Synthesis of Silver Nanoparticles Mediated by Fungi: A Review

REVIEW
published: 22 October 2019

doi: 10.3389/fbioe.2019.00287
Synthesis of Silver Nanoparticles

Mediated by Fungi: A Review
Mariana Guilger-Casagrande and Renata de Lima*
Laboratory for Evaluation of the Bioactivity and Toxicology of Nanomaterials, University of Sorocaba, Sorocaba, Brazil
The use of fungi as reducing and stabilizing agents in the biogenic synthesis of silver
nanoparticles is attractive due to the production of large quantities of proteins, high
yields, easy handling, and low toxicity of the residues. Furthermore, this synthesis
process coats the nanoparticles with biomolecules derived from the fungus, which
can improve stability and may confer biological activity. The aim of this review is to
describe studies in which silver nanoparticles were synthesized using fungi as reducing
agents, discussing the mechanisms and optimization of the synthesis, as well as the
applications. The literature shows that various species of fungus have potential for use in
biogenic synthesis, enabling the production of nanoparticles with different characteristics,
considering aspects such as their size, surface charge, and morphology. The synthesis
mechanisms have not yet been fully elucidated, although it is believed that fungal
Edited by:
Jinmyoung Joo,
biomolecules are mainly responsible for the process. The synthesis can be optimized by
Ulsan National Institute of Science and adjusting parameters such as temperature, pH, silver precursor concentration, biomass
Technology, South Korea amount, and fungus cultivation time. Silver nanoparticles synthesized using fungi enable
Reviewed by: the control of pathogens, with low toxicity and good biocompatibility. These findings
Pradipta Ranjan Rauta,
University of Texas MD Anderson open perspectives for future investigations concerning the use of these nanoparticles as
Cancer Center, United States antimicrobials in the areas of health and agriculture.
Palanivel Velmurugan,
Sri Sankara Arts and Science Keywords: biogenic synthesis, silver nanoparticles, fungi, biological activity, biomolecules
College, India
*Correspondence:
Renata de Lima INTRODUCTION
renata.lima@prof.uniso.br
Among the different types of metallic nanoparticles, silver nanoparticles can be highlighted for
Specialty section: their broad-spectrum antimicrobial potential (Prabhu and Poulose, 2012; Rai et al., 2014; Gupta
This article was submitted to et al., 2017; Loo et al., 2018). These nanoparticles adhere to the cell walls and membranes of
Nanobiotechnology, microorganisms and may reach the cell interior. They damage the cellular structures, induce the
a section of the journal production of reactive oxygen species, and alter the mechanisms of signal transduction (Kim et al.,
Frontiers in Bioengineering and
2011; Dakal et al., 2016). Several studies report applications in which good results have been
Biotechnology
obtained using silver nanoparticles for the control of pathogenic microorganisms in the areas of
Received: 19 July 2019 health and agriculture (Kim et al., 2012; Mishra and Singh, 2015; Burduşel et al., 2018).
Accepted: 07 October 2019
The commonest method used to produce silver nanoparticles is chemical synthesis, employing
Published: 22 October 2019
reagents whose function is to reduce the silver ions and stabilize the nanoparticles. These reagents
Citation: are toxic and can present risks to health and the environment (Ahmed et al., 2016; Zhang et al.,
Guilger-Casagrande M and Lima R
2016), which has led to increasing interest in biogenic synthesis methods. Such processes enable
(2019) Synthesis of Silver
Nanoparticles Mediated by Fungi: A
nanoparticles to be obtained that present lower toxicity, better physicochemical characteristics, and
Review. higher stability (Iravani et al., 2014).
Front. Bioeng. Biotechnol. 7:287. Biogenic synthesis of nanoparticles can be performed using organisms such as bacteria, fungi,
doi: 10.3389/fbioe.2019.00287 and plants, or the byproducts of their metabolism, which act as reducing and stabilizing agents
Frontiers in Bioengineering and Biotechnology | www.frontiersin.org 1 October 2019 | Volume 7 | Article 287
Guilger-Casagrande and Lima Fungal Silver Nanoparticles
(Durán et al., 2011). These nanoparticles are capped with using plants, the mycelial mass of fungi is more resistant to
biomolecules derived from the organism used in the synthesis, agitation and pressure, so it is more suitable for large-scale
which can improve stability and may present biological syntheses (Velusamy et al., 2016). Furthermore, by adjusting
activity (Ballotin et al., 2016). Biogenic synthesis is relatively culture conditions such as time, temperature, pH, and quantity
simple, clean, sustainable, and economical, and provides greater of biomass, among others, it is possible to manipulate the
biocompatibility in the uses of nanoparticles (Gholami-Shabani metabolism of fungi so as to obtain nanoparticles with the desired
et al., 2014). characteristics, such as specific size and morphology (Zielonka
The synthesis of silver nanoparticles using bacteria involves and Klimek-Ochab, 2017).
cultivating the organisms in a suitable medium, followed by
contact of the bacteria or their metabolites with a silver nitrate Biogenic Synthesis of Silver Nanoparticles
(AgNO3) solution (Singh et al., 2015). When the synthesis is
Mediated by Fungi
performed using plants, aqueous extracts are prepared from the
Fungi have excellent potential for the production of many
leaves, stems, or roots, followed by the addition of silver nitrate
compounds that can be used in different applications. Around
solution (Rheder et al., 2018). The use of fungi to synthesize silver
6,400 bioactive substances are known to be produced by
nanoparticles involves culturing the fungus on agar, followed
microscopic filamentous fungi (ascomycetes and imperfect
by transfer to a liquid medium. The biomass produced is
fungi) and other fungal species (Bérdy, 2005). These organisms
subsequently transferred to water for release of the compounds
are widely used as reducing and stabilizing agents, due
that act in the synthesis. After filtration, the biomass is discarded
to their heavy metal tolerance and capacity to internalize
and silver nitrate is added to the filtrate (Costa Silva et al., 2017;
and bioaccumulate metals. Furthermore, fungi can be easily
Guilger et al., 2017; Mekkawy et al., 2017; Ottoni et al., 2017).
cultivated on a large scale (“nanofactories”) and can produce
The purpose of this review is to provide an overview of
nanoparticles with controlled size and morphology (Gade et al.,
the main published studies concerning the use of fungi for
2008; Ahluwalia et al., 2014; Azmath et al., 2016; Khan et al.,
the biogenic synthesis of silver nanoparticles, as well as the
2017). Fungi have advantages over other microorganisms, in that
applications of these materials in different areas. The synthesis
they produce large quantities of proteins and enzymes, some
mechanisms are discussed, together with methods to optimize the
of which can be used for the fast and sustainable synthesis of
processes and the importance of cappings on the nanoparticles.
nanoparticles (Vahabi et al., 2011; Alghuthaymi et al., 2015).
Given the problems caused by pathogenic microorganisms,
The mechanism of biogenic synthesis of nanoparticles using
there is a continuing search for more effective techniques for their
fungi may be intracellular or extracellular. In the case of
control. The emergence of nanotechnology has led to increasing
intracellular synthesis, the metal precursor is added to the
interest in the antimicrobial properties of silver nanoparticles and
mycelial culture and is internalized in the biomass. Consequently,
in exploring environmentally friendly ways in which they can be
extraction of the nanoparticles is required after the synthesis,
used most effectively.
employing chemical treatment, centrifugation, and filtration
to disrupt the biomass and release the nanoparticles (Castro-
Longoria et al., 2011; Rajput et al., 2016; Molnár et al., 2018).
BIOGENIC SYNTHESIS OF SILVER In extracellular synthesis, the metal precursor is added to
NANOPARTICLES the aqueous filtrate containing only the fungal biomolecules,
resulting in the formation of free nanoparticles in the dispersion.
Most of the conventional methods used to produce nanoparticles
This last method is most widely used, since no procedures are
have disadvantages such as the use of toxic chemicals and the
required to release the nanoparticles from the cells (Azmath et al.,
generation of waste, which can cause environmental pollution
2016; Sabri et al., 2016; Costa Silva et al., 2017; Gudikandula et al.,
(Iravani et al., 2014; Ahmed et al., 2016). Consequently, in recent
2017). Nonetheless, the nanoparticle dispersion must be purified
years there has been increasing interest in eco-friendly synthesis
in order to eliminate fungal residues and impurities, which can
methods. The methods involve the use of organisms including
be achieved using methods such as simple filtration, membrane
bacteria, fungi, and plants, which can reduce metal salts and
filtration, gel filtration, dialysis, and ultracentrifugation (Ashrafi
enable the formation of nanoparticles that present the desired
et al., 2013; Qidwai et al., 2018; Yahyaei and Pourali, 2019).
size and morphology (Azmath et al., 2016). The production
of nanoparticles by biological reduction of metals is an option
that can be considered clean, non-toxic, and environmentally SYNTHESIS MECHANISMS
acceptable (Banu and Balasubramanian, 2014b).
Fungi are attractive agents for biogenic synthesis of silver How Does Extracellular Synthesis of Silver
nanoparticles, because they offer high tolerance to metals and are Nanoparticles by Fungi Occur?
easy to handle. They also secrete large quantities of extracellular Although many studies have been published concerning the
proteins that contribute to the stability of the nanoparticles biogenic synthesis of silver nanoparticles using fungi, the specific
(Balaji et al., 2009; Du et al., 2015; Netala et al., 2016). Advantages mechanisms involved have not yet been fully elucidated. It
of fungal cultures over bacterial systems are that they provide is known that extracellular synthesis of nanoparticles occurs
good biomass production and do not require additional steps according to reactions in which the enzymes present in the
to extract the filtrate (Gade et al., 2008). Compared to synthesis fungal filtrate act to reduce silver ions, producing elemental silver
(Ag0 ) at a nanometric scale. After the reaction, the color of precursor, pH, culture medium, and amount of biomass can
the filtrate changes and UV-visible spectroscopy can be used to be used to obtain nanoparticles with different physicochemical
observe surface plasmon resonance bands reflecting alteration of characteristics (Birla et al., 2013; Rajput et al., 2016; Saxena et al.,
the optical properties of the material (Ahmad et al., 2003). The 2016; Liang et al., 2017). Table 1 shows some studies in which
absorbance wavelengths of these bands vary in the range from silver nanoparticles were produced using different fungal species
400 to 450 nm, with an absorbance peak at a longer wavelength and synthesis conditions.
indicating the presence of larger nanoparticles (Elamawi et al.,
2018). The size depends on the synthesis conditions such as Effect of Temperature
fungus species, temperature, pH, and dispersion medium, as well The temperature used in the synthesis of silver nanoparticles
as the presence of cappings on the nanoparticles (Khandel and employing fungi can affect parameters such as the speed of the
Shahi, 2018; Lee and Jun, 2019). The color of the dispersion is synthesis and the size and stability of the nanoparticles (Elamawi
also directly related to the surface plasmon resonance, which et al., 2018).
varies according to the size and absorbance of the nanoparticles In synthesis performed using the filtrate of Trichoderma
(Adeeyo and Odiyo, 2018; Bhangale et al., 2019; Lee and Jun, harzianum, Ahluwalia et al. (2014) observed that the synthesis
2019). rate increased as the temperature was increased up to 40◦ C,
Many biomolecules can react with silver ions and act which was considered the ideal temperature. In other work using
in the synthesis, such as those associated with the complex the filtrate of Fusarium oxysporum, higher protein secretion
pathways involving electron transfer during the conversion by the fungal biomass was observed at temperatures between
of NADPH/NADH to NADP+ /NAD+ (Thakkar et al., 2010; 60 and 80◦ C, with progressive increases of the synthesis rate
Gudikandula et al., 2017). Nicotinamide adenine dinucleotide and surface plasmon absorbance as the temperature increased
(NADH) and NADH-dependent nitrate reductase enzymes are (Birla et al., 2013). In synthesis using the endophytic fungus
considered to be most important in the biogenic synthesis of Colleotrichum sp. ALF2-6, Azmath et al. (2016) found that the
metallic nanoparticles (Zomorodian et al., 2016; Baymiller et al., reaction rate increased at higher temperatures, with the synthesis
2017; Figure 1). being completed within 20 min at temperatures above 50◦ C.
In recent work, Hietzschold et al. (2019) showed that In the work by Phanjom and Ahmed (2017), using Aspergillus
nanoparticle synthesis occurred by the action of NADPH, oryzae (MTCC no. 1846), a higher temperature also increased
without any need for the nitrate reductase enzyme. This is the rate of synthesis, with temperatures of 30, 50, 70, and
particularly interesting, since it leads to the possibility of 90◦ C resulting in the synthesis being concluded in 6 h, 1 h,
using different organisms for the synthesis of nanoparticles, 45 min, and 20 min, respectively, while no synthesis occurred at
without the necessary condition of reductase enzyme production. 10◦ C. In the work of AbdelRahim et al. (2017), no synthesis of
However, Durán et al. (2005) synthesized silver nanoparticles silver nanoparticles was observed using the filtrate of Rhizopus
using Fusarium oxysporum and suggested that the reduction of stolonifer at 80 or 10◦ C, which was attributed to denaturation or
silver ions was due to the action of the nitrate reductase enzyme inactivation of enzymes and other molecules.
and anthraquinones. In another study, using purified nitrate Although most studies have reported faster rates of synthesis
reductase and phytochelatins from the same fungus, it was found at higher temperatures, it is important to take into account
that extracellular NADPH-dependent nitrate reductase enzymes the quality of nanoparticles. In addition to influencing the
and quinones were responsible for the formation of nanoparticles synthesis rate, the temperature can affect nanoparticle size and
(Kumar et al., 2007). stability. In the work of AbdelRahim et al. (2017), nanoparticles
were obtained with sizes of 2.86, 25.89, and 48.43 nm, at
temperatures of 40, 20, and 60◦ C, respectively, with the smallest
Optimization of Silver Nanoparticles size observed at the intermediate temperature. Shahzad et al.
Synthesis (2019) synthesized nanoparticles using the fungus Aspergillus
Although the synthesis of silver nanoparticles using fungi is fumigatus BTCB10, obtaining a size of 322.8 nm at 25◦ C and
simple and effective, the parameters employed in the procedure increasing size as the temperature was increased, reaching
must be optimized in order to achieve good monodispersity, 1073.45 nm at 55◦ C. The size increase was attributed to the
stability, and biocompatibility of the particles (Balakumaran aggregation of nanoparticles at higher temperature. Elsewhere,
et al., 2015). Given that a wide variety of fungi have Husseiny et al. (2015) used the fungus Fusarium oxysporum and
potential for use in the synthesis, it is important to consider found that the nanoparticle size decreased as the temperature
their individual characteristics and to optimize the synthesis was increased to 50◦ C, with the smallest size (30.24 nm) at
conditions accordingly (Ottoni et al., 2017). this temperature. In the work by Fayaz et al. (2009), using the
Parameters such as agitation, temperature, light, and culture fungus Trichoderma viride, the nanoparticle size was also found
and synthesis times differ depending on the fungus used and to decrease as the synthesis temperature increased.
can also be adjusted in order to obtain the desired nanoparticle These different results indicate that the effect of temperature
characteristics. Control of nanoparticle size and shape requires on the size and stability of the nanoparticles synthesized varies
adjustment of the parameters used for both cultivation of the according to the fungus species used. Banu and Balasubramanian
fungus and the synthesis process (Birla et al., 2013). Studies have (2014a) reported that 30◦ C was the optimum temperature for
found that changes in temperature, concentration of the metal production of high stability silver nanoparticles using Isaria
FIGURE 1 | Mechanisms of biogenic synthesis of silver nanoparticles.
fumosorosea. Balakumaran et al. (2015) also found that this was altered according to the concentration of protons in the reaction
the optimum temperature for synthesis of nanoparticles using medium, leading to alteration of the morphology and size of the
the fungus Guignardia mangifera. In the work of Costa Silva nanoparticles. At higher pH, there is greater competition between
et al. (2017), using Duddingtonia flagans, the optimum synthesis protons and metal ions for establishing bonds with negatively
temperature was 60 ◦ C. These differences in the effect of the charged regions, resulting in greater success of synthesis at
synthesis temperature occur even within the same fungal genus. alkaline pH (Sintubin et al., 2009).
Trichoderma longibrachiatum presented a specific synthesis Qian et al. (2013) observed that alkaline pH favored the
temperature of 28◦ C, with no production of nanoparticles at synthesis of silver nanoparticles when AgNO3 was added to the
23 or 33◦ C (Elamawi et al., 2018), while Trichoderma viride filtrate of the fungus Epicoccum nigrum. Du et al. (2015) found
presented viable synthesis at temperatures of 10, 27, and 40◦ C that a more alkaline pH resulted in a shorter synthesis time and
(Fayaz et al., 2009). smaller nanoparticle size distribution and polydispersity index
The occurrence of synthesis of nanoparticles by some fungal values. These characteristics indicate improved stability, due to
species at high temperatures indicates that electrons can be the electrostatic repulsion of anions present in the dispersion
transferred from free amino acids to silver ions. However, (Gurunathan et al., 2009). Synthesis employing Colleotrichum
very high temperatures, between 80 and 100◦ C, lead to sp. ALF2-6 at alkaline pH and a higher temperature of 50◦ C
denaturation of the proteins that compose the nanoparticle was faster than at lower pH and was completed in around
capping. This denaturation alters the nucleation of Ag+ ions, 20 min (Azmath et al., 2016). In the synthesis performed
with the nanoparticles aggregating and increasing in size (Birla by Birla et al. (2013), using Fusarium oxysporum, maximum
et al., 2013). According to Husseiny et al. (2015), unsuitable nanoparticle production occurred between pH 9 and 11, with
temperatures lead to increased nanoparticle size and loss of lower production at pH 7 and formation of aggregates between
stability, due to the low activity of the enzymes involved in pH 3 and 5. However, Husseiny et al. (2015), using the same
the synthesis. fungus, found that the nanoparticle synthesis rate decreased
as the pH was increased, which was suggested to be due to
Effect of pH lower activity of the reductases responsible for the synthesis at
Adjustment of the synthesis pH can be used to control certain higher pH.
characteristics of the nanoparticles. Nayak et al. (2011) reported Some studies have reported successful syntheses at neutral
that the conformation of nitrate reductase enzymes could be or slightly alkaline pH. Nanoparticles synthesized using
TABLE 1 | Optimization of the synthesis of silver nanoparticles by fungi.
Fungus Type of parameter Optimized conditions Nanoparticle References

