Biological Nanofactories: Using Living Forms for Metal Nanoparticle Synthesis

Abstract

Metal nanoparticles are nanosized entities with dimensions of 1-100 nm that are increasingly in demand due to applications in diverse fields like electronics, sensing, environmental remediation, oil recovery and drug delivery. Metal nanoparticles possess large surface energy and properties different from bulk materials due to their small size, large surface area with free dangling bonds and higher reactivity. High cost and pernicious effects associated with the chemical and physical methods of nanoparticle synthesis are gradually paving the way for biological methods due to their eco-friendly nature. Considering the vast potentiality of microbes and plants as sources, biological synthesis can serve as a green technique for the synthesis of nanoparticles as an alternative to conventional methods. A number of reviews are available on green synthesis of nanoparticles but few have focused on covering the entire biological agents in this process. Therefore present paper describes the use of various living organisms like bacteria, fungi, algae, bryophytes and tracheophytes in the biological synthesis of metal nanoparticles, the mechanisms involved and the advantages associated therein.

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Biological Nanofactories: Using Living Forms for Metal Nanoparticle
Synthesis
Shilpi Srivastava1, Zeba Usmani2, Atanas G. Atanasov3, Vinod Kumar Singh4, Nagendra Pratap
Singh4, Ahmed M. Abdel-Azeem5, Ram Prasad6, Govind Gupta7, Minaxi Sharma8,* and
Atul Bhargava6,*
1Amity Institute of Biotechnology, Amity University Uttar Pradesh, Lucknow Campus, Lucknow, India; 2Department of
Chemistry and Biotechnology, Tallinn University of Technology, Tallinn, Estonia; 3Department of Pharmacognosy, Uni-
versity of Vienna, Austria; 4K.S. Saket P.G. College, Ayodhya, India; 5Botany Department, Faculty of Science, Universi-
ty of Suez Canal, Ismailia, Egypt; 6Department of Botany, Mahatma Gandhi Central University, Motihari, Bihar, India;
7Sage School of Agriculture, Sage University, Bhopal, India; 8Department of Food Technology, Akal College of Agricul-
ture, Eternal University, Baru Sahib, Himachal Pradesh, India
Abstract: Metal nanoparticles are nanosized entities with dimensions of 1-100 nm that are increasing-
ly in demand due to applications in diverse fields like electronics, sensing, environmental remediation,
oil recovery and drug delivery. Metal nanoparticles possess large surface energy and properties differ-
ent from bulk materials due to their small size, large surface area with free dangling bonds and higher
reactivity. High cost and pernicious effects associated with the chemical and physical methods of na-
noparticle synthesis are gradually paving the way for biological methods due to their eco-friendly na-
ture. Considering the vast potentiality of microbes and plants as sources, biological synthesis can
serve as a green technique for the synthesis of nanoparticles as an alternative to conventional methods.
A number of reviews are available on green synthesis of nanoparticles but few have focused on cover-
ing the entire biological agents in this process. Therefore present paper describes the use of various
living organisms like bacteria, fungi, algae, bryophytes and tracheophytes in the biological synthesis
of metal nanoparticles, the mechanisms involved and the advantages associated therein.
A R T I C L E H I S T O R Y
Received: May 04, 2020
Revised: August 21, 2020
Accepted: September 08, 2020
DOI:
10.2174/1389557520999201116163012
Keywords: Metal nanoparticles, green nanotechnology, bacteria, fungi, lower plants, angiosperms.
1. INTRODUCTION
Nanotechnology has been defined as “the understanding
and control of matter at dimensions of roughly 1-100 na-
nometers, where unique phenomena enable novel applica-
tions” [1]. A nanometer (nm), an SI (Syst`eme International
d’Unit´es) unit of length, is 10-9 or a distance of one-billionth
of a meter [3, 4]. Nanotechnology enables the fabrication,
characterization, production, and utilization of structures,
devices, and systems at the nanometer scale, and has gained
attention in the last few decades due to immense applications
in energy, medicine, pharmaceutical, food, electronics, and
space industries [2, 3]. Nanotechnology aims at the shifting
down of multiple scientific disciplines like physics, chemis-
try, biology, materials science, food science, information
technology and engineering to the molecular level [5]. The
* Address correspondence to this author at the Department of Botany, Ma-
hatma Gandhi Central University, Motihari, Bihar, India; Department of
Food Technology, Akal College of Agriculture, Eternal University, Baru
Sahib, Himachal Pradesh, India; E-mails: atulbhargava@mgcub.ac.in;
minaxi86sharma@gmail.com
concept of nanotechnology was put forward in 1959 by
Richard Feynman in a lecture entitled “There’s Plenty of
Room at the Bottom” at the annual meeting of the American
Physical Society. About 15 years later, the term ‘nanotech-
nology’ was coined by Norio Tanigutchi while describing
precision manufacturing at the scale of nanometres. Nanobi-
otechnology is the combination of nanoscience with biotech-
nology that enables mankind to design and produce func-
tionalized biological materials or devices taking advantage of
elements or effects that occur at the nanometer scale [6]. The
interdisciplinary nature is at the core of nanobiotechnology,
which spans across all branches of science, engineering,
technology, and encompasses their diverse applications [3, 7,
8]. Nanomaterials have potential applications in diverse
fields like electronics and photonics, information technology,
energy, magnetic separation, chemical sensing and imaging,
environmental science, food industry, diagnostics, drug de-
livery and biological labeling [9-14]. Nanotechnology,
termed as the next industrial revolution, has stimulated re-
search and innovative thinking throughout the scientific
world.

