Diversity of Mycogenic Oxide and Chalcogenide Nanoparticles: A Review

Abstract

Oxide and chalcogenide nanoparticles have great potential for use in biomedicine, engineering, agriculture, environmental protection, and other research fields. The myco-synthesis of nanoparticles with fungal cultures, their metabolites, culture liquids, and mycelial and fruit body extracts is simple, cheap and environmentally friendly. The characteristics of nanoparticles, including their size, shape, homogeneity, stability, physical properties and biological activity, can be tuned by changing the myco-synthesis conditions. This review summarizes the data on the diversity of oxide and chalcogenide nanoparticles produced by various fungal species under different experimental conditions.

1. Introduction

Nanotechnology and nanomaterials science are rapidly developing fields, which contribute greatly to the development of modern technology and biomedicine. An important challenge is the development of simple, effective, and cheap methods of producing highly monodispersed, stable, and biocompatible nanoparticles (NPs) with the required chemical composition, shape, size, biological activity, and other properties. The recent increase in attention to environmental safety, natural resource exhaustibility, and human health safety has led to the increasing development of green NP-producing technologies by biosynthesis methods [1,2,3,4]. Owing to its being environmentally benign and less resource-intensive than other methods, the synthesis of nontoxic and biocompatible NPs by using living organisms and a variety of biological materials derived from them is a promising alternative to physical and chemical fabrication methods.

The ability to biosynthesize NPs has been found in many organisms, including animals, plants, bacteria, fungi, actinomycetes, algae, lichens, and viruses [5]. Among this diversity of biological objects used for green NP synthesis, a special place is occupied by fungi [6,7,8]. Fungal cultures produce a wide range of proteins with high enzymatic activity, and due to that they can convert metals and other elements into less toxic forms. This includes the formation of NPs, which then accumulate in large quantities within the mycelium and/or extracellularly. As a result, micro- and macro-mycetes from different taxonomic groups can be successfully used to produce NPs and nanomaterials on an industrial scale. The applications of fungi in myco-nano-synthesis are also highly versatile. NPs with different characteristics can be obtained either by growing fungal cultures on media with precursors or by incubating these precursors with mycelial bio-mass, culture liquid filtrates, extracts from vegetative mycelium, fruiting bodies and other morpho-structures, and purified proteins and other metabolites isolated from fungi [5]. In addition, the properties of biogenic NPs depend on medium composition, chemical composition and concentration of the precursor, incubation time, stirring rate, temperature, pH and other conditions. By varying these, the chemical composition, shape, size, homogeneity, stability, and biological activity of formed particles can be controlled [9,10,11,12].

Fungal cultures can form NPs of various chemical compositions. The myco-synthesis of elementary gold and silver NPs is the most commonly studied so far, whereas a number of other metals and metalloids have been studied to a lesser extent. In addition, fungi can form NPs of a more complex chemical composition, such as oxides and salts. Among the inorganic NPs, metal oxide and chalcogenide (sulfide, selenide, and telluride) NPs are of great interest for multidisciplinary nanotechnology. They can find a wide range of applications owing to their special physical, chemical, and biological properties, which distinguish them from bulk materials of the same chemical composition [13,14].

Oxide NPs are promising for use in nano-catalysis, biosensing, biomedicine, wastewater purification, and removal of heavy metals, dyes, and microbial contaminants [14,15,16,17,18,19]. Applications for chalcogenide NPs include cell imaging, cancer research and therapy, antimicrobials, and energy and optoelectronics applications [13,20,21,22]. An important group of NPs are quantum dots (QDs), a type of small (less than 10 nm) colloidal fluorescent semiconducting nanocrystalline particles composed of group II–VI, III–V, or IV elements [13,23,24]. Owing to their unique structural, optical, electrochemical, and photochemical properties, QDs can be used in numerous technological applications, such as biosensing, bioimaging, photovoltaics, nanomedicine, and drug delivery.