characteristics
Trichoderma harzianum Temperature and concentration of 40◦ C 51.10 nm Ahluwalia et al., 2014
AgNO3 1 mM AgNO3 −17.19 mV
Spherical
Fusarium oxysporum Culture media, quantity of MGYP 10–20 nm Birla et al., 2013
biomass, light intensity, pH, 6 g of biomass 30 mV
temperature, and concentration of 190.7 Lux and sun light Spherical
AgNO3 pH 9 and 11
40 and 60◦ C
1.5 mM AgNO3
Colleotrichum sp. ALF2-6 Temperature and pH 50–80◦ C 5–60 nm Azmath et al., 2016
Alkaline pH Myriad shapes
Aspergillus oryzae (MTCC no. Temperature, pH and 90◦ C 7–27 nm Phanjom and Ahmed, 2017
1846) concentration of AgNO3 pH 10 Spherical
1 mM AgNO3
Rhizopus stolonifer Temperature and concentration of 40◦ C 2.86 nm AbdelRahim et al., 2017
AgNO3 10 mM AgNO3 Spherical
Aspergillus fumigatus BTCB10 Temperature, fungal culture age, 25◦ C 322.8 nm Shahzad et al., 2019
quantity of biomass, pH, 7 days of culture PDI 0.278
concentration of AgNO3 , ratio of 7 g of biomass Spherical
cell-free filtrate/silver nitrate pH 6
1 mM AgNO3
Cell-free filtrate/silver nitrate 3:2
Fusarium oxysporum Temperature, quantity of biomass, 50◦ C 5–13 nm Husseiny et al., 2015
pH and concentration of AgNO3, 11 g of biomass Spherical
pH 6
10 mM AgNO3
Trichoderma viride Temperature 27◦ C 2–4 nm Fayaz et al., 2009
Spherical
Isaria fumosorosea Temperature, pH and agitation 30◦ C 51.31–111.02 nm Banu and Balasubramanian,
pH 8.5 Spherical 2014a
150 rpm
Guignardia mangifera Temperature, quantity of biomass, 30◦ C 5–30 nm Balakumaran et al., 2015
pH and concentration of AgNO3 10 g of biomass Spherical
pH 7
1 mM AgNO3
Duddingtonia flagans Temperature and pH 60◦ C 30-409 nm Costa Silva et al., 2017
pH 10 −28,655 mV
Spherical
Trichoderma longibrachiatum Temperature, quantity of biomass 28◦ C 24.43 nm Elamawi et al., 2018
and agitation 10 g of biomass PDI 0.420
Without agitation −19,7 mV
Spherical
Penicillium pH and concentration of AgNO3 pH 8 8–10 nm Nayak et al., 2011
purpurogenum 1 mM AgNO3 Spherical
Epicoccum nigrum Temperature, pH and 55◦ C 1–22 nm Qian et al., 2013
concentration of AgNO3 Alkaline pH Spherical or near
1 mM AgNO3 to spherical
Penicillium oxalicum pH pH 12 36.53 nm Du et al., 2015
0.273
−25.9 mV
Arthroderma fulvum Temperature, pH, concentration 55◦ C 20.56 nm Xue et al., 2016
of AgNO3 and time of reaction pH 10 PDI 0.27
1.5 mM AgNO3 Spherical
12 h
Sclerotinia sclerotiorum Culture media, quantity of Potato dextrose broth 10–15 nm Saxena et al., 2016
MTCC 8785 biomass, concentration of 10 gm of biomass Spherical
AgNO3, pH and temperature 2 mM AgNO3
pH 11
80◦ C
(Continued)
TABLE 1 | Continued
Fungus Type of parameter Optimized conditions Nanoparticle References