246 Mini-Reviews in Medicinal Chemistry, 2021, Vol. 21, No. 2 Srivastava et al.
Metal nanoparticles are nanosized metals with dimen-
sions of 1-100 nm and composed mostly of heavy metals
having a density of > 5 g/cm3 [15]. These metals are transi-
tion elements with the d orbital of the atom being partially
filled. Their main features also include a unique transition
between molecular and metallic states, a short-range order-
ing and the higher number of kinks, corners and edges [16,
17]. Metal nanoparticles possess large surface energy which
enables them to adsorb small molecules, thereby conferring
numerous environmental and bioanalytical applications.
Metal nanoparticles possess unique properties that are differ-
ent from bulk materials due to their small sizes, large surface
area with free dangling bonds that generate high local ener-
gy, and higher reactivity over their bulk counterparts [18-
21]. A suitable modification in the size, shape and chemical
composition of the materials can lead to precise manipula-
tion in the electrical, chemical, optical, and other properties
of the nanoparticles. Also, the optical, electronic, and cata-
lytic properties of metal nanoparticles are greatly influenced
by their size, shape, and crystal structure [22]. Currently na-
noscale analogs are increasingly being explored due to their
unusual functional attributes quite unlike the bulk. However,
the use of nanomaterials has been questioned due to their
miniature size, surface modification, easy interaction with
biological systems and possible nonbiodegradable composi-
tion that facilitates their rapid distribution and bioaccumula-
tion in the environment with consequences that are unknown
today [23]. The toxic nature of nanoparticles is not only
mass-dependent but may also depend on the physical and
chemical properties that are normally not considered in rou-
tine toxicoligical studies [24-27].
The popularity and use of metal nanoparticles are on the
upswing due to their immense use in biomedical sciences,
especially as diagnostic and therapeutic agents [28, 29]. The
general applications of metal nanoparticles in biological sci-
ences are depicted in Fig. (1) [30]. Gold and silver nanopar-
ticles are in much demand in biomedical science since they
exhibit broad spectrum antimicrobial activity against a wide
range of pathogens [31-38]. Antifungal activities of a num-
ber of metal nanoparticles have also been extensively report-
ed [39-43]. Metal and metal oxide nanoparticles are widely
used in commercial medical and consumer products like self-
cleaning coatings, topical sunscreens, and antimicrobial de-
tergents [44-46]. Antiviral activity of metal nanoparticles has
also been reported in recent years [47-53]. Silver nanoparti-
cles are larvicidal against filariasis, malaria vectors and other
plasmodial pathogens [54-61]. Recently, broad range of po-
tential applications of nanotechnology has been suggested in
agriculture [62] especially for the design and development of
novel tools for sustainable agriculture [62-65]. The metals
and metal oxide nanomaterials absorb environmental con-
taminants that aid in increasing soil remediation capacity and
reduction in the times and costs of the treatments [66].
Synthesis of metal nanoparticles has been carried out
through two approaches viz. the top down and the bottom up
approaches (Fig. 2) [67-69]. In the top down approach, a big
component is broken down into smaller ones of the desired
size, while the bottom up approach is primarily based on
atomic transformations and molecular condensation. The
physical methods are energy intensive, require costly vacu-
um systems or equipment to prepare nanoparticles, besides
having limitations like the use of high temperature [70-71].
Several dry methods like the use of UV irradiation, aerosols
and lithography are also not considered environmentally
friendly [22]. The wet-chemical methods that have been
conventionally used for the synthesis of nanoparticles in-
volve growing nanoparticles in a liquid medium containing
various reactants, particularly the reducing agents like potas-
Fig. (1). Applications of metal nanoparticles [30].

Using Living Forms for Metal Nanoparticle Synthesis Mini-Reviews in Medicinal Chemistry, 2020, Vol. 20, No. 2 247
sium bitartrate (KC4H5O6) [72], methoxypolyethylene glycol
[73], tri-sodium citrate and hydrazine (N2H4) [74]. The reac-
tion mixture is also supplemented with a stabilizing agent
such as sodium dodecyl benzyl sulfate or polyvinyl pyrroli-
done to prevent the agglomeration of metallic nanoparticles
[75]. The wet chemical methods have drawbacks like being
capital extensive and use of toxic solvents like Tetrakis (hy-
droxymethyl)phosphonium chloride (THPC) [Chemical for-
mula: (HOCH2)4PCl], poly-N-vinyl pyrrolidone (PVP)
[Chemical formula: (C6H9NO)n], and hydroxylamine
(H3NO), generation of hazardous byproducts and the imper-
fection of the surface structure [76, 77]. The chemical meth-
ods generally increase particle reactivity and toxicity, and
produce toxic wastes that might harm human health and the
environment [76]. Toxic chemicals accumulate on nanoparti-
cles and non-polar solvents that often limit their applications
in medical biology. These production methods are expen-
sive, labor-intensive, and are potentially hazardous to the
environment as whole and living organisms in particular
[78]. Thus, there is an urgent need to develop environmental-
ly friendly methods for the synthesis of nanoparticles using
techniques that are clean, biocompatible and non-toxic [79-
81].
Recently ‘green’ environmentally friendly processes in
chemistry and chemical technology have been accorded pri-
ority and are becoming increasingly popular due to world-
wide problems associated with environmental contamination
[78-82]. The term ‘green chemistry’, coined by P.T. Anastas
in 1991, focuses on the design of chemical products to min-
imize their inherent hazard. Green nanotechnology is an off-
shoot of green chemistry and refers to the application of sus-
tainable chemistry and eco-friendly engineering approaches
to evolve methods, materials and techniques in nanotechnol-
ogy for diverse applications ranging from energy generation
to non-toxic cleaning products [23]. It aims at effectively
reducing the potential environmental, health, and safety risks
associated with the manufacture and use of nano-scale prod-
ucts [83, 84]. Green nanotechnology also aims to make more
resource efficient, inherently safer design molecules, manu-
facturing processes for nanomaterials and products more
environmentally friendly.