Because of this widespread demand for nanoparticles and nanomaterials of oxides and chalcogenides, the study of their synthesis by fungi has started to develop rapidly in recent years. However, until now, little attention has been paid to the comparison of the properties of nanoparticles of the same compound obtained with different species of fungi and under different conditions, and, consequently, to the optimization of the process to obtain nanoparticles with the desired properties. This review summarizes the current information on the myco-synthesis of nanoparticles of oxides, sulfides, selenides, and tellurides by fungi belonging to different taxonomic groups, the variety of their characteristics under different synthetic conditions, and the potential for their further application.

2. Myco-Synthesis of Oxide Nanoparticles

To date, the ability to form elementary metal and metalloid NPs has been found in many fungal species. However, the number of elements that can be sources of mycogenic NPs is rather small and includes gold, silver, platinum, palladium, iron, copper, selenium, and tellurium [5]. For oxides and salts, the range of chemical composition for mycogenic NPs is much wider, yet most of them remain very poorly studied. Among fungi-mediated oxide NPs, titanium, zinc, iron, and copper oxides have been studied to the greatest extent.

2.1. Myco-Synthesis of Copper Oxide Nanoparticles

Copper oxide NPs have attracted high attention because copper is one of the most important elements in modern technologies and is readily accessible [25]. Copper oxide is widely used in catalysis, superconductors, thermoelectric and sensing materials, ceramics, gas sensors, and many other fields. Biomedical applications of these NPs include biosensors, cancer medicine, and antimicrobials [26]. In recent years, the fungi-mediated synthesis of copper oxide NPs has become of interest (

Table 1. Myco-synthesis of copper oxide nanoparticles.

NP	Species	Source	Precursors	Shape and Size	Reference
CuO	Aspergillus flavus	Culture liquid	CuSO4	Spherical (average size of 32.4 nm)	[27]
CuO	Aspergillus terreus	Culture liquid	CuSO4	–	[28,29]
CuO	Aspergillus terreus	Culture liquid	CuSO4	Below 100 nm	[30]
CuO	Penicillium chrysogenum	Culture liquid	CuSO4	Spherical (average size of 9.7 nm)	[31]
CuO	Trichoderma asperellum	Mycelial extract	Cu(NO3)2	Spherical (10–190 nm)	[32]
CuO	Trichoderma harzianum	Mycelial extract	CuSO4	Nano-fibers (38–77 nm in width, 135–320 nm in length)	[33]
Cu2O, CuO	Stereum hirsutum	Mycelial extract	CuCl2	Spherical (5–20 nm)	[34]
CuxOy	Penicillium aurantiogriseum	Culture liquid	CuSO4	Spherical (89–250 nm)	[35]
CuxOy	Penicillium citrinum	Culture liquid	CuSO4	Spherical (85–295 nm)	[35]
CuxOy	Penicillium waksmanii	Culture liquid	CuSO4	Spherical (79–179 nm)	[35]
CuxOy	Pleurotus florida	Bio-mass	CuCl2	Spherical, partially spherical, oval (22.55–60.09 nm)	[36]
			CuSO4	Hexagonal, partially spherical (12.82–48.86 nm)

).

CuO nanospheres (average size 32.4 nm) with high antimicrobial and antitumor activities were obtained with Aspergillus flavus culture liquid [27]. CuO NPs synthesized with Aspergillus terreus culture liquid showed anticancer activity in a concentration-dependent manner [30]. Other works showed that CuO nanospheres synthesized with A. terreus culture liquid had potent antioxidant and antimicrobial activities [28,29].

Honary et al. studied copper oxide NP synthesis by three Penicillium species [35]. Penicillium aurantiogriseum, Penicillium citrinum, and Penicillium waksmanii culture liquids mediated the fabrication of copper oxide nanospheres of various diameters. The effect of several parameters on the particle size and the polydispersity index for the synthesis of NPs under ambient conditions was also investigated. It was concluded that there is a direct correlation among pH value, precursor concentration, polydispersity index, and particle size. Spherical CuO NPs were also obtained with a Penicillium chrysogenum culture liquid filtrate with the aid of gamma rays at various doses [31]. The NPs were an active antibacterial agent against fungal and bacterial crop pathogens.