characteristics
Fusarium oxysporum Concentration of AgNO3 and 5 mM AgNO3 25–50 nm Korbekandi et al., 2013
quantity of biomass 4.96 g/L of biomass Almost spherical
Fusarium oxysporum Temperature culture media 28◦ C 24 nm Hamedi et al., 2017
Modified medium for PDI 0.23
nitrate reductase Spherical
Rhizoctonia solani Culture media Potato glucose broth 2–22 nm Ashrafi et al., 2013
Spherical
Penicillium oxalicum GRS-1 Temperature, quantity of 60◦ C 10–40 nm Rose et al., 2019
biomassa, concentration of 25 g of biomass Spherical
AgNO3 and pH 1.5 mM AgNO3
pH 7
Isaria fumosorosea at pH 8.5 showed better physicochemical These findings suggest that there is a limit to the concentration
characteristics, compared to nanoparticles synthesized at pH 4.5 of AgNO3 used, in order to obtain nanoparticles with satisfactory
and 6.5 (Banu and Balasubramanian, 2014a). In synthesis using physicochemical characteristics. The addition of excess amounts
Guignardia mangiferae, no color change was observed between of metal ions results in very large nanoparticles with irregular
pH 1 and 4, while coloration started to appear at pH 5 and 6. As morphology (AbdelRahim et al., 2017), due to competition
the pH was increased, the intensity of the dispersion increased, between the silver ions and functional groups from the fungus
with the nanoparticles presenting greater monodispersion and filtrate (Shahzad et al., 2019). As the concentration of the metal
stability at pH 7 (Balakumaran et al., 2015). precursor increases, so also does the intensity of color of the
dispersion (Ahluwalia et al., 2014; Phanjom and Ahmed, 2017).
In addition, a higher concentration of AgNO3 may lead to greater
Effect of AgNO3 Concentration toxicity (Balakumaran et al., 2015).
In most of the studies employing fungi for extracellular synthesis
of silver nanoparticles, AgNO3 was used at a concentration of Effect of the Culture Medium
1 mM (Saxena et al., 2016; Xue et al., 2016). In some cases, It is known that microorganisms present different responses,
a lower metal precursor concentration resulted in a smaller depending on the culture medium and the cultivation conditions.
nanoparticle size and an improved dispersion (Kaviya et al., 2011; Changes in these conditions result in the synthesis of different
Phanjom and Ahmed, 2017). However, other studies obtained metabolites and proteins (Costa Silva et al., 2017).
smaller sizes when intermediate AgNO3 concentrations were In nanoparticle synthesis using fungi, a culture medium
used. AbdelRahim et al. (2017), employing the fungus Rhizopus containing substrate specific for the enzymes that act in the
stolonifer, obtained the smallest nanoparticle size (2.86 nm) at synthesis can induce their production and release by the
10 mM AgNO3 , while sizes of 54.67 and 14.23 nm were obtained fungus, enhancing the reduction of silver and the formation of
at 100 and 1 mM, respectively. Similar results were reported by nanoparticles (Husseiny et al., 2015). In the work by Hamedi et al.
Husseiny et al. (2015), using Fusarium oxysporum. (2017), Fusarium oxysporum was cultivated in a culture medium
Phanjom and Ahmed (2017) studied the synthesis of modified to induce nitrate reductase enzyme activity (0.35% yeast
nanoparticles using Aspergillus oryzae and different AgNO3 extract, 1% peptone, 0.35% potassium nitrate, and 1.5% glucose),
concentrations between 1 and 10 mM. It was observed that at as well as in malt glucose yeast peptone (MGYP) medium
AgNO3 concentrations up to 8 mM, the nanoparticles presented without enzyme induction (0.3% malt extract, 1% glucose, 0.3%
sizes between 7.22 and 17.06 nm, while the size increased to yeast extract, and 0.5% peptone). The nanoparticle dispersions
45.93 and 62.12 nm at AgNO3 concentrations of 9 and 10 mM, produced using the filtrate from the fungus cultivated in the
respectively. This effect was attributed to the lack of functional enzyme induction medium presented higher concentrations and
groups available for the reaction when the metal precursor smaller sizes of the nanoparticles, which was attributed to
concentration was increased. stimulation of the enzymatic activity by the nitrogen source in the
In addition to the effect on nanoparticle size, the AgNO3 modified medium, hence increasing nanoparticle production.
concentration is related to the quantity of nanoparticles Different behaviors were observed in studies in which
produced. In a study employing Fusarium oxysporum, it was different media were tested for the cultivation of fungi. Saxena
found that the quantity of nanoparticles increased as the et al. (2016) synthesized silver nanoparticles using Sclerotinia
precursor concentration was increased between 0.1 and 1.5 mM, sclerotiorum cultivated in various broths, with the highest
while no differences were observed at higher concentrations nanoparticle production achieved using potato dextrose medium.
(Birla et al., 2013). Similar results were reported elsewhere for In work by Costa Silva et al. (2017), using the fungus
syntheses employing Penicillium purpurogenum (Nayak et al., Duddingyonia flagans for the synthesis of silver nanoparticles, the
2011) and Fusarium oxysporum (Korbekandi et al., 2013). biomass was transferred to pure water and to water containing
insect carapaces as a natural source of chitin (a substrate bacterial resistance to antibiotics and phytopathogens that affect
for fungal enzymes). The filtrate supplemented with chitin agricultural production.
contained around three times more protein and presented higher
nanoparticle production.
Birla et al. (2013) tested 10 different media for cultivation Importance of Capping and Stabilization of
of Fusarium oxysporum, obtaining higher production of silver the Nanoparticles
nanoparticles using the filtrate from the fungus cultivated in The synthesis of nanoparticles by non-biogenic methods requires
MGYP medium. Conversely, Ashrafi et al. (2013) found that the an additional step in which polymers and surfactants are used
same medium inhibited the production of silver nanoparticles to coat their surfaces. This process, known as functionalization,
using the filtrate from Rhizoctonia solani, while the synthesis was employs biomolecules that facilitate the anchoring of desired
successful when potato dextrose medium was used to cultivate substances on the nanoparticle surfaces (Mout et al., 2012). In
the fungus. It was suggested that the activity of the enzyme the case of biogenic synthesis, formation of the capping occurs
responsible for the reduction process could have been inhibited simultaneously with formation of the nanoparticles, employing
by a component of the medium. biomolecules derived from the organism used in the synthesis, so
no additional steps are required (Chowdhury et al., 2014).
Biomolecules derived from the reducing organism have high
Effect of the Quantity of Biomass capacities for binding to metals, with proteins and amino acid
The amount of biomass used can affect the synthesis and residues binding to the nanoparticle surfaces to form cappings
characteristics of silver nanoparticles. Some studies have that confer stability and prevent particle agglomeration and
reported higher nanoparticle production using lower biomass aggregation (Basavaraja et al., 2008; Gopinath et al., 2012). The
concentrations, while others have found higher synthesis rates binding of proteins at the surfaces, with consequent stabilization,
using higher concentrations (Birla et al., 2013; Korbekandi et al., may involve free amino groups or cysteine residues. Stabilization
2013; Balakumaran et al., 2015; Elamawi et al., 2018). can also be provided by mycelial cell wall enzymes present in
Balakumaran et al. (2015) used the filtrate obtained from the filtrate, whose negative carboxyl groups provide electrostatic
10, 20, and 30 g quantities of Guignardia mangiferae biomass attraction (Gole et al., 2001; Husseiny et al., 2015). According
in 100 mL of water, obtaining silver nanoparticles with to Gurunathan et al. (2009), the stability of silver nanoparticles
better physicochemical characteristics when the lowest biomass is also provided by nucleophilic OH− ions that are adsorbed
concentration was used. Shahzad et al. (2019) evaluated the use on the surfaces, preventing aggregation and contributing to the
of 1, 4, 7, and 10 g quantities of Aspergillus fumigatus BTCB10 synthesis of smaller nanoparticles by providing electrons for the
biomass, observing greater production, smaller size, and better reduction of silver ions.
dispersion of the nanoparticles when the synthesis was based In addition to conferring stability to the nanoparticles, the
on the use of 7 g of biomass. In the work of Rose et al. protein capping resulting from biogenic synthesis can act in
(2019), employing Penicillium oxalicum, greater nanoparticle the anchoring of drugs and genetic material for subsequent
production was obtained using a higher biomass concentration, transport into cells (Hu et al., 2011; Zhang et al., 2016). The
which was attributed to greater release of the nitrate reductase non-toxic organic composition of the capping means that it is
enzyme by the mycelium. Saxena et al. (2016) observed higher biocompatible, which can increase the rate of internalization and
silver nanoparticle production when the amount of Sclerotinia retention of nanoparticles (Rodrigues et al., 2013; Mohanta et al.,
sclerotiorum biomass was increased. Birla et al. (2013) reported 2018; Figure 2).
the existence of a relationship between the amount of biomass Despite their importance, there have been few studies of
and the release of biomolecules responsible for the synthesis. the cappings on biogenic nanoparticles. Gade et al. (2008)
Despite the differences in the amount of biomass used, detected sulfur atoms in samples of silver nanoparticles
depending on the fungus species employed, it can be concluded synthesized using Aspergillus niger, indicative of the presence
that successful synthesis of nanoparticles necessitates a suitable of proteins enveloping the nanoparticles. Chowdhury et al.
balance between the amount of organic material, derived from (2014) used scanning electron microscopy to detect the
the fungus, and the amount of metal precursor (Phanjom and presence of cappings on biogenic silver nanoparticles. The
Ahmed, 2017; Shahzad et al., 2019). nanoparticles were spherical, polydispersed, and were not in
In summary, it is clear that different synthesis conditions can direct contact, even within aggregates, indicating good stability.
result in different characteristics of the nanoparticles, as well as The SDS-Page protein electrophoresis technique was employed
success or failure of the synthesis. However, the effects of the to characterize the extracellular fungal proteins associated with
different parameters remain unclear, requiring further detailed the nanoparticles. Molecular weight bands between 50 and
studies for each organism used. It is also important to define 116 kDa were attributed to proteins responsible for synthesis
the desired physicochemical characteristics of the nanoparticles, and stabilization of the nanoparticles. Both the filtrate and