2. BIOLOGICAL SYNTHESIS OF NANOPARTICLES
Within the realm of green chemistry, the synthesis of na-
noparticles from various biological sources is a rapidly up-
coming area that has caught the attention of researchers
working in line with long term sustainability goals. Green
synthesis using living forms is a bottom up approach that is
similar to the chemical reduction method with the difference
in the use of a natural product instead of an expensive chem-
ical reducing agent [85]. The chemical and physical methods
of nanoparticle synthesis are gradually paving the way for
ecofriendly biological methods due to cost and environmen-
tal toxicity factors [86]. Use of living organisms or their bi-
omass could be an alternative to the conventional chemical
and physical methods of nanoparticle synthesis [86-88].
Apart from being inexpensive and ecofriendly, the biological
process enables the recycling of expensive metal salts like
gold and silver contained in water bodies. Biological synthe-
sis of nanoparticles also allows easy separation of the nano-
particles from the reaction media or up concentration by cen-
trifugation [89]. Moreover, the coating of biological mole-
cules on the surface of nanoparticles makes them biocompat-
ible in comparison with the nanoparticles obtained by chem-
ical methods [90-92]. The biocompatibility of biologically
synthesized nanoparticles offers very interesting applications
in biomedicine and related fields [93].
A great deal of effort has been put into the biosynthesis
of metal nanoparticles using different living forms like
Fig. (2). Bottom-up and top-down approaches for nanoparticle production [67].

248 Mini-Reviews in Medicinal Chemistry, 2021, Vol. 21, No. 2 Srivastava et al.
Fig. (3). Diagram summarizing the possible mechanism of biologically mediated synthesis of nanoparticles [96].
prokaryotes (bacteria) to eukaryotes (fungi), virus and plants
(non-vascular to the vascular system). These living entities
can serve as biological nanofactories for the production of
nanomaterials due to their wide distribution along the eco-
logical boundaries, easy availability, safety in handling and
presence of a broad range of metabolites [94]. The size and
shape of nanoparticles are determined by the nature of bio-
logical entities, their concentrations and the type of organic
reducing agents [95]. The dimensions of the nanoparticles
are also strongly influenced by the type of growth medium
parameters such as pH, temperature, salt concentration and
exposure time [96]. The prokaryotic bacterial cells and the
extracts of multicellular eukaryotes reduce the metal precur-
sors to form nanoparticles of desired size and shapes [97].
Apart from this, biological entities possess capping and sta-
bilizing agents required for inhibition of the aggrega-
tion/agglomeration process and termination of growth [78,
98]. Bio-reduction of metal precursors can take place both in
vitro or in vivo wherein biomolecules (enzymes, proteins and
sugars) and phytochemicals (flavonoids, phenolics and ter-
penoids) enhance the stability and persistence of nanoparti-
cles by acting as reducing as well as stabilizing agents (Fig. 3)
[78, 98]. The cations formed after dissociation of metal salts
are saturated to form hydroxyl complexes followed by crys-
tallite growth of metal with oxygen leading to the formation
of crystalline planes having different energy levels. This
carries on till the activation of the capping agent that ulti-
mately arrests the growth of high-energy atomic growth
planes, the process ending with the formation of metal nano-
particles. The newly formed nanoparticles are in a high-
surface energy state and tend to convert to their low-surface
energy conformations by aggregation. The presence of high-
er con of reducing agents and stabilizing agents prevents the
aggregation of nanoparticles and promotes the production of
smaller NPs. Additionally, proteins can trap metal ions on
their surface and convert them to their corresponding nuclei,
which could further aggregate and, consequently, form NPs
Considering the vast potentiality of microbes and plants as
sources, the biological synthesis can serve as a green tech-
nique for the synthesis of nanoparticles as an alternative to
conventional methods.
3. GREEN SYNTHESIS OF NANOPARTICLES BY
BACTERIA AND FUNGI
3.1. Bacteria
Prokaryotes possess numerous advantages for nanoparti-
cle synthesis over eukaryotic systems like faster growth rates
and inherent mechanisms to overcome the extreme toxicity
of heavy metals that constitute the core of these nanoparti-
cles [99]. These mechanisms include processes such as metal
reduction and/or precipitation, generating nontoxic or less
toxic metal nanoarrays [80]. Due to their relative ease of
manipulation, bacteria have been extensively utilized in the
production of metallic nanoparticles (Table 1). Bacteria are
abundantly found in the environment, are fast growing, less
expensive to cultivate and adapt easily to extreme condi-
tions. Besides this, the growth conditions such as tempera-
ture, oxygenation and incubation time can also be easily ma-
nipulated. Both intracellular and extracellular production of
silver, gold, cadmium and sulphide nanoparticles by bacteria
has been reported by different workers [147]. The extracellu-
lar synthesis of nanoparticles is rapidly gaining ground and
the bacterial cells could prove to be a potential source for the
synthesis of metal nanoparticles instead of physical and
chemical procedures [147]. The possible mechanism of na-
noparticle formation by bacteria includes alteration of solu-
bility and toxicity via redox reactions, biosorption, bioaccu-
mulation, extracellular complexation or precipitation of met-
als. Although enzymes are known to play a major role in the
bioreduction process of Au3+, Pd2+, Fe3+, U6+, Tc7+, Ni2+ and
Cr6+ [109, 148-150], prokaryotic microbes like Bacillus
megaterium D01 and Lactobacillus sp. A09 are known to
reduce metal ions via nonenzymatic mechanisms like inter-
action with groups like ionized carboxyl of amino acid

Using Living Forms for Metal Nanoparticle Synthesis Mini-Reviews in Medicinal Chemistry, 2020, Vol. 20, No. 2 249
Table 1. List of nanoparticles synthesized by bacteria and fungi.
Scientific Name
Nanoparticle
Size (nm)
Refs.
Bacteria
Acinetobacter sp.