Copper oxide NPs of various sizes and shapes were synthesized with Pleurotus florida bio-mass and two different precursor salts [36]. Spherical, partially spherical, and oval particles (22.55–60.09 nm) were formed after the incubation with CuCl₂, whereas the use of CuSO₄ resulted in hexagonal and partially spherical NPs (12.82–48.86 nm).

Spherical copper oxide NPs with a size of 10 to 190 nm and an average diameter of 110 nm were synthesized with a cell-free extract of Trichoderma asperellum [32]. These NPs induced photo-thermolysis of human lung cancer cells. CuO NPs with a rare morphology were obtained by Consolo and colleagues with a Trichoderma harzianum extract [33]. These particles were in the shape of elongated fibers 38–77 nm in width and 135–320 nm in length, and were inhibitory to fungal phytopathogens.

A Stereum hirsutum mycelial extract was found to be effective at synthesizing copper NPs [34]. Copper/copper oxide NP fabrication was studied under different pH conditions and in the presence of three copper salts (CuCl₂, CuSO₄, and Cu(NO₃)₂). Greater NP formation was shown with 5 mM CuCl₂ under alkaline conditions. The resulting NPs were mainly spherical and had sizes of 5 to 20 nm.

2.2. Myco-Synthesis of Iron Oxide Nanoparticles

Iron oxide is a mineral compound that exists in various polymorphic forms, the main of which are hematite (α-Fe₂O₃), maghemite (γ-Fe₂O₃), and magnetite (Fe₃O₄) [15]. Mycogenic NPs of iron oxides (III) and (IV) obtained by different researchers with different biological objects and precursors differ greatly in both size and shape (

Table 2. Myco-synthesis of iron oxide nanoparticles.

NP	Species	Source	Precursors	Shape and Size	Reference
α-Fe2O3	Trichoderma harzianum	Mycelial extract	FeCl3	Spherical (average size of 207 nm)	[37]
γ-Fe2O3	Penicillium expansum	Mycelial extract	FeCl3	Spherical (15.0–66.0 nm)	[38]
γ-Fe2O3/α-Fe2O3	Alternaria alternata	Mycelial extract	Fe(NO3)3	Cubic (average size of 9 nm)	[39]
Fe2O3	Aspergillus niger	Bio-mass	FeCl3	–	[40]
Fe2O3	Fusarium incarnatum	Culture liquid	FeCl2 + FeCl3	Spherical (average size of 30.56 nm)	[41]
Fe2O3	Phialemoniopsis ocularis	Culture liquid	FeCl2 + FeCl3	Spherical (average size of 13.13 nm)	[41]
Fe2O3	Penicillium pimiteouiense	Culture liquid	FeCl2 + FeCl3	Spherical (2–16 nm)	[42]
Fe2O3	Trichoderma asperellum	Culture liquid	FeCl2 + FeCl3	Spherical (average size of 25 nm)	[41]
Fe3O4	Aspergillus niger	Mycelial extract	FeCl3	Nanoflakes (20–40 nm)	[43]
Fe3O4	Aspergillus terreus	Culture liquid	Fe(NO3)3	Spherical	[28,29]
Fe3O4	Aspergillus tamarii	Culture liquid	FeSO4 + FeCl3	Spherical (5–22 nm)	[44]
Fe3O4	Fusarium oxysporum	Bio-mass	K3[Fe(CN)6] + K4[Fe(CN)6]	Quasi-spherical (20–50 nm)	[45]
Fe3O4	Fusarium solani	Bio-mass	Fe2O3	Cubic, spherical, irregular (55.3–84.2 nm)	[46]
Fe3O4	Verticillium sp.	Bio-mass	K3[Fe(CN)6] + K4[Fe(CN)6]	Cubo-octahedral (100–400 nm)	[45]
FexOy	Amanita muscaria	Fruit body extract	FeCl2 + FeCl3	2.2–2.5 nm	[47]
FexOy	Aspergillus japonicus	Bio-mass	K3[Fe(CN)6] + K4[Fe(CN)6]	Cubic (60–70 nm)	[48]
FexOy	Pleurotus florida	Bio-mass	FeCl2	Cubic (11.90–167.63 nm)	[36]
			FeSO4	Spherical (11.16–98.81 nm), highly agglomerated

