDF solution then agitated and warmed 1046
995 with PdNPs after the bioreduction of palladium precursor, then until the mixture became viscous. The process resulted in thin 1047
996 modified and tested as anodes in a fuel cell. The mutant strain nanocomposite sheets that exhibited significantly enhanced 1048
997 IC007 showed a threefold greater power conversion compared dielectric properties. Torres-Chavolla et al. [156] biosynthesized 1049
998 with the parent strain, but produced about half of the power of AuNPs using three species of actinomycetes, Thermomonospora 1050
999 commercial Pd powder or biosynthesized PdNPs made with curvata, T. fusca and T. chromogena, and stabilized the NPs using 1051
1000 D. desulfuricans. the cross-linker glutaraldehyde for enhanced biosensing applica- 1052
1001 Yong et al. [151] described the coupling of waste biorefining tions. Shilov et al. [157] investigated different electrophysical 1053
1002 with fuel cell power generation using biosynthesis to recover pre- characteristics, such as cell zeta potential, surface conductivity, 1054
1003 cious metals and form nanocatalysts. Palladium was biorecovered electrophoretic mobility and the dispersion of cell conductivity, 1055
1004 from industrial processing waste and transformed into biosupport- of Candida albicans yeast cells with Ag precipitate prepared using 1056
1005 ed PdNPs using D. desulfuricans, E. coli and Cupriavidus metallidu- the reducer hydrazine. 1057
1006 rans. The study also described the biosynthesis and performance Du et al. [158] introduced the bioreduction of Au by E. coli cells 1058
1007 of a mixed metal catalyst produced from the waste stream. and their application for direct electrochemical sensing of hemo- 1059
globin. Biosynthesized AuNPs bound to the surface of the bacterial 1060

1008 4.3. Electrodes and sensors cells were incorporated on a GCE. The authors performed cyclic 1061
voltammetry measurements for different electrode configurations 1062

1009 Fundamental electrochemical phenomena can be better on small samples of hemoglobin placed directly on the electrode 1063

1010 understood through nanoscale science and nanotechnology, and surface. The results showed a pair of redox peaks with a formal 1064

1011 performance of electrodes and sensors can be altered or enhanced potential of 0.325 V vs. an Ag/AgCl reference electrode. This study 1065

1012 using biosynthesized nanoparticles. Several aspects of biosynthe- demonstrated that biosynthesized nanocomposites can assist elec- 1066

1013 sized metallic nanoparticles have been studied in detail, including tron transfer between hemoglobin and the surface of a GCE. 1067

1014 their surface chemistry, biological compatibility and electrical con- Biosynthesized CdSNPs have also been used to fabricate a het- 1068

1015 ductivity. For nanoelectrochemical applications, special attention erojunction with asymmetric electronic transfer properties [159]. 1069

1016 has been paid to AuNPs because they provide a suitable substrate Semiconducting wurtzite-type structured NPs were prepared using 1070

1017 for the immobilization of biomolecules without altering their bio- Schizosaccharomyces pombe. Tin-doped indium oxide-coated glass 1071

1018 logical activity, and they provide excellent electron transfer was covered by a thin film of spin-coated polyphenylene vinylene 1072

1019 between the biomolecule and the electrode surface [152]. The and washed with S. pombe. While polyphenylene vinylene is a 1073

1020 presence of capping agents and surfactants in biosynthesized p-type material, CdSNPs represent an n-type material. With added 1074

1021 AuNPs can modulate electrode functionality and may enhance Ag contacts, the resulting diode had a forward current of 1075

1022 the operating range or selectivity compared with conventional 75 mA cm2 at 10 V and experienced breakdown at approximately 1076

1023 materials (see Table 12). 15 V in reverse mode. 1077

Table 11
Energy-related applications.

NP Organism used Application References

Pd Cupriavidus necator, Pseudomonas putida, Paracoccus denitrificans Hydrogen production from hypophosphite Bunge et al. [101]
Pd/TiO2 Gardenia jasminoides Photocatalytic H2 evolution from pure water Wu et al. [145]
Pd Escherichia coli Biohydrogen production Macaskie et al.[146]
Pd Desulfovibrio desulfuricans fuel cell electrode Yong et al. [147]
Pt Saccharomyces cerevisiae Pt biorecovery, fuel cell electrode Dimitriadis et al.[148]
Pd S. oneidensis Fuel cell electrode Ogi et al. [149]
Pd E. coli Fuel cell electrode Orozco et al. [150]
Pd D. desulfuricans, E. coli, Cupriavidus metallidurans Waste biorefining, fuel cell electrode Yong et al. [151]

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Table 12
Electrodes and sensors.