Silver
10-18
[100]
Bacillus brevis
Silver
41-68
[101]
Bacillus haynesii
Zinc oxide
50
[102]
Bacillus mycoides
Titanium dioxide
40-60
[103]
Bacillus thuringiensis
Silver
43.52-142.97
[104]
Brevibacterium casei
Silver
10-50
[105]
Clostridium pasteurianum
Molybdenum
5-20
[106]
Enterobacter cloacae
Silver
7-25
[107]
Geobacillus sp.
Gold
5-50
[108]
Geobacter sulfurreducens
Silver
30
[109]
Gluconobacter roseus
Silver
10
[110]
Halococcus salifodinae
Selenium
28
[111]
Idiomarina sp.
Silver
26
[112]
Klebsiella pneumoniae
Silver
15-37
[113]
Lactobacillus rhamnosus
Silver
233
[114]
Morganella spp.
Silver
10-50
[115]
Proteus mirabilis
Silver
10-20
[116]
Pseudomonas fluorescens
Gold
50-70
[117]
Pseudomonas fragi
CdS Quantum dots
2-16
[118]
Rhodobacter capsulatus
Tellurium
200-700
[119]
Salmonella typhirium
Silver
87
[120]
Shewanella algae
Platinum
5
[121]
Streptomyces sp.
Iron
65-86.7
[122]
Ureibacillus thermosphaericus
Silver
10-100
[123]
Vibrio natriegens
Selenium
100-400
[124]
Xanthomonas oryzae
Silver
14.86
[125]
Fungi
Agaricus bisporus
Gold
2-5
[126]
Agaricus arvensis
Selenium
150-550
[126]
Alternaria alternata
Gold
12
[127]
Amylomyces rouxii
Silver
5-27
[128]
Arthroderma fulvum
Silver
15.5
[42]
Aspergillus versicolor
Copper
23-82
[129]
Aspergillus niger
Zinc oxide
53-69
[130]
(Table 1) contd…

250 Mini-Reviews in Medicinal Chemistry, 2021, Vol. 21, No. 2 Srivastava et al.
Scientific Name
Nanoparticle
Size (nm)
Refs.
Candida albicans
Silver
20-80
[131]
Duddingtonia flagrans
Silver
10.29-12.17
[132]
Emericella nidulans
Silver
10-20
[133]
Epicoccum nigrum
Silver
1-22
[134]
Fusarium oxysporum
Cadmium-selenide
Silver
11
1-50
[135]
[136]
Lentinus sajor caju
Silver
53
[137]
Macrophomina phaseolina
Silver
5-40
[138]
Neurospora crassa
Platinum
4-35
[139]
Penicillium italicum
Silver
32-100
[140]
Pleurotus sp
Iron
-
[141]
Phaenerochaete chrysosporium
Silver
34-90
[142]
Phoma sp.
Silver
71.06
[143]
Schizophyllum commune
Silver
1-100
[144]
Trichoderma longibrachiatum
Silver
10
[145]
Trichosporon jirovecii
Cadmium sulfide
6-15
[146]
residues and the amide of peptide chains on the microbial
cell wall [151, 152]. The reduction of ions or the formation
of water insoluble complexes by bacteria is in fact, a defense
mechanism employed by the microbe to overcome the toxici-
ty of the metal ions.
Another interesting application area using bacteria is the
production of gold (Au) nanoparticles since some bacteria
have developed resistance mechanisms to the inert metal by
activating discrete metabolic pathways that reduce ionic gold
to solid gold and aid in green synthesis of gold nanoparticles
besides metal detoxification and recovery of gold. Several
bacteria have been utilized in the biomineralization of gold
from solutions, notably Bacillus subtilis, Shewanella algae,
Rhodopseudomonas capsulata, Cupriavidus metallidurans
and Delftia acidovorans [153-157]. Studies with the Gram-
negative β-proteobacterium C. metallidurans have revealed
that it takes up aqueous Au complexes and forms inert gold
nanoparticles within its cytoplasm, thus actively detoxifying
Au complexes via efflux and reductive precipitation [153,
154]. D. acidovorans, another Gram-negative non-spore-
forming bacterium is reported to secrete a secondary metabo-
lite that causes gold mineralization and protects the bacte-
rium from the toxic effects of gold, a mechanism mediated
by the secretion of the ribosomal extracellular peptide delfti-
bactin [155]. This offers unique opportunities for biological
synthesis of AuNPs, and recovery of gold from the environ-
ment. In a recent study [158], D. acidovorans neutralized
Ag3+ ions present in the medium by excreting a nonriboso-
mal peptide formed extracellular gold nanonuggets via com-
plexation with metal ions.
3.2. Fungi
Fungi have been at the forefront of metallic nanoparticle
synthesis due to their metal tolerance and bioaccumulation
ability, ease in handling and efficient scale-up mechanisms
[75]. Fungi also secrete higher amounts of proteins than bac-
teria which directly translate to higher productivity of nano-
particle formation [88]. Fungi secrete specific enzymes that
aid in the synthesis of nanoparticles which would lead to the
possibility of genetically modified microorganisms to over
express specific reducing molecules and capping agents and
thereby control the size and shape of the biogenic nanoparti-
cles [159]. However, the genetic manipulation of fungi for
overexpression of specific enzymes that facilitate nanoparti-
cle synthesis is more cumbersome in fungi as compared to
prokaryotic cells [75]. Numerous fungi have been found to
produce gold, silver, platinum, cadmium and titanium diox-
ide nanoparticles both at intracellular and extracellular levels
(Table 1). Metal nanoparticles have even been produced
from giant oyster mushroom [160], branched oyster mush-
room [161] and pearl oyster mushroom [162]. Biological
synthesis of metal nanoparticles using fungi may be intracel-
lular or extracellular. Intracellular synthesis involves the
addition of the metal precursor to the fungal culture which is
later internalized in the biomass. Due to this, the nanoparti-
cles have to be extracted by disrupting the biomass using
chemical methods, centrifugation, and filtration [163, 164].