). Spherical, cubic, irregular, octahedral, and flakelike iron oxide nanoparticles were obtained with mushroom cultures.

Maghemite (γ-Fe₂O₃) nanospheres (15–66 nm) were synthesized with a Penicillium expansum mycelial extract filtrate [38]. These NPs were effective biocatalysts for the decolorization and degradation of textile and tanning wastewater effluents in a dose- and time-dependent manner. Spherical hematite (α-Fe₂O₃) NPs with a mean size of 207 nm, fabricated with a T. harzianum extract, enhanced T. harzianum biocontrol activity against the phytopathogen Sclerotinia sclerotiorum [37]. Small cubic Fe₂O₃ NPs with an average size of 9 nm, active against Gram-positive and Gram-negative bacteria, were obtained with an Alternaria alternata mycelial extract [39]. Synthesis of Fe₂O₃ nanospheres was also achieved with culture liquids of the manglicolous fungi T. asperellum, Phialemoniopsis ocularis, Fusarium incarnatum, and Penicillium pimiteouiense [41,42]. Their size varied depending on the species of fungus used for myco-synthesis. Manglicolous fungi–derived Fe₂O₃ NPs were effective in removing Cr (VI) from synthetic wastewater [42].

The fungi Fusarium oxysporum and Verticillium sp. formed iron oxide NPs predominantly in the magnetite (Fe₃O₄) phase [45]. Incubation of F. oxysporum bio-mass with precursors yielded quasi-spherical NPs, whereas Verticillium sp. produced cubo-octahedral particles. Superparamagnetic Fe₃O₄ nanoflakes 20–40 nm in width were fabricated with an Aspergillus niger mycelial extract [43]. The NPs were successfully used for Cr (VI) removal from an aqueous solution, which provides an eco-friendly, sustainable, and effective route to heavy metal remediation and wastewater treatment. Fe₃O₄ NPs obtained with lyophilized bio-mass of Fusarium solani were mostly cubic and spherical, with a mean size of 55.3–84.2 nm [46]. They had bactericidal activity against various bacteria, although it was weaker in comparison with that of silver NPs synthesized by F. solani in the same study. Mousa et al. fabricated Fe₃O₄ nanospheres with A. terreus culture liquid and determined optimal conditions for the maximal NP yield [28,29]. These NPs showed promising antioxidant activity and a potent effect against several plant and human pathogens.

Cubic iron oxide NPs (60–70 nm) were obtained with Aspergillus japonicus bio-mass, with K₃[Fe(CN)₆] and K₄[Fe(CN)₆] as precursors [48]. Incubation of P. florida mycelium with FeCl₂ yielded cubic NPs with an average size of 11.90 to 167.63 nm, whereas the FeSO₄ precursor produced highly agglomerated nanospheres with an average size of 11.16 to 98.81 nm [36].

Abdeen et al. used a combined method to produce magnetic Fe₃O₄ NPs [40]. A. niger bio-mass was used for the decomposition of FeSO₄ and FeCl₃ to FeS and Fe₂O₃, respectively. Then, the FeS and Fe₂O₃ NPs were used to produce pure iron and Fe₃O₄ nanospheres by a physical method.