in order to establish the parameters used in the synthesis, such the capping removed from nanoparticles showed a band at 85
as temperature, pH, and time, among others. The optimization kDa, which corresponded to a protein that was suggested to be
of synthesis techniques should enable the achievement of fast responsible for the stability of the nanoparticles.
large-scale nanoparticle production. This opens avenues for Elgorban et al. (2016) synthesized biogenic silver
the use of these nanomaterials to solve problems such as nanoparticles and confirmed the presence of a capping
FIGURE 2 | Differences between capped and uncapped silver nanoparticles.
by microscopic analyses. The use of transmission electron based on fungi may be advantageous in terms of production, due
microscopy revealed a thin layer of organic material surrounding to the large quantities of metabolites produced. Another factor
the particles. Signals corresponding to oxygen and carbon were to consider is the capacity of fungi to produce antibiotics that
observed using scanning electron microscopy, indicating the could be contained in the capping and act in synergy with the
presence of organic compounds derived from the filtrate, which nanoparticle core.
were adsorbed on the nanoparticle surfaces. Many studies of biogenic synthesis of nanoparticles using
Devi and Joshi (2015) synthesized silver nanoparticles using fungi have shown results that are promising for the application
the endophytic fungi Aspergillus tamarii, Aspergillus niger, and of these systems in controlling pathogenic fungi and bacteria,
Penicillium ochrochloron. UV-Vis absorption analysis revealed combating cancer cells and viruses, and providing larvicidal and
peaks at 419, 430, and 430 nm, respectively. A peak at 280 nm insecticidal activities (Figure 3).
was attributed to the presence in the filtrate of amino acid
residues such as tryptophan and tyrosine, which were secreted
by the fungi. Health Applications
Given the importance of the cappings on biogenic Several studies have described the use of biogenic silver
nanoparticles, future studies are needed to investigate their nanoparticles for applications in the area of health, involving
compositions and biological activities. The use of synergy the control of bacteria and fungi. Bacterial growth is directly
between nanometric silver and biomolecule cappings active inhibited by the nanoparticles, which contact the cell wall and
against specific pathogens is likely to be a development in the cause progressive metabolic responses, with the production of
near future. reactive oxygen species (Gudikandula et al., 2017).
The size of nanoparticles is one of the factors determining
their antimicrobial potential, since smaller nanoparticles have
APPLICATIONS greater effects (Lu et al., 2013). Small nanoparticles can penetrate
the bacterial cell membrane and damage the respiratory chain,
Silver nanoparticles synthesized using fungi have various alter permeability, cause DNA and RNA damage, affect cell
potential applications in the areas of health, agriculture, and pest division, and lead to cell death (Morones et al., 2005; Rai
control. There are no reports concerning the better or worse et al., 2009). Nanoparticles also interact with the thiol groups of
activities of biogenic nanoparticles synthesized from different essential enzymes, releasing Ag+ ions that form complexes with
sources, such as fungi, bacteria, or plants. However, synthesis nucleotides, damaging the microorganism DNA and inhibiting
FIGURE 3 | Applications of silver nanoparticles synthesized using fungi.
the activity of DNases (Li et al., 2010; Baker and Satish, The lower effects of silver nanoparticles toward gram-positive
2012). bacteria may be because the peptidoglycans that compose the
Materials with antifungal potential (such as biogenic silver cell wall act as a barrier that prevents internalization of the
nanoparticles) that are obtained from sustainable sources can nanoparticles (Shrivastava et al., 2007). However, in some
be inexpensive and safe options for the treatment of systemic studies, the nanoparticles exhibited inhibitory effects against
and surface fungal infections, enabling the control of resistant this bacterial type. In evaluation of the antimicrobial activity
fungi (Ashajyothi et al., 2016). The large surface area of silver of silver nanoparticles synthesized using Aspergillus niger, Gade
nanoparticles and the release of ions can contribute to high et al. (2008) observed inhibitory effects against the bacteria
antimicrobial activity. The toxic ions bind to proteins containing E. coli and S. aureus that were equivalent to those of the
sulfur, affecting cell permeability and leading to alteration of the antibiotic gentamicin, with the gram-positive bacterium (S.
DNA replication process. The inactivation of some enzymes is aureus) showing higher sensitivity.
also caused by the binding of nanoparticles with thiol groups. Silver nanoparticles have also been used in combination
This inactivation leads to oxidative stress, which influences with antibiotics and antifungals, representing a possible solution
electron transport and protein oxidation (Reidy et al., 2013; Rai to the problem of resistance toward these drugs used in the
et al., 2014; Fátima et al., 2016). health area. Bhat et al. (2015) synthesized silver nanoparticles
Table 2 shows some studies in which silver nanoparticles using Candida albicans and evaluated their effects when used
synthesized from different fungal species were employed for alone or in combination with the antibiotic ciprofloxacin against
health issues. Staphylococcus aureus, Escherichia coli, Bacillus cereus, Vibrio
Ahluwalia et al. (2014) synthesized silver nanoparticles cholerae, and Proteus vulgaris. It was found that the activity
using Trichoderma harzianum, which were used to control of the antibiotic increased when it was used together with
the bacteria Staphylococcus aureus and Klebsiella pneumoniae the nanoparticles, while the latter also showed antimicrobial
in vitro. The inhibition rates were concentration-dependent, potential when they were used alone.
with the gram-negative bacterium (K. pneumoniae) showing Fátima et al. (2016) evaluated the antimicrobial and
higher sensitivity. Balakumaran et al. (2015) reported antifungal activities of silver nanoparticles synthesized using the
the potential of silver nanoparticles synthesized using filtrate from Aspergillus flavus. The nanoparticles were effective
the fungus Guignardia mangiferae for the control of in controlling the bacteria Bacillus cereus, Bacillus subtilis,
gram-negative bacteria, with effects including increased Enterobacter aerogenes, Escherichia coli, and Staphylococcus
permeability, alteration of membrane transport, and release of aureus, with B. subtilis and E. coli being most sensitive.
nucleic acids. The activity was concentration-dependent, with better results
TABLE 2 | Health applications of silver nanoparticles synthesized by fungi.
Synthesis source Bioactivity Target organism Effective concentration References
Macrophomina phaseolina Antibacterial Multidrug resistant strains of Escherichia coli 0.51; 0.36; 0.25; 0.10; and 0.05 µg/mL Chowdhury et al., 2014
(concentration-dependent)
Aspergillus tubingiensis and Antibacterial Candida sp. and Pseudomonas aeruginosa 0.11–1.75 µg/mL (Candida sp.) and Rodrigues et al., 2013
Bionectria ochroleuca 0.28 µg/mL (P. aeruginosa)
Rhizopus arrhizus IPT1011; Antibacterial E. coli, Staphylococcus aureus, and P. aeruginosa 1.0; 5.0; 10; 50; and 100 µg/mL Ottoni et al., 2017
Rhizopus arrhizus IPT1013;
Trichoderma gamsii IPT853;
Aspergillus niger IPT856
Fusarium verticillioides Antibacterial S. aureus and E. coli 5 and 10 mM Mekkawy et al., 2017
Alternaria sp. Antibacterial Bacillus subtilis, S. aureus, E. Coli, and Serratia 5, 10, 15, 20, and 25 mg/mL Singh et al., 2017
marcescens (concentration-dependent)
Penicillium aculeatum Su1 Antibacterial E. coli, P. aeruginosa, S. aureus, B. Subtilis, and 50, 100, and 200 µg/mL Liang et al., 2017
Candida albicans (concentration-dependent)
Pleurotus cornucopiae var. Antifungal Candida spp. 20, 40, and 60 mg/well Owaid et al., 2015
citrinopileatus
Inonotus obliquus Antibacterial E. coli KCTC 2441 30 µL/disk Nagajyothi et al., 2014
and A549 (lung cancer) and MCF-7 (breast cancer)
antiproliferative
in cancer cells
Pleurotus djamor var. roseus Antiproliferative PC3 cells (prostate cancer) 10–40 µg/mL Raman et al., 2015
in cancer cells
Sclerotinia sclerotiorum Antibacterial E. coli and S. aureus 100, 200, and 400 ppm Saxena et al., 2016
MTCC8785
Colletotrichum sp. ALF2-6 Antibacterial E. coli, Salmonella typhi, B. Subtilis, and S. aureus 50 µg/mL (S. aureus) and 100 µg/mL Azmath et al., 2016
(others)
Penicillium chrysogenum and Antifungal Trichophyton rubrum P. chrysogenum 0.5 µg/mL and A. oryzae Pereira et al., 2014
Aspergillus oryzae >7.5 µg/mL
Schizophyllum radiatum Antibacterial B. subtilis and Salmonella paratyphi 60 µL/well Metuku et al., 2014
Trichophyton rubrum, T. Antifungal C. albicans 4 µg/mL Moazeni et al., 2012
mentagrophytes and
Microsporum canis
Aspergillus flavus Synergism Bacillus spp., Micrococus luteus, S. aureus, 100 ppm Naqvi et al., 2013
with Enterococcus faecalis, E. coli, P. aeruginosa,
conventional Acinetobacter baumanii, and Krebsiella
antibiotics pneumoniae
against
multidrug-
resistant
bacteria
Penicillium italicum Antibacterial Multidrug-resistant S. aureus, Shewanella 25 µL/disk Nayak et al., 2018
and antifungal putrefaciens, and C. albicans
Arthroderma fulvum Antifungal Candida sp. and Aspergillus sp. 0.125–4.00 µg/mL Xue et al., 2016
Aspergillus versicolor Antibacterial S. aureus, Streptococcus pneumonia, P. 1 mg/mL Netala et al., 2016
Aeruginosa, and K. pneumoniae
Aspergillus terreus Antibacterial Salmonella typhi, S. Aureus, and E. coli 11.43 µg/mL Rani et al., 2017
−308 µg/mL
Fusarium oxysporum Antifungal Candida spp. and Cryptococcus spp. Candida spp. 0.84–1.68 µg/mL and Ishida et al., 2014
Cryptococcus spp. 0.42–0.84 µg/mL
achieved using the nanoparticles in combination with the luteus, Bacillus cereus, Bacillus megaterium, Escherichia coli,
antibiotic tetracycline, rather than on their own. Concentration- Enterobacter aerogens, Klebsiella pneumoniae, Salmonella
dependent activity of the nanoparticles was also observed against typhimurium, Proteus vulgaris, Pseudomonas aeruginosa, and
the fungi Aspergillus niger and Trichoderma harzianum. Salmonella paratyphi). Both types of nanoparticle were effective
Gudikandula et al. (2017) used silver nanoparticles in controlling all the bacteria.
synthesized from the fungi Trametes ljubarsky and Ganoderma Ibrahim and Hassan (2016) synthesized silver nanoparticles
enigmaticum for the control of gram-positive and gram-negative using Alternaria alternata, which were capped with butyl
bacteria (Bacillus subtilis, Staphylococcus aureus, Micrococcus acrylate and applied on cotton to inhibit the proliferation
of microorganisms. At all the concentrations tested, the Agriculture and Pest Control Applications