Extracellular synthesis, the most widely employed method,
entails addition of the metal precursor to the aqueous fungal
filtrate that contains only the biomolecules leading to the
formation of nanoparticles in the medium [165-168]. Several

Using Living Forms for Metal Nanoparticle Synthesis Mini-Reviews in Medicinal Chemistry, 2020, Vol. 20, No. 2 251
enzymes like nicotinamide adenine dinucleotide (NADH),
NADH-dependent nitrate reductase, oxidoreductases, ni-
trate/nitrite reductase, sulfate and sulfite reductase and hy-
drolases play an important role in the green synthesis of met-
al nanoparticles [169, 170]. Although the intracellular for-
mation mechanism of AuNPs and AgNPs by fungi has not
been fully worked out, it has been speculated that electrostat-
ic interaction is responsible for the binding of gold and silver
ions on the fungal cell surface [22]. The enzymes present in
the cell wall reduce the adsorbed metal ions, leading to the
formation of the metal nuclei, which subsequently grow
through further reduction of metal ions.
Fusarium, a ubiquitous, anamorphic filamentous fungus
widely distributed in soil, water, subterranean and aerial
plant parts, plant debris and other organic substrates have
been extensively used for the synthesis of silver nanoparti-
cles and needs special mention [171]. Although most species
are harmless saprobes and members of the soil microbial
community, many species are mycotoxin producers and are
pathogenic to plants and humans [40]. F. oxysporum reduces
metal ions action of reductase enzymes and electron shuttle
quinones extracellularly to generate nanoparticles of con-
sistent size distribution [172, 173]. Biosynthesis of metal
nanoparticles has also been carried out using dead biomass
of a number of fungi [174-176].
Fungi provide numerous advantages as compared to other
microorganisms in the production of nanoparticles. The fun-
gal mycelium can withstand a considerable amount of flow,
pressure, agitation and other conditions in bioreactors or
other chambers as compared to prokaryotic bacterial cells as
well as plants [147]. The fungal cells grow rapidly, are easy
to handle and fabricate. The extracellular secretion of pro-
teins is more which can be easily handled in downstream
processing. There is an absence of cellular components since
the nanoparticles precipitate outside the cell, and therefore
the nanoparticles produced can be directly used in various
applications [147]. However, the main limitation of using
fungi in nanoparticle production is the pathogenic nature of
the filamentous fungi that have been extensively used for the
purpose of extracellular biomass free synthesis. The handling
and disposal of the biomass is a major source of inconven-
ience toward the commercialization of the process. There-
fore, there is a need for the development of novel approaches
of utilizing nonpathogenic species for the successful synthe-
sis and capping of nanosized particles. Significant efforts
have been made in this direction by utilizing nonpathogenic
fungus like Neurospora and Trichoderma [177]. Silver na-
noparticles of 51 nm size range were synthesized from
Trichoderma harzianum [145]. Silver nanoparticles were
synthesized using a filtrate of T. harzianum and average size
distribution of 58.0"±"4.0"nm was obtained, with a concentra-
tion of 3.16"×"1012 nanoparticles/mL [178].
4. ALGAE
Algae denote a polyphyletic, non-cohesive and artificial
assemblage of oxygen evolving photosynthetic organisms
[179]. Apart from their immense ecological significance,
these oxygenic photosynthesizers other than embryophyte
land plants are known to account for more than half the total
primary productivity [180].
Biological synthesis of nanoparticles using algae has be-
come prevalent in the last few years due to their easy access
and efficacy [181] (Table 2). However, there has been less
exploitation of the biomolecules present in the algal extract
in comparison to fungi, bacteria or plants. In algae, the re-
duction and fabrication of metal and metal oxide nanoparti-
cles are possibly mediated by the amino and carboxyl func-
tional groups and enzymes present in the algal cell walls that
act as reducing agents at ambient conditions. Nanoparticle
production has been reported from virtually all algal groups,
including blue green algae, green algae, diatoms, brown al-
gae and red algae [191, 192, 222, 223]. Synthesis of metal
and metal oxide nanoparticles of well-defined shape and size
depends on the concentration of algal extract/biomass, pH of
the reaction mixture, temperature, incubation time and the
type of metal salt used [165]. For example, an increase in the
size of the nanoparticles, with an increase in temperature has
been observed [171].
Thus, the use of algae for nanoparticle synthesis provides
an ecofriendly, low priced technology that avoids the toxic
chemicals and the high energy demand required for physio-
chemical fabrication [224]. Various algal biomolecules like
proteins, polysaccharides, amines, amino acids, alcohols,
pigments, carboxylic acids, carbohydrates and sugars have
been shown to reduce agents. These large amphiphilic mole-
cules act as surfactants causing aggregation of the surfactant
at the surface and reduce the surface tension as well as the
orientation of the molecule at the surface. They also reduce
interfacial energy by acting as capping agents and also serve
as stabilizing agents for the fabricated nanoparticles. Marine
microalgae have more potential in reducing metal salts to
nanoparticles since they are more exposed to salts in the
seawater. However, a big challenge in their utilization is the
fabrication of monodispersed nanoparticles that is not easy to
achieve even in the presence of long chain surfactant mole-
cules.
5. PLANTS
5.1. Bryophytes
Bryophytes consist of non-vascular plants inhabiting
moist environments that are an important component of eco-
system biodiversity [225, 226]. Bryophytes, considered as
early-diverging land plants having about 23000 species
worldwide, have been broadly classified into liverworts,
mosses and hornworts [227, 228]. In these embryophytes,
the sporophyte is permanently associated with the gameto-
phyte and never establishes direct contact with the substra-
tum [229]. Molecular phylogenetic studies have indicated
that the three extant bryophyte lineages (liverworts, mosses
and hornworts) separated before the lineage ancestral to pre-
sent-day tracheophytes [230].