Several researchers have used fungal cultures to obtain iron oxide nanocomposite materials with enhanced properties. Fe₃O₄ NPs with spherical morphology and size varying from 5 to 22 nm were myco-synthesized with an Aspergillus tamarii culture filtrate [44]. The conditions for NP production were optimized, including incubation period, stirring speed and time, temperature, and pH. The resulting Fe₃O₄ NPs were impregnated into chitosan beads to produce magnetic nanocomposite for textile wastewater treatment. The modified beads showed a good removal capability with improved stability and regeneration, as compared with the control chitosan beads. Another iron oxide NP–based biomaterial was obtained with a spent substrate for Agrocybe cylindracea [49]. The Fe₃O₄ NP–coated biomaterial described in that study was effective at Cr (VI) removal from wastewater. Ince et al. developed fungal bio-nanocomposite Fe₃O₄ materials effective at metal removal from drinks and wastewater. They synthesized chitosan-coated magnetic Fe₃O₄ NPs with an Agaricus campestris fruit body extract [50] and alginate-coated superparamagnetic Fe₃O₄ NPs with an Amanita vaginata fruit body extract [51]. Ultrasmall iron oxide NPs were fabricated with an Amanita muscaria fruit body extract [47]. Using these NPs, Ivashchenko and colleagues developed a gel formulation for local anticancer therapy, containing A. muscaria–derived iron oxide and silver NPs.

2.3. Titanium Oxide NPs

Titanium oxide (TiO₂) NPs are yet another important NPs with outstanding properties. Three mineral forms of TiO₂ that are known to occur naturally are anatase, rutile, and brookite. TiO₂ NPs have a wide range of applications owing to their chemical stability, low toxicity, biocompatibility, and good corrosion resistance [52]. Thanks to their high antibacterial, antifungal, antiviral, and anticancer activity, they are important tools in diagnostics, therapeutics, and drug delivery [53]. Various micro- and macro-mycetes can produce TiO₂ NPs with their living cultures, extracts, bio-mass, and even spores (

Table 3. Myco-synthesis of titanium oxide nanoparticles.

NP	Species	Source	Precursors	Shape and Size	Reference
TiO2	Agaricus bisporus	Spores	Ti(OC3H7)4	–	[54]
TiO2	Aspergillus flavus	Bio-mass	TiO2	Spherical, oval (62–74 nm)	[55]
TiO2	Aspergillus flavus	Mycelial extract	TiO2	12–15 nm	[56]
TiO2	Aspergillus niger	Mycelial extract	TiO2 salt	Spherical (73.58–106.9 nm)	[57]
TiO2	Aspergillus tubingensis	Mycelial extract	TiO2 salt	Cubic, pentangular (1.5–30 nm)	[58]
TiO2	Fomes fomentarius	Fruit body extract	Ti{OCH(CH3)2}4	Irregular (80–120 nm)	[59]
TiO2	Fomitopsis pinicola	Fruit body extract	Ti{OCH(CH3)2}4	Irregular (80–120 nm)	[60]
TiO	Fusarium oxysporum	Bio-mass	K2TiF6	Spherical (6–13 nm)	[61]
TiO2	Humicola sp.	Bio-mass	Bulk TiO2	Spherical (5–28 nm)	[62]
TiO2	Hypsizygus ulmarius	Fruit body extract	TiCl4	Spherical (average size of 80 nm)	[63]
TiO2	Pleurotus djamor	Fruit body extract	TiCl4	Spherical (average size of 31 nm)	[64]
TiO2	Pleurotus sajor caju	Fruit body extract	TiCl4	Spherical (average size of 85 nm)	[65]
TiO2	Sachharomyces cerevisae	Living culture	TiO(OH)2	Spherical (average size of 12.57 nm)	[66]
TiO2	Sachharomyces cerevisae	Living culture	TiCl4	Oval (10–12 nm), mesoporous	[67]
TiO2	Sachharomyces cerevisae	Living culture	TiCl3	Spherical (average size of 6.7 nm)	[68]
TiO2	Tricoderma citrinoviride	Mycelial extract	Ti{OCH(CH3)2}4	Irregular, triangular, pentagonal, spherical, rod-shaped (10–400 nm)	[69]
TiO2	Trichoderma viride	Culture liquid	TiO(OH)2	Spherical (60–86.67 nm)	[70]

).