NP Organism used Application References

Au Scutellaria barbata Direct electrochemistry of 4-NP Wang et al. [153]
Ag, Au Rosa damascena Modified glassy carbon electrode Ghoreishi et al. [154]
BaTiO3 Lactobacillus sp. Nanocomposite with significantly enhanced dielectric properties Jha and Prasad [155]
Au Thermomonospora curvata, T. fusca, T. chromogena Applications in enhanced biosensors Torres-Chavolla et al. [156]
Au Escherichia coli Direct electrochemistry of hemoglobin Du et al. [158]
CdS Schizosaccharomyces pombe Construction of ideal diode Kowshik et al. [159]
Au Black tea Capacitors construction Uddin et al. [160]
Au, Ag Solanum lycopersicum Metallic ion detection Bindhu and Umadevi [161]

1078 Biogenic AuNPs in polyvinyl alcohol–KH2PO4 films were used production and can produce magnetic particles at a fraction of 1115
1079 by Uddin et al. [160] to ameliorate the percolative behavior of the cost of traditional chemical synthesis [171]. 1116
1080 these nanocomposite films and to generate high dielectric permit- Telling et al. [172] employed MNPs to catalyze Cr(VI) reduction 1117
1081 tivity at room temperature. The performance of the material is (see also Section 3.4). MNPs were biosynthesized by Geobacter 1118
1082 promising for use in capacitors. sulfurreducens and the reduction of Cr(VI) to Cr(III) at sites within 1119
1083 The unique optical properties of metallic nanoparticles can be the magnetic spinel surface were studied using X-ray absorption 1120
1084 also used for chemical sensing. AuNPs and AgNPs reduced using and X-ray magnetic circular dichroism. The same group also 1121
1085 extract from the tomato Solanum lycopersicum were used for detec- investigated the use of biosynthesized magnetites produced by 1122
1086 tion of metallic ions, including Fe3+ and Cu4+, in water based on G. sulfurreducens for recovery of metal contaminants from water 1123
1087 subtle changes in their surface plasmon resonance spectra [161]. [173]. MNPs produced by the bacterial reduction of powdered 1124
schwertmannite (an iron-oxyhydroxysulfate mineral) were found 1125
1088 5. Applications for magnetically responsive NPs to be more efficient at reducing Cr(VI) than ferrihydrite (an 1126
oxyhydroxide mineral), ‘‘gel’’-derived biomagnetite and 1127
1089 Magnetotactic bacteria have a natural ability to synthesize commercial nanoscale Fe3O4. 1128
1090 magnetite NPs (MNPs), which are useful for various applications One key advantage of MNPs is the ease of collection and recov- 1129
1091 (Table 13). Only certain NP forms are synthesized spontaneously ery. Magnetic properties can also ensure that particles remain 1130
1092 by magnetotactic bacteria [162,163]. The biological synthesis of dispersed and distributed throughout a reaction vessel. Coker 1131
1093 magnetically responsive NPs is well established, and their use in et al. [174] employed MNPs synthesized by G. sulfurreducens as a 1132
1094 various medical, environmental and industrial applications has biomagnetic support for palladium nanocatalyst. The Pd-MNPs 1133
1095 been reviewed [164–166]. were used to catalyze the C–C bond-forming Mizoroki–Heck reac- 1134
1096 The yield and properties of MNPs can be manipulated and opti- tion, coupling iodobenzene to ethyl acrylate or styrene. Crean et al. 1135
1097 mized to suit a particular purpose. Kundu et al. [167] described [175] used a similar approach for the continuous removal of Cr(VI). 1136
1098 changes in magnetosome size, number, and alignment with bio-
1099 synthesis performed in the presence of Zn and Ni salts. Other 6. Biosynthesis of unique formulations and geometries 1137
1100 investigators have described the formation of zinc–ferrite NPs by
1101 Q9 Thermoanaerobacter strain TOR-39 [168]. Coker et al. [160] The properties and potential applications of nanoscale materials 1138
1102 described improvement of magnetic properties of biosynthesized are determined by their chemical composition, crystal structure, 1139
1103 magnetic NPs. In the study, FeCo-oxyhydroxides were created by particle size and particle shape. Several studies have described 1140
1104 adding CoCl2.6H2O to FeCl3 precursor and then treating them with the biosynthesis of NPs with unique compositions and/or physical 1141
1105 Geobacter sulfurreducens culture. The resulting cobalt ferrite forms that will modulate performance in a range of applications 1142
1106 (CoFe2O4) NPs exhibited dramatically enhanced magnetic proper- (Table 14). 1143
1107 ties compared with simultaneously produced magnetite MNPs. NPs with certain chemical compositions have been difficult to 1144
1108 Staniland et al. [169] described controlled cobalt doping of mag- synthesize using conventional chemical methods. Ahmad et al. 1145
1109 netosomes in vivo, where an estimated cobalt content of between [176] described fungal biosynthesis of transparent p-type 1146
1110 0.2 and 1.4% resulted in a 36–45% increase in the coercive field. Roh conducting oxide CuAlO2 NPs with Humicola sp. In this case, 1147
1111 et al. [170] also reported Co, Cr, Mn and Ni doping of magnetite traditional chemical synthesis is challenging because high 1148
1112 biosynthesized extracellularly by Thermoanaerobacter ethanolicus temperatures are necessary for overcoming reaction barriers, but 1149
1113 and a psychrotolerant Shewanella sp. In a follow-up report, these low temperatures are necessary for maintaining the Cu(1+) 1150
1114 authors described how the process is amenable to large-scale valence. Ankamwar et al. [177] introduced a biosynthetic approach 1151

Table 13
Application enhancements using magnetically responsive NPs.