The use of bryophytes for nanoparticle production is a
comparatively recent phenomenon and has come to the fore-
front only during the last decade. However, available litera-
ture at our disposal points out that currently, the use of bryo-
phytes for nanoparticle synthesis is rather limited (Table 2).
In fact this plant group is one of the least explored concern-
ing nanoparticle production. Earnest efforts are required for

252 Mini-Reviews in Medicinal Chemistry, 2021, Vol. 21, No. 2 Srivastava et al.
Table 2. List of nanoparticles synthesized by algae, bryophytes, pteridophytes and gymnosperms.
Plant Group
Nanoparticle
Size (nm)
Refs.
Algae
Botryococcus braunii
Copper
10-70
[182]
Caulerpa serrulata
Silver
10
[183]
Chaetomorpha linum
Silver
3-44
[184]
Chlorella vulgaris
Gold
2-10
[185]
Cladosiphon okamuranus
Gold
8-10
[186]
Cystoseira trinodis
Copper oxide
6-7.8
[187]
Ecklonia cava
Gold
30
[188]
Fucus vesiculosus
Gold
-
[189]
Galaxaura elongate
Gold
3.85-77.13
[190]
Navicula
Silver
70-80
[191]
Padina pavonia
Silver
49.58-86.37
[192]
Prasiola crispa
Gold
5-25
[193]
Rhizoclonium
Gold
16
[194]
Sargassum wightii
Zirconia
5
[195]
Stoechospermum marginatum
Gold
18.7-93.7
[196]
Stephanopyxis turris
Gold
10-30
[197]
Turbinaria conoides
Gold
2-19
[198]
Tetraselmis kochinensis
Gold
5-35
[199]
Bryophytes
Anthoceros
Silver
20-50
[200]
Campylopus flexuosus
Silver
50-70
[201]
Fissidens minutus
Silver
-
[202]
Riccia sp.
Silver
20-50
[203]
Pteridophytes
Adiantum philippense
Gold, Silver
10-18
[204]
Azolla microphylla
Gold
3-20
[205]
Dicranopteris linearis
Silver
40-60
[206]
Gleichenia pectinata
Silver
7.51
[207]
Pteridium aquilinum
Silver
1-50
[61]
Pteris tripartita
Silver
32
[208]
Salvinia minima
Lead
17.2
[209]
Salvinia molesta
Silver
10
[210]
Gymnosperms
Cupressus goveniana
Gold
-
[211]
(Table 2) contd…

Using Living Forms for Metal Nanoparticle Synthesis Mini-Reviews in Medicinal Chemistry, 2020, Vol. 20, No. 2 253
Plant Group
Nanoparticle
Size (nm)
Refs.
Cupressus sempervirens
Silver
10-80
[212]
Cycas sp.
Silver
2-6
[213]
Ephedra intermedia
Silver
10-36
[214]
Ephedra procera
Silver
20.4
[215]
Ginkgo biloba
Silver
15-500
[216]
Juniper communis
Gold
40-70
[217]
Pinus densiflora
Silver
30-80
[218]
Pinus eldarica
Silver
10-40
[219]
Platycladus orientalis
Platinum
2.4
[220]
Taxus yunnanensis
Silver
6.4-27.2
[221]
exploring bryophytes in the fabrication of nanoparticles for
diverse uses.
5.2. Pteridophytes
Like bryophytes, the use of pteridophytes for biological
production has been limited and has been restricted to stud-
ies in a few genera (Table 2). Sant et al. [204] assessed the
potential of an aqueous extract of Adiantum philippense L.
fronds for the green synthesis of gold and silver nanoparti-
cles. The particle size of AuNPs and AgNPs ranged between
10 and 18"nm was obtained. Baskaran et al. [208] synthe-
sized silver nanoparticles using an aqueous leaf extract of
Pteris tripartita, a critically endangered fern and obtained
nanoparticles in the range of 22-41 nm. The nanoparticles
obtained were of different morphologies like hexagonal,
sphere, and rod-shaped. Biosynthesis of silver nanoparticles
was carried out using the aqueous leaf-extract of an aquatic
fern, Salvinia molesta [210]. Spherical shaped AgNPs with
size ranging from 1 nm to 35 nm were obtained. Due to the
paucity of studies in the use of pteridophytes for nanoparticle
production, a lot needs to be done with respect to the explo-
ration of this plant group for effective utilization in further-
ing green nanotechnology.
5.3. Gymnosperms
There are 5 known lineages of seed plants viz. cycads, co-
nifers, Ginkgo, gnetophytes and angiosperms that inhabit dif-
ferent world regions. The first four comprise gymnosperms, a
group having about 1000 species and characterized by the
presence of a naked ovule before fertilization [231]. Gymno-
sperm is an emerging group that has recently drawn great in-
terest from the scientific community for the biogenic synthesis
of metal nanoparticles. All the four major groups of gymno-
sperms mentioned above have been utilized for the production
of metal nanoparticles and almost all the studies involving
gymnosperms have been carried out in the last decade (Table 2).
Zheng et al. [220] synthesized platinum nanoparticles by
reducing Na2PtCl4 with Cacumen platycladi extract. Cacu-
men platycladi is the tender twig and leaf of Platycladus
orientalis (L.) (Family: Cupressaceae). The results showed
that platinum nanoparticles of 2.4±0.8 nm were obtained
under the reaction temperature of 90°C, 70 % concentration
of extract, 0.5 mM Pt(II) concentration and a reaction time of
25h. Reducing sugars and flavonoids were found to be main-
ly responsible for the bioreduction mechanism.