The ability to synthesize TiO₂ NPs was found in various Aspergillus species. Spherical and oval 62–74-nm TiO₂ NPs with antibacterial properties were fabricated with A. flavus bio-mass [55]. TiO₂ NPs of 12–15 nm synthesized with an A. flavus mycelial extract demonstrated a strong growth-enhancing effect on mung beans and thus can be used as a plant nutrient fertilizer [56]. TiO₂ nanospheres (73.58–106.9 nm) generated with an A. niger extract were found a potent mosquito larvicidal agent [57]. TiO₂ NPs produced with an Aspergillus tubingensis mycelial extract were cubic and pentameric, with a size of 1.5–30 nm [58].

Bansal et al. showed that spherical titania particles (6–13 nm) can be produced with F. oxysporum bio-mass and K₂TiF₆ as a precursor [61]. Al-Timini and Sermon showed that NPs can be synthesized on the surfaces of Portobello mushroom spores [54]. Using this approach, they prepared TiO_x, Ag–TiO_x, and Au–TiO_x NPs. Nanohybrids of these NPs with mushroom spores showed antibacterial and/or antifungal activity.

Rehman et al. fabricated irregularly shaped TiO₂ NPs (80–120 nm) with Fomes fomentarius [59] and Fomitopsis pinicola [60] fruit body extracts. Both F. pinicola and F. fomentarius–mediated NPs were active against Gram-positive and Gram-negative bacteria and had an anticancer effect. Protein-capped NPs of TiO₂ (5–28 nm) were formed directly from micron-sized TiO₂ powder (150–250 nm) by incubation with Humicola sp. mycelium at 50°C [62]. Fungal processing of these large-sized particles bioleached them and transformed them into NPs of a different phase and shape (brookite (circular-shaped)), as compared with the parent material (anatase (disc-shaped powder)).

Manimaran et al. synthesized TiO₂ NPs with Hypsizygus ulmarius, Pleurotus djamor, and Pleurotus sajor caju fruit body extracts [63,64,65]. The NPs fabricated with H. ulmarius expressed a broad-spectrum antimicrobial effect against pathogenic bacteria and anticancer activity [63]. Pleurotus-derived TiO₂ NPs possessed mosquito larvicidal, antibacterial, and anticancer activities [64,65].

Small mesoporous TiO₂ NPs (10–12 nm) with outstanding photocatalytic performance were formed when Sachharomyces cerevisae yeast cells were cultivated with TiCl₄ [67]. By incubating an S. cerevisae culture with TiO(OH)₂, nanospheres with an average size of 12.57 nm were fabricated [66]. In another study, baker’s yeast was incubated with TiCl₃ to produce anatase TiO₂ nanospheres (average size 6.7 nm) [68]. These mycogenic NPs had prominent antibacterial and antifungal properties and were highly photocatalytic in comparison to commercially available 21-nm TiO₂ NPs.

TiO₂ NPs obtained with Trichoderma viride culture liquid were spherical, with a size of 60–86.67 nm [70]. Their larvicidal, antifeedant and pupicidal activities against the cultivated crop pest Helicoverpa armigera can help in eco-friendly pest management. With a Tricoderma citrinoviride mycelial extract, irregular, triangular, pentagonal, spherical, and rod-shaped TiO₂ NPs were synthesized, whose sizes ranged between 10 and 400 nm [69]. They showed excellent antioxidant potential and antibacterial activity against extremely drug-resistant Pseudomonas aeruginosa clinical isolates.