nanoparticle-treated cotton presented high antimicrobial activity There have been few studies to evaluate the potential of silver
against E. coli and S. aureus, achieving 99.9% inhibition. nanoparticles synthesized using biogenic methods for the control
Biogenic silver nanoparticles can also be effective against of phytopathogenic fungi in agriculture and pests. Table 3
resistant microorganisms. For example, Singh et al. (2014) used shows some studies in which silver nanoparticles synthesized
an optimized synthesis process employing Penicillium sp. to from different fungal species were employed in agriculture and
produce silver nanoparticles that showed potential for the control pests control.
of multidrug-resistant E. coli and S. aureus. Elgorban et al. (2016) synthesized silver nanoparticles using
In addition to their antimicrobial potential, biogenic silver the fungus Aspergillus versicolor and observed their effects against
nanoparticles can exert effects on tumor cells. Husseiny et al. Sclerotinia sclerotiorum and Botrytis cinerea in strawberry plants.
(2015) evaluated the antibacterial and antitumor potential of The nanoparticles showed concentration-dependent activity
silver nanoparticles synthesized using Fusarium oxysporum. The toward both pests, with the greatest effect against B. cinerea.
nanoparticles were effective in controlling E. coli and S. aureus, Qian et al. (2013) synthesized silver nanoparticles using the
as well as a tumor cell line. A low IC50 value (121.23 µg fungus Epicoccum nigrum and observed their activity against
cm3 ) for MCF-7 cells (human breast adenocarcinoma) was isolates of the pathogenic fungi C. albicans, Fusarium solani,
obtained following exposure of the cells to the nanoparticles, Sporothrix schenckii, Cryptococcus neoformans, Aspergillus flavus,
indicating high cytotoxicity and the potential for tumor control. and Aspergillus fumigatus. Balakumaran et al. (2015) synthesized
The effect was attributed to the involvement of the silver silver nanoparticles using the fungus Guignardia mangiferae
nanoparticles in disruption of the mitochondrial respiratory and reported their potential to control the phytopathogenic
chain, which led to the production of reactive oxygen species fungi Colletotrichum sp., Rhizoctonia solani, and Curvularia
and hindered the synthesis of adenosine triphosphate (ATP), lunata. In other work, silver nanoparticles synthesized using
consequently damaging the nucleic acids (Husseiny et al., the phytopathogenic fungus Fusarium solani isolated from
2015). wheat were shown to be effective for the treatment of wheat,
Balakumaran et al. (2015) evaluated the cytotoxic potential barley, and maize seeds contaminated by different species of
of silver nanoparticles, synthesized using the fungus Guignardia phytopathogenic fungi (Abd El-Aziz et al., 2015).
mangiferae, against HeLa (human cervical carcinoma) and MCF- Several studies have investigated the combination of biogenic
7 tumor cells, as well as normal Vero cells (African monkey nanoparticles and conventional biocides. Gajbhiye et al. (2009)
kidney). Higher cytotoxicity was observed against the tumor synthesized silver nanoparticles using the fungus Alternaria
cells, which showed signs of apoptosis, with condensed nuclei, alternata and evaluated their potential, in combination with the
membrane damage, and the presence of apoptotic bodies. antifungal compound fluconazole, against the phytopathogenic
El-Sonbaty (2013) evaluated silver nanoparticles synthesized fungi Phoma glomerata, Phoma herbarum, and Fusarium
using the fungus Agaricus bisporus for their antitumor potential semitectum, as well as the biological control agent Trichoderma
in vitro against MCF-7 tumor cells and in vivo against Ehrlich sp. and the human pathogenic fungus Candida albicans. The
carcinoma in mice. The nanoparticles presented concentration- combination of the nanoparticles and fluconazole was effective,
dependent activity in reducing the viability of the breast with C. albicans showing the highest sensitivity after exposure,
carcinoma cells. In the case of Ehrlich carcinoma, there was followed by Trichoderma sp. and P. glomerata. Potentiation
a decrease of blood vessels and an increase of apoptotic cells, of antifungal activity was not observed for F. semitectum
with these effects being intensified when the application of or P. herbarum. Gherbawy et al. (2013) synthesized silver
nanoparticles was combined with exposure to gamma radiation. nanoparticles using Trichoderma harzianum and applied them
The cytotoxic effects of silver nanoparticles occur due to the in combination with triclabendazole for controlling the parasite
interactions of the silver atoms with the groups of intracellular Fasciola sp., which affects sheep and cattle. The nanoparticles
proteins and with the nitrogenous bases and phosphate groups combined with triclabendazole inhibited egg hatching by 90.6%,
of DNA (Sriram et al., 2010). Although the application of while use of the drug alone caused 70.6% inhibition. It was
nanoparticles for the control of cancer is of considerable interest suggested that use of the nanoparticles together with the drug
and has shown promising results in several studies, this technique could be a way to overcome the resistance that the parasite has
still requires further investigation and the use of clinical trials developed toward the drug.
(Balakumaran et al., 2015). Other studies have investigated the use of biogenic
Biogenic silver nanoparticles have also shown effects against nanoparticles to control insect vectors. Sundaravadivelan
viruses. Gaikwad et al. (2013) synthesized silver nanoparticles and Padmanabhan (2014) synthesized silver nanoparticles
using the fungi Alternaria sp., Fusarium oxysporum, Curvularia using the filtrate from Trichoderma harzianum and observed
sp., Chaetomium indicum, and Phoma sp., which showed concentration-dependent mortality when they were tested
potential for reducing the replication of HSV-1, HSV-2, and against the larvae and pupae of the dengue vector mosquito Aedes
HPIV-3 in cell cultures. The nanoparticles produced using F. aegypti. In other work by Banu and Balasubramanian (2014a),
oxysporum, Curvularia sp., and C. indicum were the most silver nanoparticles synthesized using the entomopathogenic
effective and presented low cytotoxicity, while the other two types fungus Isaria fumosorosea were tested for control of the mosquito
were not used, due to their cytotoxicity. species Culex quinquefasciatus and Aedes aegypti, when applied
TABLE 3 | Applications of silver nanoparticles synthesized by fungi in agriculture and pests control.
Synthesis source Bioactivity Target organism Effective concentration References
Trichoderma harzianum Antifungal Sclerotinia sclerotiorum 0.15 × 1012 and 0.31 × Guilger et al., 2017
1012 NPs/mL
Beauveria bassiana Insecticide Lipaphis erysimi (Concentration-dependent) Kamil et al., 2017
Trichoderma harzianum Antifungal Helminthosporium sp., Alternaria alternata, 100 µg/mL El-Moslamy et al., 2017
SYA.F4 Phytophthora arenaria, and Botrytis sp.
Arthroderma fulvum Antifungal Fusarium sp. 0.125–4.00 µg/mL Xue et al., 2016
Aspergillus versicolor Antifungal S. sclerotiorum and Botrytis cinerea 150 ppm Elgorban et al., 2016
Epicoccum nigrum Antifungal Fusarium solani, Sporothrix schenckii, 0.125–1.00 µg/mL Qian et al., 2013
Cryptococcus neoformans, Aspergillus
flavus, and Aspergillus fumigatus
Guignardia mangiferae Antifungal Colletotrichum sp., Rhizoctonia solani, and 1 mg/mL Balakumaran et al., 2015
Curvularia lunata
Fusarium solani Antifungal Several fungal species isolated from wheat, 1, 2, and 4% Abd El-Aziz et al., 2015
barley and corn
Alternaria alternata Antifungal Phoma glomerata, Phoma herbarum, and 20 µL/disk Gajbhiye et al., 2009
combined Fusarium semitectum
with
Fluconazol
Trichoderma harzianum Antiparasitic Fasciola hepatica 50 µg/mL Gherbawy et al., 2013
combined
with
Triclabendazol
Trichoderma harzianum Insecticide Aedes aegypti 0.2–1.0% Sundaravadivelan and Padmanabhan, 2014
Isaria fumosorosea Insecticide Culex quinquefasciatus and Aedes aegypti 0.3–1.0 ppm Banu and Balasubramanian, 2014a
Beauveria bassiana Insecticide Aedes aegypti 0.06–1.0 ppm Banu and Balasubramanian, 2014b
between instars 1 and 4. Potential concentration-dependent However, in order to successfully use fungi for biogenic synthesis,
control was observed for both species, with the greatest there are a number of disadvantages that must be overcome.
effectiveness against Aedes aegypti, for which the mortality These include the need to know which fungus to use, its growth
of 1st instar larvae reached 100% within 24 h. The 4th instar parameters, the need for sterile conditions, and the time required
larvae of both species showed lower susceptibility to the for fungal growth and for the synthesis to be completed. There
nanoparticles. Based on these results, these nanoparticles were can also be difficulties associated with scale-up, including the
considered as potential larvicides for mosquito control. The need for further investigation concerning the mechanisms of
same authors synthesized silver nanoparticles using the mycelial formation of capping layers and the molecules present in them.
extract of the entomopathogenic fungus Beauveria bassiana Although progress is required on some issues, the
and obtained 100% mortality of the 1st and 2nd instar larvae studies published to date show that the use of fungi for
of Aedes aegypti within 21 h of exposure to the nanoparticles. biogenic synthesis of silver nanoparticles can lead to a wide
The authors concluded that use of the nanoparticles could be range of possible applications. These nanoparticles offer
an environmentally safe strategy for vector control, following considerable potential for exploitation in the control of
scale-up of production and field applications (Banu and pathogenic microorganisms.
Balasubramanian, 2014b).
AUTHOR CONTRIBUTIONS
CONCLUSION
MG-C and RL wrote the manuscript and prepared the figures. All
Recent studies show that the biogenic synthesis of silver authors read and approved the final manuscript.
nanoparticles using fungi offers several advantages and that these
materials have promising potential for a range of applications FUNDING
in the areas of health and agriculture. The nanoparticles
possess cappings derived from the fungi, which confer stability. This work was supported by the University of Sorocaba/UNISO
Depending on the fungus used, this capping may also exhibit and São Paulo Research Foundation (FAPESP) (Grant
biological activity, acting in synergy with the effect of the #2016/13692-6 and #2017/13328-5).
nanoparticle core. The ability to use different species of fungi
and to perform the synthesis under different conditions of ACKNOWLEDGMENTS
temperature, pH, quantity of biomass, and concentration of
the metal precursor, among others, enables the production of The authors are grateful to University of Sorocaba/UNISO for
nanoparticles that have different physicochemical characteristics. supporting the publication charges.
REFERENCES Bérdy, J. (2005). Bioactive microbial metabolites. J. Antibiot. 58, 1–26.