5.4. Angiosperms
Angiosperms include flowering plants that possess seeds
enclosed in a capsule and dominate the terrestrial biota with
about 300000 species besides being major sources of food
and medicine [232, 233]. Angiosperms have dominated
earth's vegetation since the mid-Cretaceous and are widely
distributed along diverse ecological boundaries [234]. Alt-
hough the ability of plant extracts to reduce metal ions has
been known since long, the use of plants or plant extracts for
reducing metal salts to produce nanoparticles is underutilized
and has gathered pace only within the last 2-3 decades (Ta-
ble 3). Plant extracts may act as reducing as well as stabiliz-
ing agents during the synthesis of nanoparticles. Plant ex-
tracts of different plant species influence the characteristics
of the nanoparticles since these extracts vary in the concen-
tration and combination of reducing agents [86]. For plant
extract-mediated synthesis of nanoparticles, an aqueous ex-
tract of the plant is made and treated with an aqueous solu-
tion of the metal salt [31]. The reaction is carried out at room
temperature and the production of nanoparticles is completed
within a short duration. The size and shape of these biologi-
cally synthesized nanoparticles are dependent on the nature
of the plant extract containing different combinations and
concentrations of biomolecules, pH (acidic, basic, or neu-
tral), incubation temperature, reaction time, and the electro-
chemical potential of the ion. The reduction potential of the
ion or complex to be reduced significantly influences the rate
of nanoparticle production [259]. Plants are more efficient in
reducing metal ions having a large positive electrochemical
potential [259]. Higher temperatures are known to increase
the reaction rate that in turn enhances nanoparticle synthesis
along with an effect on the structural form of the synthesized
nanoparticles [260]. Also the reducing capacity and synthesis

254 Mini-Reviews in Medicinal Chemistry, 2021, Vol. 21, No. 2 Srivastava et al.
of nanoparticles by plant is not unlimited despite the varying
concentration of the metal ions in solution.
Different plant parts like root, stem, leaves, flowers, fruit,
seed, bark, peel and pulp have been utilized for the synthesis
of nanoparticles (Table 3). It is interesting to note that this
ability to produce nanoparticles has been observed across
angiospermic families and includes not just the economically
important plants but medicinal ones, and even common
weeds. The production of nanoparticles from weeds opens
up new avenues for their utilization in this upcoming excit-
ing technology.
Plant mediated synthesis of metal nanoparticles is
thought to be assisted by various phytochemicals like mono,
di and polysaccharides, proteins, ketones, terpenoids, ster-
oids, sapogenins, amides, flavonoids, carboxylic acids and
aldehydes which lead to the reduction of the metal ions in
the reaction mixture. Recently, anthocyanin rich extracts
have been used as reducing and stabilizing agents for the
production of gold nanoparticles from red raspberry (Rubus
idaeus), strawberry (Fragaria ananassa), and blackberry
(Rubus fruticosus) and red cabbage (Brassica oleracea)
[261]. Among the biomacromolecules, proteins have been
exhaustively used for green synthesis of a range of multi-
functional nanostructures with excellent stability and bio-
compatibility due to their nanoscale dimensions and multiple
binding sites with inorganic ions [262-265]. Likewise, DNA
has also an important role in the synthesis of unique
nanostructures, a field termed as structural DNA nanotech-
nology [266]. The attachment DNA motifs with nanoparti-
cles gives rise to a wide variety of metallic nanostructures
that exhibit unique properties due to the synergistic activity
of both components. DNA directed nanoparticle synthesis
has been successfully achieved for a variety of metals and
metal oxides [267-269]. The chemical synthesis involves the
use of capping and stabilizing agents for size stabilization of
nanoparticles. It has been established that reducing agents
from the plant extracts such as steroids, sapogenins, carbo-
hydrates and flavonoids act as the capping and stabilizing
agents, which is both economical as well as advantageous
since there is no requirement for extraneous addition of toxic
chemicals. The mechanism of nanoparticle production using
angiosperms involves three major steps. The initial step,
known as the activation step, involves the reduction of metal
ions and nucleation of the reduced metal atoms. Thereafter
occurs the growth phase in which small nanoentities come
together spontaneously and merge into nanoparticles of
greater dimensions along with enhancement in their thermo-
dynamic stability. The last step, known as the termination
phase, determines the final shape of the mature nanoparticles
[270-272].
The recently introduced concept of nanoflowers needs
special mention. Nanoflowers are tiny entities of the dimen-
sions of 100-500 nm that show structural similarity to plant
flowers and have evoked interest among nanotechnologists
for diverse biomedical uses [273, 274]. Nanoflowers can be
considered as organic-inorganic hybrid nanostructures
formed using proteins/enzymes present in the plant extracts
as organic parts and metal ions as inorganic parts. Since
plant extracts offer numerous advantages in nanomaterials
synthesis due to their low cost, ease in availability, low con-
tamination risk, and no sophisticated instrumentation re-
quirement, they have also been utilized in the green synthesis
of nanoflowers [275, 276]. The nanoflowers display greater
stability and catalytic activities due to their shape and syner-
gistic effect between enzyme and metal ion [277]. The syn-
thesis of nanoflowers using diverse elements like copper,
calcium and magnesium have successfully carried out where
protein has been used as the organic form [278-279]. How-
ever, a number of non-protein incorporated hybrid
nanostructures have also been produced [275, 280-283]. The
nanoflowers have been successfully explored for their anti-
bacterial [275, 277, 284], antifungal [285, 286], anticancer
activity [287, 288] and as biosensors to determine the pres-
ence of biomolecules and pathogens [289-291].
Plant extracts offer several advantages over the use of
whole plants and other living forms. The process of making
use of plant extracts is simple, easily available, less expen-
sive, non-pathogenic and readily scalable [31]. For the pro-
duction of nanoparticles, this group is abundant, safe to han-
dle, equipped with a wide array of metabolites, eliminates
elaborate maintenance of cell cultures and is truly green
while undertaking any chemical protocol [71]. However, a
lot needs to be done with respect to the industrial application
of this technology. These include the heterogeneity in the
size and shape of nanoparticles, low production potential and
cost effective extraction and purification of nanoparticles
from the plant material.