NP Organism used Application References

Fe3O4 Thermoanaerobacter sp. TOR-39 Magnetite substituted with Zn Yeary et al. [168]
CoFe2O4 Geobacter sulfurreducens Enhanced magnetic properties of biosynthesized composite Coker et al. [174]
Fe3O4 Magnetospirillum gryphiswaldense, Magnetospirillum Cobalt doping of magnetosomes Staniland et al.
magnetotacticum [169]
Fe3O4 Thermoanaerobacter ethanolicus, Shewanella sp. Magnetite substituted with Co, Ni, Cr, Mn Roh et al. [170]
Fe3O4 Thermoanaerobacter sp. TOR-39 Magnetite substituted with Co, Ni, Cr, Mn, Zn and rare earth Moon et al. [171]
metals
Fe3O4 G. sulfurreducens Cr(VI) remediation Telling et al. [172]
Fe3O4 G. sulfurreducens Cr(VI) and Tc(VII) remediation Cutting et al. [173]
Fe3O4 G. sulfurreducens Magnetically recoverable Pd nanocatalyst Coker et al. [174]
Fe3O4 G. sulfurreducens Cr(VI) remediation Crean et al. [175]

Please cite this article in press as: Schröfel A et al. Applications of biosynthesized metallic nanoparticles – A review. Acta Biomater (2014), http://
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 ACTBIO 3244 No. of Pages 20, Model 5G
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16 A. Schröfel et al. / Acta Biomaterialia xxx (2014) xxx–xxx

Table 14
Unique formulations and geometries.

NP Organism used Application References

CuAlO2 Humicola sp. Difficult-to-synthesize NPs Ahmad et al. [176]
Au, Ag Emblica officinalis Phase transfer, transmetallation Ankamwar et al. [177]
Au–Ag–Cu Brassica juncea Alloy Haverkamp et al. [178]
Au–Ag Fusarium oxysporum Alloy Senapati et al. [179]
Au–Ag Fusarium semitectum Alloy Sawle et al. [180]
Au–Pd Escherichia coli Core/shell Au/Pd NPs Deplanche et al. [181]
Au Tamarindus indica Nanotriangles, vapor sensing Ankamwar et al. [182]
PbS, ZnS Streptococcus thermophilus, Hollow nanostructures; light harvesting Zhou et al. [122]
Lactobacillus bulgaricus, Lactobacillus acidophilus and photocatalytic properties
Au Hansenula anomala Bio-ink Sathish Kumar et al. [184]

1152 using transmetallation reactions. AgNPs and AuNPs phytosynthe- especially in medical applications, due to the potential introduc- 1202
1153 sized using Emblica officinalis fruit extract were transferred into tion of allergens or pathogens. 1203
1154 methanol solution using a cationic surfactant, and transmetallation Considering the volume and growth in NP biosynthesis research 1204
1155 was carried out between AgNPs and chloroaurate ions in in recent years, the field appears to be on the threshold of much 1205
1156 chloroform. more widespread and intensive research into applications. Q101206
1157 The creation of metal alloys by casting requires heavy Meanwhile, further research and development of the underlying 1207
1158 equipment and high temperatures. Bottom-up biosynthesis of biosynthesis methods themselves and the creation of novel biosyn- 1208
1159 Au–Ag–Cu alloys by Brassica juncea seed was introduced by Hav- thetic NP forms is anticipated. 1209
1160 erkamp et al. [178]. Similar studies reported bimetallic Au–Ag alloy
1161 biosynthesis employing the fungus Fusarium [179,180]. Deplanche Appendix A. Figures with essential colour discrimination 1210
1162 et al. [181] likewise introduced a hybrid two-step method for the
1163 production of core–shell Pd–Au NPs by means of E. coli cells. Certain figures in this article, particularly Figs. 1–4 are difficult 1211
1164 NP biosynthesis can also result in NPs with various useful to interpret in black and white. The full colour images can be found 1212
1165 shapes. Ankamwar et al. [182] described the phytosynthesis of in the on-line version, at doi:http://dx.doi.org/10.1016/j.actbio. 1213
1166 Au nanotriangles using tamarind (Tamarindus indica) leaf extract. 2014.05.022). 1214
1167 The authors measured the electrical conductivity of these
1168 triangular NPs in different organic solvents, and suggested a possi-
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Please cite this article in press as: Schröfel A et al. Applications of biosynthesized metallic nanoparticles – A review. Acta Biomater (2014), http://
dx.doi.org/10.1016/j.actbio.2014.05.022