doi: 10.1038/ja.2005.1
Abd El-Aziz, A. R. M., Al-Othman, M. R., Mahmoud, M. A., and Metwaly, H. Bhangale, H. G., Bachhav, S. G., Nerkar, D. M., Sarode, K. M., and Patil,
A. (2015). Biosynthesis of silver nanoparticles using Fusarium solani and its D. R. (2019). Study on optical properties of green synthesized silver
impact on grain borne fungi. Dig. J. Nanomater Bios. 10, 655–662. nanoparticles for surface plasmon resonance. J. Nanosci. Tech. 5, 658–661.
AbdelRahim, K., Mahmoud, S. Y., Ali, A. M., Almaary, K. S., Mustafa, A. E. doi: 10.30799/jnst.230.19050203
Z. M.A., and Husseiny, S. M. (2017). Extracellular biosynthesis of silver Bhat, M. A., Nayak, B. K., and Nanda, A. (2015). Evaluation of bactericidal
nanoparticles using Rhizopus stolonifer. Saudi J. Biol. Sci. 24, 208–216. activity of biologically synthesized silver nanoparticles from Candida albicans
doi: 10.1016/j.sjbs.2016.02.025 in combination with Ciprofloxacin. Mater Today Proc. 2, 4395–4401.
Adeeyo, A. O., and Odiyo, J. O. (2018). Biogenic synthesis of silver nanoparticle doi: 10.1016/j.matpr.2015.10.036
from mushroom exopolysaccharides and its potentials in water purification. Birla, S. S., Gaikwad, S. C., Gade, A. K., and Rai, M. K. (2013). Rapid synthesis of
Open Chem. 5, 64–75. doi: 10.2174/1874842201805010064 silver nanoparticles from Fusarium oxysporum by optimizing physicocultural
Ahluwalia, V., Kumar, J., Sisodia, R., Shakil, N. A., and Walia, S. (2014). Green conditions. Sci World J. 2013:796018. doi: 10.1155/2013/796018
synthesis of silver nanoparticles by Trichoderma harzianum and their bio- Burduşel, A. C., Gherasim, O., Grumezescu, A. M., Mogoant,ã, L., Ficai, A., and
efficacy evaluation against Staphylococcus aureus and Klebsiella pneumonia. Andronescu, E. (2018). Biomedical applications of silver nanoparticles: an
Ind. Crops Prod. 55, 202–206. doi: 10.1016/j.indcrop.2014.01.026 up-to-date overview. Nanomaterials 8:E681. doi: 10.3390/nano8090681
Ahmad, A., Mukherjee, P., Senapati, S., Mandal, D., Kahn, M. I., Kumar, R., Castro-Longoria, E., Vilchis-Nestor, A. R., and Avalos-Borja, M. (2011).
et al. (2003). Extracellular biosynthesis of silver nanoparticles using the Biosynthesis of silver, gold and bimetallic nanoparticles using the
fungus Fusarium oxysporum. Colloids Surf. B Biointerfaces 28, 313–318. filamentous fungus Neurospora crassa. Colloids Surf. B Biointerfaces 83,
doi: 10.1016/S0927-7765(02)00174-1 42–48. doi: 10.1016/j.colsurfb.2010.10.035
Ahmed, S., Ahmad, M., Swami, B. L., and Ikram, S. (2016). A review Chowdhury, S., Basu, A., and Kundu, S. (2014). Green synthesis of protein capped
on plants extract mediated synthesis of silver nanoparticles for silver nanoparticles from phytopathogenic fungus Macrophomina paseolina.
antimicrobial applications: a green expertise. J Adv Res. 7, 17–28. Nanoscale Res. Lett. 9:365. doi: 10.1186/1556-276X-9-365
doi: 10.1016/j.jare.2015.02.007 Costa Silva, L. P., Oliveira, J. P., Keijok, W. J., Silva, A. R., Aguiar, A. R., Guimarães,
Alghuthaymi, M. A., Almoammar, H., Rai, M., Said-Galiev, E., and Abd- M. C. C., et al. (2017). Extracellular biosynthesis of silver nanoparticles using
Elsalam, K. A. (2015). Myconanoparticles: synthesis and their role in the cell-free filtrate of nematophagus fungus Duddingtonia flagans. Int. J.
phytopathogens management. Biotechnol. Biotechnol. Equip. 29, 221–236. Nanomed. 12, 6373–6381. doi: 10.2147/IJN.S137703
doi: 10.1080/13102818.2015.1008194 Dakal, T. C., Kumar, A., Majumdar, R. S., and Yadav, V. (2016). Mechanistic
Ashajyothi, C., Praburajeshwar, C., Harish, K. H., and Chandrakanth, K. R. basis of antimicrobial actions of silver nanoparticles. Front. Microbiol. 16:1831.
(2016). Investigation of antifungal and anti-mycelium activities using biogenic doi: 10.3389/fmicb.2016.01831
nanoparticles: an eco-friendly approach. Environ. Nanotechnol. Monit. Manage. Devi, L. S., and Joshi, S. R. (2015). Ultrastructures of silver nanoparticles
5, 81–87. doi: 10.1016/j.enmm.2016.04.002 biosynthesized using endophytic fungi. J. Microsc. Ultrastruct. 3, 29–37.
Ashrafi, S. J., Rastegar, M. F., Ashrafi, M., Yazdian, F., Pourrahim, R., and Suresh, doi: 10.1016/j.jmau.2014.10.004
A. K. (2013). Influence of external factors on the production and morphology Du, L., Xu, Q., Huang, M., Xian, L., and Feng, J.-X. (2015). Synthesis of small
of biogenic silver nanocrystallites. J. Nanosci. Nanotechnol. 13, 2295–2301. silver nanoparticles under light radiation by fungus Penicillium oxalicum and
doi: 10.1166/jnn.2013.6791 its application for the catalytic reduction of methylene blue. Mater. Chem. Phys.
Azmath, P., Baker, S., Rakshith, D., and Satish, S. (2016). Mycosynthesis of 160, 40–47. doi: 10.1016/j.matchemphys.2015.04.003
silver nanoparticles bearing antibacterial activity. Saudi Pharm. J. 24, 140–146. Durán, N., Marcato, P. D., Alves, O. L., De Souza, G. I. H., and Esposito, E. (2005).
doi: 10.1016/j.jsps.2015.01.008 Mechanistic aspects of biosynthesis of silver nanoparticles by several Fusarium
Baker, S., and Satish, S. (2012). Endophytes: toward a vision in synthesis of oxysporum strains. J Nanobiotechnol. 3:8. doi: 10.1186/1477-3155-3-8
nanoparticle for future therapeutic agents. Int. J. Bio Inorg. Hybd. Nanomat. Durán, N., Marcato, P. D., Durán, M., Yadav, A., Gade, A., and Rai, M.
1, 67–77. (2011). Mechanistic aspects in the biogenic synthesis of extracelular metal
Balaji, D. S., Basavaraja, S., Deshpande, R., Mahesh, D. B., Prabhakar, B. K., and nanoparticles by peptides, bacteria, fungi and plants. Appl. Microbiol.
Venkataraman, A. (2009). Extracellular biosynthesis of functionalized silver Biotechnol. 90, 1609–1624. doi: 10.1007/s00253-011-3249-8
nanoparticles by strains of Cladosporium cladosporioides fungus. Colloids Surf. Elamawi, R. M., Al-Harbi, R. E., and Hendi, A. A. (2018). Biosynthesis and
B Biointerfaces 68, 88–92. doi: 10.1016/j.colsurfb.2008.09.022 characterization of silver nanoparticles using Trichoderma longibrachiatum
Balakumaran, M. D., Ramachandran, R., and Kalaicheilvan, P. T. (2015). and their effect on phytopathogenic fungi. Egypt J Biol Pest Control 28:28.
Exploitation of endophytic fungus, Guignardia mangiferae for extracellular doi: 10.1186/s41938-018-0028-1
synthesis of silver nanoparticles and their in vitro biological activities. Elgorban, A. M., Aref, S. M., Seham, S. M., Elhindi, K. M., Bahkali, A. H., Sayed, S.
Microbiol. Res. 178, 9–17. doi: 10.1016/j.micres.2015.05.009 R., et al. (2016). Extracellular synthesis of silver nanoparticles using Aspergillus
Ballotin, D., Fulaz, S., Souza, M. L., Corio, P., Rodrigues, A. G., Souza, A. versicolor and evaluation of their activity on plant pathogenic fungi. Mycosphere
O., et al. (2016). Elucidating protein involvement in the stabilization 7, 844–852. doi: 10.5943/mycosphere/7/6/15
of the biogenic silver nanoparticles. Nanoscale Res. Lett. 11:313. El-Moslamy, S. H., Elkady, M. F., Rezk, A. H., and Abdel-Fattah, Y. R. (2017).
doi: 10.1186/s11671-016-1538-y Applying Taguchi design and large-scale strategy for mycosynthesis of nano-
Banu, A. N., and Balasubramanian, C. (2014a). Optimization and synthesis of silver from endophytic Trichoderma harzianum SYA.F4 and its application
silver nanoparticles using Isaria fumosorosea against human vector mosquitoes. against phytopathogens. Sci. Rep. 7:45297. doi: 10.1038/srep45297
Parasitol. Res. 113, 3843–3851. doi: 10.1007/s00436-014-4052-0 El-Sonbaty, S. M. (2013). Fungus-mediated synthesis of silver nanoparticles
Banu, A. N., and Balasubramanian, C. (2014b). Mycosynthesis of and evaluation of antitumor activity. Cancer Nanotechnol. 4, 73–79.
silver nanoparticles using Beauveria bassiana against dengue vector, doi: 10.1007/s12645-013-0038-3
Aedes aegypti (Diptera:Culicidae). Parasitol. Res. 113, 2869–77. Fátima, F., Verma, S. R., Pathak, N., and Bajpai, P. (2016). Extracellular
doi: 10.1007/s00436-013-3656-0 mycosynthesis of silver nanoparticles and their microbicidal activity. J. Glob.
Basavaraja, S., Balaji, S. D., Lagashetty, A., Rajasab, A. H., and Venkataraman, Antimicrob. Resist. 7, 88–92. doi: 10.1016/j.jgar.2016.07.013
A. (2008). Extracellular biosynthesis of silver nanoparticles using Fayaz, A. M., Balaji, K., Kalaichelvan, P. T., and Venkatesan, R. (2009).
the fungus Fusarium semitectum. Mater. Res. Bull. 43, 1164–1170. Fungal based synthesis of silver nanoparticles—an effect of temperature
doi: 10.1016/j.materresbull.2007.06.020 on the size of particles. Colloids Surf. B Biointerfaces. 74, 123–126.
Baymiller, M., Huang, F., and Rogelj, S. (2017). Rapid one-step synthesis of doi: 10.1016/j.colsurfb.2009.07.002
gold nanoparticles using the ubiquitous coenzyme NADH. Matters. 2017, 1–4. Gade, A. K., Bonde, P., Ingle, A. P., Marcato, P. D., Durán, N., and Rai,
doi: 10.19185/matters.201705000007 M. K. (2008). Exploitation of Aspergillus niger for synthesis of silver
nanoparticles. J. Biobased Mater. Bioenergy. 2, 243–247. doi: 10.1166/jbmb.20 activity against pathogenic yeasts. Mem. Inst. Oswaldo Cruz. 109, 220–228.
08.401 doi: 10.1590/0074-0276130269
Gaikwad, S., Ingle, A., Gade, A., Rai, M., Falanga, A., Incoronato, N., et al. Kamil, D., Prameeladevi, T., Ganesh, S., Prabakharan, N., Nareshkumar, R.,
(2013). Antiviral activity of mycosynthesized silver nanoparticles against herpes and Thomas, S. P. (2017). Green synthesis of silver nanoparticles by
simplex virus and human parainfluenza virus type 3. Int. J. Nanomed. 8, entomopathogenic fungus Beauveria bassiana and their bioefficacy against
4303–4314. doi: 10.2147/IJN.S50070 mustard aphid (Lipaphis erysimi Kalt.). Indian J. Exp. Biol. 55, 555–561.
Gajbhiye, M., Kesharwani, J., Ingle, A., Gade, A., and Rai, M. (2009). Kaviya, S., Santhanalakshmi, J., and Viswanathan, B. (2011). Green synthesis
Fungus-mediated synthesis of silver nanoparticles and their activity against of silver nanoparticles using Polyalthia longifolia leaf extract along with
pathogenic fungi in combination with fluconazole. Nanomedicine 5, 382–386. D-sorbitol: study of antibacterial activity. J. Nanotechnol. 2011:152970.
doi: 10.1016/j.nano.2009.06.005 doi: 10.1155/2011/152970
Gherbawy, Y. A., Shalaby, I. M., El-Sadek, M. S. A., Elhariry, H. M., and Banaja, Khan, N. T., Khan, M. J., Jameel, J., Jameel, N., and Rheman, S. U. A. (2017).