6. APPLICATIONS OF BIOLOGICALLY SYNTHE-
SIZED NANOPARTICLES
There has been a recent uptrend in the demand of biolog-
ically synthesized nanoparticles in diverse areas ranging
from biomedical sciences to catalytic applications, separation
science and biosensors [292]. This is due to the fact that the
nanoparticles synthesized using green methods are much
more stable and safe as compared to those using classical
methods. The antibacterial activity of green nanoparticles is
increasingly being utilized for the development of new bac-
tericide agents. It is worthwhile to note that silver has been
the most investigated and explored metal for the biosynthesis
of nanoparticles. This is due to the fact that silver nanoparti-
cles have exclusive properties like good conductivity, chem-
ical stability and catalytic activity that can be successfully
utilized for industrial applications like in the preparation of
biosensors, composite fibers, superconducting materials,
cosmetics and electronics [293, 294]. Besides this, silver
nanoparticles exhibit anti-inflammatory, anti-cancerous, an-
tiplatelet and broad biocidal effect against a vast array of
pathogenic microorganisms that facilitates its use in diverse
areas of biomedical science [295-296]. Various metal and
metal oxide nanoparticles have been tested against a range of
pathogenic and non-pathogenic microbes like Shewanella,
Staphylococcus, Pseudomonas, Klebsiella, Escherichia and
Salmonella [129, 136, 297-300].
In a recent study [301] silver nanoparticles synthesized
using S. cerevisiae, B. subtilis and E. coli, and observed an-
tibacterial activity against five genera of both Gram negative
and Gram positive bacteria as compared to a positive control
(Ampicillin) and negative control (AgNO3). It has been

Using Living Forms for Metal Nanoparticle Synthesis Mini-Reviews in Medicinal Chemistry, 2020, Vol. 20, No. 2 255
Table 3. List of nanoparticles synthesized by angiosperms.
Scientific Name
Plant Family
Type of Nanoparticle
Size (nm)
Refs.
Annona reticulata
Annonaceae
Silver
6.48-8.13
[235]
Berberis aristata
Barberidaceae
ZnO
20-40
[236]
Caesalpinia pulcherrima
Fabaceae
Silver
12
[237]
Coleus aromaticus
Lamiaceae
Silver
44
[238]
Diospyros paniculata
Ebenaceae
Silver
17
[239]
Eleutherococcus senticosus
Araliaceae
Gold
200
[240]
Eucalyptus oleosa
Myrtaceae
Silver
21
[241]
Falcaria vulgaris
Apiaceae
Copper
20
[242]
Garcinia mangostana
Clusiaceae
Gold
32.96
[243]
Hyssops officinalis
Lamiaceae
ZnO
10-100
[244]
Impatiens balsamina
Balsaminaceae
Silver
12-20
[245]
Ipomoea batatas
Convolvulaceae
Silver
-
[246]
Lantana camara
Verbenaceae
Silver
3.2-12
[245]
Momordica cymbalaria
Cucurbitaceae
Silver
15.5
[247]
Moringa oleifera
Moringaceae
Silver
9-11
[248]
Ononidis radix
Fabaceae
Platinum
20
[249]
Origanum vulgare
Lamiaceae
Silver
2-25
[250]
Oryza sativa
Poaceae
Silver
10.6
[251]
Papaver somniferum
Papaveraceae
PbO
Fe2O3
23
38
[252]
[252]
Parkia speciosa
Fabaceae
Silver
114.41-160.67
[253]
Punica granatum
Punicaceae
Silver
20-40
[254]
Senna alata
Fabaceae
Silver
10-30
[255]
Silybum marianum
Asteraceae
ZnO
30.8-46
[256]
Solanum lycopersicum
Solanaceae
Silver
41.1
[251]
Syzygium aromaticum
Myrtaceae
ZnO
30-40
[257]
Terminalia belerica
Combretaceae
ZnO
9-11
[258]
observed that biologically synthesized nanoparticles exhibit
higher antimicrobial activity as compared to nanoparticles
synthesized through physical and chemical methods. Apart
from this biologically synthesized nanoparticles have also
been explored in diagnosis and treatment of diseases, drug
and gene delivery, biodetection of pathogens, tissue engi-
neering, regenerative medicine and cancer theranostics [302-
307]. Greater biocompatibility and efficacy of biologically
produced nanoparticles have been proved as compared to
physiochemical nanoparticles for biomedical applications.
Several studies have also discussed the mosquitocidal effica-
cy of plant derived nanoparticles at low concentrations (1-30
ppm) against mosquitoes spreading yellow fever, dengue and
malaria with less toxicity on aquatic organisms at the doses
lethal to mosquito young instars [308-310].
CONCLUSION
Since research on the use of biological systems for metal
nanoparticle synthesis has recently picked up, earnest efforts
are needed to explore their untapped potential. Synthesis of
such nanomaterials from extracts of natural sources has the
advantages of sustainability, eco-friendliness, cost-
effectiveness and having fewer chemical contaminants for
use in biomedical applications. Apart from being produced
easily on a large scale, non-toxic waste products can be easi-
ly disposed of. The biologically synthesized nanoparticles

256 Mini-Reviews in Medicinal Chemistry, 2021, Vol. 21, No. 2 Srivastava et al.
are also more stable and effective as compared with those
produced by physical and chemical methods. However, a lot
needs to be researched with respect to understanding the
biochemical and molecular mechanisms of nanoparticle syn-
thesis by living forms.
CONFLICT OF INTEREST
The authors declare no conflict of interest, financial or
otherwise.
FUNDING
Declared None.
CONSENT FOR PUBLICATION
The authors declare no Consent for Publication.
ACKNOWLEDGEMENTS
Declared None.
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