A. A. (2013). The anti-fasciolasis properties of silver nanoparticles produced An overview: biological organisms that serves as nanofactories for metallic
by Trichoderma harzianum and their improvement of the anti-fasciolasis drug nanoparticles synthesis and fungi being the most appropriate. Bioceram Dev.
triclabendazole. Int. J. Mol. Sci. 14, 21887–21898. doi: 10.3390/ijms141121887 Appl. 7:101. doi: 10.4172/2090-5025.1000101
Gholami-Shabani, M., Akbarzadeh, A., Norouzian, D., Amini, A., Gholami- Khandel, P., and Shahi, S. K. (2018). Mycogenic nanoparticles and their bio-
Shabani, Z., Imani, A., et al. (2014). Antimicrobial activity and physical prospective applications:current status and future challenges. J. Nanostr. Chem.
characterization of silver nanoparticles green synthesized using nitrate 8, 369–391. doi: 10.1007/s40097-018-0285-2
reductase from Fusarium oxysporum. Appl. Biochem. Biotechnol. 172, Kim, S. H., Lee, H. S., Ryu, D. S., Choi, S. J., and Lee, D. S. (2011). Antibacterial
4084–4098. doi: 10.1007/s12010-014-0809-2 activity of silver-nanoparticles against Staphylococcus aureus and Escherichia
Gole, A., Dash, C., Ramakrishnan, V., Sainkar, S. R., Mandale, A. B., Rao, M., coli. Korean J. Microbiol. Biotechnol. 39, 77–85.
et al. (2001). Pepsin–gold colloid conjugates: preparation, characterization, and Kim, S. W., Jung, J. H., Lamsal, K., Kim, Y. S., Min, J. S., and Lee, Y. S.
enzymatic activity. Langmuir 17, 1674–1679. doi: 10.1021/la001164w (2012). Antifungal effects of silver nanoparticles (AgNPs) against various plant
Gopinath, V., Mubarakali, D., Priyadarshini, S., Priyadarsshini, M., Thajuddin, N., pathogenic fungi. Mycobiology 40, 53–58. doi: 10.5941/MYCO.2012.40.1.053
and Velusamy, P. (2012). Biosynthesis of silver nanoparticles from Tribulus Korbekandi, H., Ashari, Z., Iravani, S., and Abbasi, S. (2013). Optimization of
terrestris and its antimicrobial activity: a novel biological approach. Colloids biological synthesis of silver nanoparticles using Fusarium oxysporum. Iran. J.
Surf. B Biointerfaces 96, 69–74. doi: 10.1016/j.colsurfb.2012.03.023 Pharm. Res. 12, 289–298.
Gudikandula, K., Vadapally, P., and Charya, M. A. S. (2017). Biogenic synthesis Kumar, S. A., Abyaneh, M. K., Gosavi, S. W., Kulkarni, S. K., Pasricha, N., Ahmad,
of silver nanoparticles from white rot fungi: their characterization and A., et al. (2007). Nitrate reductase-mediated synthesis of silver nanoparticles
antibacterial studies. Open Nano 2, 64–78. doi: 10.1016/j.onano.2017.07.002 from AgNO3 . Biotechnol. Lett. 29, 439–445. doi: 10.1007/s10529-006-9256-7
Guilger, M., Pasquoto-Stigliani, T., Bilesky-Jose, N., Grillo, R., Abhilash, P. C., Lee, S. H., and Jun, B. H. (2019). Silver nanoparticles: synthesis and application for
Fraceto, L. F., et al. (2017). Biogenic silver nanoparticles based on Trichoderma nanomedicine. Int. J. Mol. Sci. 20:E865. doi: 10.3390/ijms20040865
harzianum: synthesis, characterization, toxicity evaluation and biological Li, W., Xie, X., Shi, Q., Zeng, H., Ou-Yang, Y., and Chen, Y. (2010). Antibacterial
activity. Sci. Rep. 7:44421. doi: 10.1038/srep44421 activity and mechanism of silver nanoparticles on Escherichia coli. Appl.
Gupta, R. K., Kumar, V., Gundampati, R. K., Malviya, M., Hasan, S. H., Microbiol. Biotechnol. 85, 1115–1122. doi: 10.1007/s00253-009-2159-5
Jagannadham, M. V., et al. (2017). Biosynthesis of silver nanoparticles from Liang, M., Wei, S., Jian-Xin, L., Xiao-Xi, Z., Zhi, H., Wen, L., et al. (2017).
the novel strain of Streptomyces Sp. BHUMBU-80 with highly efficient Optimization for extracellular biosynthesis of silver nanoparticles by
electroanalytical detection of hydrogen peroxide and antibacterial activity. J. Penicillium aculeatum Su1 and their antimicrobial activity and cytotoxic
Environ. Chem. Eng. 5, 5624–5635. doi: 10.1016/j.jece.2017.09.029 effect compared with silver ions. Mater. Sci. Eng. C 77, 963–971.
Gurunathan, S., Kalishwaralal, K., Vaidyanathan, R., Deepak, V., Pandian, S. R. doi: 10.1016/j.msec.2017.03.294
K., Muniyand, J., et al. (2009). Biosynthesis, purification and characterization Loo, Y. Y., Rukayadil, Y., Nor-Khaizura, M. A. R., Kuan, C. H., Chieng, B.
of silver nanoparticles using Escherichia coli. Colloids Surf. B Biointerfaces 74, W., Nishibuchi, M., et al. (2018). In vitro antimicrobial activity of green
328–335. doi: 10.1016/j.colsurfb.2009.07.048 synthesized silver nanoparticles against selected gram-negative foodborne
Hamedi, S., Ghaseminezhad, M., Shokrollahzadeh, S., and Shojaosadati, pathogens. Front. Microbiol. 9:1555. doi: 10.3389/fmicb.2018.01555
S. A. (2017). Controlled biosynthesis of silver nanoparticles using Lu, Z., Rong, K., Li, J., Yang, H., and Chen, R. (2013). Size-dependent antibacterial
nitrate reductase enzyme induction of filamentous fungus and their activities of silver nanoparticles against oral anaerobic pathogenic bacteria. J.
antibacterial evaluation. Artif. Cells Nanomed. Biotechnol. 45, 1588–1596. Mater. Sci. 24, 1465–1471. doi: 10.1007/s10856-013-4894-5
doi: 10.1080/21691401.2016.1267011 Mekkawy, A. I., El-Mokhtar, M. A., Nafady, N. A., Yousef, N., Hamad, M.
Hietzschold, S., Walter, A., Davis, C., Taylor, A. A., and Sepunaru, L. (2019). A., El-Shanawany, S. M., et al. (2017). In vitro and in vivo evaluation of
Does nitrate reductase play a role in silver nanoparticle synthesis? Evidence for biologically synthesized silver nanoparticles for topical applications: effect of
NADPH as the sole reducing agent. ACS Sustain. Chem. Eng. 7, 8070–8076. surface coating and loading into hydrogels. Int. J. Nanomed. 12, 759–777.
doi: 10.1021/acssuschemeng.9b00506 doi: 10.2147/IJN.S124294
Hu, C. J., Zhang, L., Aryal, S., Cheung, C., Fang, R. H., and Zhang, L. Metuku, R. P., Pabba, S., Burra, S., Hima Bindu N, S. V. S. S. S. L., Gudikandula,
(2011). Erythrocyte membrane-camouflaged polymeric nanoparticles as a K., Singara and Charya, M. A. (2014). Biosynthesis of silver nanoparticles from
biomimetic delivery platform. Proc. Natl. Acad. Sci. U.S.A. 108, 10980–10985. Schizophyllum radiatum HE 863742.1: their characterization and antimicrobial
doi: 10.1073/pnas.1106634108 activity. 3 Biotech 4, 227–234. doi: 10.1007/s13205-013-0138-0
Husseiny, S. M., Salah, T. A., and Anter, H. A. (2015). Biosynthesis of size Mishra, S., and Singh, H. B. (2015). Biosynthesized silver nanoparticles
controlled silver nanoparticles by Fusarium oxysporum, their antibacterial as a nanoweapon against phytopathogens: exploring their scope and
and antitumoral activities. Beni Suef Univer. J. Basic Appl. Sci. 4, 225–31. potential in agriculture. Appl. Microbiol. Biotechnol. 99, 1097–1107.
doi: 10.1016/j.bjbas.2015.07.004 doi: 10.1007/s00253-014-6296-0
Ibrahim, H. M. M., and Hassan, M. S. (2016). Characterization and antimicrobial Moazeni, M., Rashidi, N., Shahverdi, A. R., Noorbakhsh, F., and Rezaie, S. (2012).
properties of cotton fabric loaded with green synthesized silver nanoparticles. Extracellular production of silver nanoparticles by using three common species
Carbohydr. Polym. 151, 841–850. doi: 10.1016/j.carbpol.2016.05.041 of dermatophytes: Trichophyton rubrum, Trichophyton mentagrophytes and
Iravani, S., Korbekandi, H., Mirmohammadi, S. V., and Zolfaghari, B. (2014). Microsporum canis. Iran. Biomed. J. 16, 52–58. doi: 10.6091/IBJ.1001.2012
Synthesis of silver nanoparticles: chemical, physical and biological methods. Mohanta, Y. K., Nayak, D., Biswas, K., Singdevsachan, S. K., Abd_Allah,
Res. Pharm. Sci. 9, 385–406. E. F., Hashem, A., et al. (2018). Silver nanoparticles synthesized
Ishida, K., Cipriano, T. F., Rocha, G. M., Weissmüller, G., Gomes, F., using wild mushroom show potential antimicrobial activities against
Miranda, K., et al. (2014). Silver nanoparticle production by the fungus food borne pathogens. Molecules 23, 1–18. doi: 10.3390/molecules230
Fusarium oxysporum: nanoparticle characterisation and analysis of antifungal 30655
Molnár, Z., Bódai, V., Szakacs, G., Erdélyi, B., Fogarassy, Z., Sáfrán, G., et al. (2018). Rani, R., Sharma, D., Chaturvedi, M., and Yadav, J. P. (2017). Green
Green synthesis of gold nanoparticles by thermophilic filamentous fungi. Sci. synthesis, characterization and antibacterial activity of silver nanoparticles
Rep. 8:3943. doi: 10.1038/s41598-018-22112-3 of endophytic fungi Aspergillus terreus. J. Nanomed. Nanotechnol. 8:4.
Morones, J. R., Elichiguerra, J. L., Camacho, A., Holt, K., Kouri, J. B., Ramírez, J. doi: 10.4172/2157-7439.1000457
T., et al. (2005). The bactericidal effect of silver nanoparticles. Nanotechnology Reidy, B., Haase, A., Luch, A., and Dawson, K. (2013). Mechanisms of silver
16, 2346–2353. doi: 10.1088/0957-4484/16/10/059 nanoparticle release, transformation and toxicity: a critical review of current
Mout, R., Moyano, D. F., Rana, S., and Rotello, V. M. (2012). Surface knowledge and recommendations for future studies and applications. Materials
functionalization of nanoparticles for nanomedicine. Chem. Soc. Rev. 41, 6, 2295–2350. doi: 10.3390/ma6062295
2539–2544. doi: 10.1039/c2cs15294k Rheder, D. T., Guilger, M., Bilesky-José, N., Germano-Costa, T., Pasquoto-
Nagajyothi, P. C., Sreekanth, T. V. M., Lee, J., and Lee, K. D. (2014). Mycosynthesis: Stigliani, T., Gallep, T. B. B., et al. (2018). Synthesis of biogenic silver
antibacterial, antioxidant and antiproliferative activities of silver nanoparticles nanoparticles using Althaea officinalis as reducing agent: evaluation of toxicity
synthesized from Inonotus obliquus (Chaga mushroom) extract. J. Photochem. and ecotoxicity. Sci Rep. 8:12397. doi: 10.1038/s41598-018-30317-9
Photobiol. B 130, 299–304. doi: 10.1016/j.jphotobiol.2013.11.022 Rodrigues, A. G., Ping, L. Y., Marcato, P. D., Alves, O. L., Silva, M. C. P.,
Naqvi, S. Z. H., Kiran, U., Ali, M. I., Jamal, A., Hameed, A., Ahmed, S., et al. (2013). Ruiz, R. C., et al. (2013). Biogenic antimicrobial silver nanoparticles produced
Combined efficacy of biologically synthesized silver nanoparticles and different by fungi. Appl. Microbiol. Biotechnol. 97, 775–782. doi: 10.1007/s00253-012-
antibiotics against multidrug-resistant bacteria. Int. J. Nanomed. 8, 3187–3195. 4209-7
doi: 10.2147/IJN.S49284 Rose, G. K., Soni, R., Rishi, P., and Soni, S. K. (2019). Optimization of the biological
Nayak, B. K., Nanda, A., and Prabhakar, V. (2018). Biogenic synthesis of synthesis of silver nanoparticles using Penicillium oxalicum GRS-1 and their
silver nanoparticle from wasp nest soil fungus, Penicillium italicum and its antimicrobial effects against common food-borne pathogens. Green Process
analysis against multi drug resistance pathogens. Biocatal. Agric. Biotechnol. 16, Synth. 8, 144–156. doi: 10.1515/gps-2018-0042
412–418. doi: 10.1016/j.bcab.2018.09.014 Sabri, M. A., Umer, A., Awan, G. H., Hassan, M. F., and Hasnain, A. (2016).
Nayak, R. R., Pradhan, N., Behera, D., Pradhan, K. M., Mishra, S., Sukla, Selection of suitable biological method for the synthesis of silver nanoparticles.
L. B., et al. (2011). Green synthesis of silver nanoparticle by Penicillium Nanomater Nanotechnol. 6, 1–20. doi: 10.5772/62644
purpurogenum NPMF: the process and optimization. J. Nanopart. Res. 13, Saxena, J., Sharma, P. K., Sharma, M. M., and Singh, A. (2016). Process
3129–3137. doi: 10.1007/s11051-010-0208-8 optimization for green synthesis of silver nanoparticles by Sclerotinia
Netala, V. R., Bethu, M. S., Pushpalatah, B., Baki, V. B., Aishwarya, S., Rao, J. sclerotiorum MTCC 8785 and evaluation of its antibacterial properties.
V., et al. (2016). Biogenesis of silver nanoparticles using endophytic fungus Springerplus 5:861. doi: 10.1186/s40064-016-2558-x
Pestalotiopsis microspora and evaluation of their antioxidant and anticancer Shahzad, A., Saeed, H., Iqtedar, M., Hussain, S. Z., Kaleem, A., and Abdullah,
activities. Int. J. Nanomed. 11, 5683–5696. doi: 10.2147/IJN.S112857 R. (2019). Size-controlled production of silver nanoparticles by Aspergillus
Ottoni, C. A., Simões, M. F., Fernandes, S., Santos, J. G., Silva, E. S., Souza, R. fumigatus BTCB10: likely antibacterial and cytotoxic effects. J. Nanomater.
F. B., et al. (2017). Screening of filamentous fungi for antimicrobial silver 2019:5168698. doi: 10.1155/2019/5168698
nanoparticles synthesis. AMB Express 7:31. doi: 10.1186/s13568-017-0332-2 Shrivastava, S., Bera, T., Roy, A., Singh, G., Ramachandrarao, P.,
Owaid, M. N., Raman, J., Lakshmanan, H., Al-Saeedi, S. S. S., Sabaratnam, V., and Dash, D. (2007). Characterization of enhanced antibacterial
and Abed, I. A. (2015). Mycosynthesis of silver nanoparticles by Pleurotus effects of novel silver nanoparticles. Nanotechnology 18:225103.
cornucopiae var. citrinopileatus and its inhibitory effects against Candida sp. doi: 10.1088/0957-4484/18/22/225103
Mater. Lett. 153, 186–190. doi: 10.1016/j.matlet.2015.04.023 Singh, D., Rathod, V., Ninganagouda, S., Hiremath, J., Singh, A. K., and Mathew, J.
Pereira, L., Dias, N., Carvalho, J., Fernandes, S., Santos, C., and Lima, N. (2014). (2014). Optimization and characterization of silver nanoparticle by endophytic
Synthesis, characterization and antifungal activity of chemically and fungal- fungi Penicillium sp. isolated from Curcuma longa (Turmeric) and application
produced silver nanoparticles against Trichophyton rubrum. J. Appl. Microbiol. studies against MDR E. coli and S. aureus. Bioinorg. Chem. Appl. 2014:408021.
117, 1601–1613. doi: 10.1111/jam.12652 doi: 10.1155/2014/408021
Phanjom, P., and Ahmed, G. (2017). Effect of different physicochemical conditions Singh, R., Shedbalkar, U. U., Wadhwani, S. A., and Chopade, B. A. (2015).
on the synthesis of silver nanoparticles using fungal cell filtrate of Aspergillus Bacteriagenic silver nanoparticles: synthesis, mechanism, and applications.
oryzae (MTCC No. 1846) and their antibacterial effects. Adv. Nat. Sci. Nanosci. Appl. Microbiol. Biotechnol. 99, 4579–4593. doi: 10.1007/s00253-015-
Nanotechnol. 8, 1–13. doi: 10.1088/2043-6254/aa92bc 6622-1
Prabhu, S., and Poulose, E. K. (2012). Silver Nanoparticles: mechanism of Singh, T., Jyoti, K., Patnaik, A., Singh, A., Chauhan, R., and Chandel, S. S. (2017).
antimicrobial action, synthesis, medical applications, and toxicity effects. Int. Biosynthesis, characterization and antibacterial activity of silver nanoparticles
Nano Lett. 2:32. doi: 10.1186/2228-5326-2-32 using an endophytic fungal supernatant of Raphanus sativus. J. Genet. Eng.
Qian, Y., Yu, H., He, D., Yang, H., Wang, W., Wan, X., et al. (2013). Biosynthesis Biotechnol. 15, 31–39. doi: 10.1016/j.jgeb.2017.04.005
of silver nanoparticles by the endophytic fungus Epicoccum nigrum and their Sintubin, L., Windt, W. D., Dick, J., Mast, J., Ha, D. V. D., Verstraete, W., et al.
activity against pathogenic fungi. Bioprocess Biosyst. Eng. 36, 1613–1619. (2009). Lactic acid bacteria as reducing and capping agent for the fast and
doi: 10.1007/s00449-013-0937-z efficient production of silver nanoparticles. Appl. Microbiol. Biotechnol. 84,
Qidwai, A., Pandey, A., Kumar, R., Shukla, S. K., and Dikshit, A. (2018). Advances 741–749. doi: 10.1007/s00253-009-2032-6
in biogenic nanoparticles and the mechanisms of antimicrobial effects. Indian Sriram, M. I., Kanth, S. B. M., Kalishwaralal, K., and Gurunathan, S. (2010).
J. Pharm. Sci. 80, 592–603. doi: 10.4172/pharmaceutical-sciences.1000398 Antitumor activity of silver nanoparticles in Dalton’s lymphoma ascites tumor
Rai, M., Kon, K., Ingle, A., Duran, N., Galdiero, S., and Galdiero, M. model. Int. J. Nanomed. 5, 753–762. doi: 10.2147/IJN.S11727
(2014). Broad-spectrum bioactivities of silver nanoparticles: the emerging Sundaravadivelan, C., and Padmanabhan, M. N. (2014). Effect of mycosynthesized
trends and future prospects. Appl. Microbiol. Biotechnol. 98, 1951–1961. silver nanoparticles from filtrate of Trichoderma harzianum against larvae and
doi: 10.1007/s00253-013-5473-x pupa of dengue vector Aedes aegypti L. Environ. Sci. Pollut. Res. 21, 4624–4633.
Rai, M., Yadav, A., and Gade, A. (2009). Silver nanoparticles as a doi: 10.1007/s11356-013-2358-6
new generation of antimicrobials. Biotechnol. Adv. 27, 76–83. Thakkar, K. N., Mhatre, S. S., and Parikh, R. Y. (2010). Biological
doi: 10.1016/j.biotechadv.2008.09.002 synthesis of metallic nanoparticles. Nanomedicine 6, 257–262.
Rajput, S., Werezuk, R., Lange, R. M., and Mcdermott, M. T. (2016). Fungal doi: 10.1016/j.nano.2009.07.002
isolate optimized for biogenesis of silver nanoparticles with enhanced colloidal Vahabi, K., Mansoori, G. A., and Karimi, S. (2011). Biosynthesis of
stability. Langmuir 32, 8688–8697. doi: 10.1021/acs.langmuir.6b01813 silver nanoparticles by fungus Trichoderma reesei. Insci. J. 1, 65–79.
Raman, J., Reddy, G. R., Lakshmanan, H., Selvaraj, V., Gajendran, B., Nanjian, R., doi: 10.5640/insc.010165
et al. (2015). Mycosynthesis and characterization of silver nanoparticles from Velusamy, P., Kumar, G. V., Jeyanthi, V., Das, J., and Pachaiappan, R. (2016).
Pleurotus djamor var. roseus and their in vitro cytotoxicity effect onPC3 cells. Bio-inspired green nanoparticles: synthesis, mechanism, and antibacterial
Process Biochem. 50, 140–147. doi: 10.1016/j.procbio.2014.11.003 application. Toxicol. Res. 32, 95–102. doi: 10.5487/TR.2016.32.2.095
Xue, B., He, D., Gao, S., Wang, D., Yokoyama, K., and Wang, L. (2016). Zomorodian, K., Pourshahid, S., Sadatsharifi, A., Mehryar, P., Pakshir, K., Rahimi,
Biosynthesis of silver nanoparticles by the fungus Arthroderma fulvum and its M. J., et al. (2016). Biosynthesis and characterization of silver nanoparticles by
antifungal activity against genera of Candida, Aspergillus and Fusarium. Int. J. Aspergillus species. Biomed Res. Int. 2016:5435397. doi: 10.1155/2016/5435397
Nanomed. 11, 1899–1906. doi: 10.2147/IJN.S98339
Yahyaei, B., and Pourali, P. (2019). One step conjugation of some Conflict of Interest: The authors declare that the research was conducted in the
chemotherapeutic drugs to the biologically produced gold nanoparticles absence of any commercial or financial relationships that could be construed as a
and assessment of their anticancer effects. Sci. Rep. 9:10242. potential conflict of interest.
doi: 10.1038/s41598-019-46602-0
Zhang, X. F., Liu, Z. G., Shen, W., and Gurunathan, S. (2016). Silver Copyright © 2019 Guilger-Casagrande and Lima. This is an open-access article
nanoparticles: synthesis, characterization, properties, applications, and distributed under the terms of the Creative Commons Attribution License (CC BY).
therapeutic approaches. Int. J. Mol. Sci. 17:E1534. doi: 10.3390/ijms170 The use, distribution or reproduction in other forums is permitted, provided the
91534 original author(s) and the copyright owner(s) are credited and that the original
Zielonka, A., and Klimek-Ochab, M. (2017). Fungal synthesis of size- publication in this journal is cited, in accordance with accepted academic practice.
defined nanoparticles. Adv. Nat. Sci.: Nanosci. Nanotechnol. 8:043001. No use, distribution or reproduction is permitted which does not comply with these
doi: 10.1088/2043-6254/aa84d4 terms.

Synthesis of Silver Nanoparticles Mediated by Fungi: A Review

Uploaded by

Document Informationclick to expand document information

Copyright:

Available Formats

Synthesis of Silver Nanoparticles Mediated by Fungi: A Review

Uploaded by

Document Information

Original Title

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

Synthesis of Silver Nanoparticles Mediated by Fungi: A Review

Uploaded by

Copyright:

Available Formats

REVIEW

published: 22 October 2019

Synthesis of Silver Nanoparticles

FIGURE 1 | Mechanisms of biogenic synthesis of silver nanoparticles.

TABLE 1 | Optimization of the synthesis of silver nanoparticles by fungi.

Fungus Type of parameter Optimized conditions Nanoparticle References

Fungus Type of parameter Optimized conditions Nanoparticle References

FIGURE 2 | Differences between capped and uncapped silver nanoparticles.

FIGURE 3 | Applications of silver nanoparticles synthesized using fungi.

TABLE 2 | Health applications of silver nanoparticles synthesized by fungi.

Synthesis source Bioactivity Target organism Effective concentration References

Synthesis source Bioactivity Target organism Effective concentration References

REFERENCES Bérdy, J. (2005). Bioactive microbial metabolites. J. Antibiot. 58, 1–26.

You might also like