2.4. Myco-Synthesis of Zinc Oxide Nanoparticles

Zinc oxide (ZnO) NPs have caught the attention of researchers owing to their extensive biological properties, including antibacterial, antifungal, anticancer, anti-inflammatory, antidiabetic, antioxidant, antiviral, wound healing, and cardioprotective activity [71,72]. Their exceptional optical, electrical, and physiochemical properties make ZnO NPs an excellent option for electronics, optoelectronics, bioimaging, biosensors, drug and gene delivery [72,73]. To date, these NPs have been the most commonly studied of all mycogenic oxide NPs (

Table 4. Myco-synthesis of zinc oxide nanoparticles.

NP	Species	Source	Precursors	Shape and Size	Reference
ZnO	Acremonium potronii	Mycelial extract	Zn(CH3CO2)2	Spherical (13–15 nm)	[74]
ZnO	Agarius bisporus	Fruit body extract	Zn(CH3CO2)2	Spherical (average size of 14.48 nm)	[75]
ZnO	Aspergillus aeneus	Mycelial extract	Zn(CH3CO2)2	Spherical (100–140 nm)	[76]
ZnO	Aspergillus fumigatus	Culture liquid	ZnSO4	Spherical (60–80 nm)	[77]
ZnO	Aspergillus fumigatus	Mycelial extract	Zn(NO3)2	Oblate spherical and hexagonal (1.2–6.8 nm)	[78]
ZnO	Aspergillus niger	Mycelial extract	Zn(CH3CO2)2	Nanorods (8–38 nm)	[79]
ZnO	Aspergillus niger	Crushed fungal powder	ZnCl2	Hexagonal (average size of 66 nm)	[80]
ZnO	Aspergillus terreus	Culture liquid	ZnSO4	Spherical (28–63 nm)	[81]
ZnO	Aspergillus terreus	Mycelial extract	Zn(CH3CO2)2	Spherical (10–45 nm)	[82]
ZnO	Aspergillus terreus	Culture liquid	ZnC4H6O4	Almost spherical	[28,29]
ZnO	Cochliobolus geniculatus	Mycelial extract	Zn(CH3CO2)2	Quasi-spherical (2–6 nm)	[83]
ZnO	Cordyceps militaris	Fruit body extract	Zn(CH3CO2)2	Spherical, irregular (average size of 1.83 nm)	[84]
ZnO	Daedalea sp.	Fruit body extract	Zn(CH3CO2)2	Irregular (average size of 14.58 nm)	[85]
ZnO	Fusarium keratoplasticum	Mycelial extract	Zn(CH3CO2)2	Hexagonal (10–42 nm)	[79]
ZnO	Lentinula edodes	Fruit body extract	Zn(NO3)2	Cubic, hexagonal (average size of 50 nm)	[86]
ZnO	Periconium sp.	Mycelial extract	Zn(NO3)2	Quasi-spherical (16–78 nm)	[87]
ZnO	Pichia kudriavzevii	Fungal extract	Zn(CH3CO2)2	Hexagonal (average size of 32 nm)	[88]
ZnO	Pleurotus djamor	Fruit body extract	Zn(NO3)2	Nanorods, clusters (average size of 70–80 nm)	[64]
ZnO	Pleurotus florida	Bio-mass	ZnCl2	Semi-spherical (21.27–118.36 nm)	[36]
			ZnSO4	Semi-spherical (9.36–58.13 nm)
ZnO	Pleurotus floridanus	Culture liquid	Zn(NO3)2	Spherical (average size of 34.98 nm)	[89]
ZnO	Pleurotus ostreatus	Fruit body extract	Zn(NO3)2	Spherical (average size of 7.50 nm)	[90]
ZnO	Trichoderma harzianum	Mycelial extract	ZnSO4	Fan- and bouquet-like structures (27–40 nm in width, 134–200 nm in length)	[33]
ZnO	Trichoderma harzianum	Mycelial extract	Zn(CH3CO2)2	Spherical (average size of 30.34 nm)	[91]
ZnO	Trichoderma viride	Culture liquid	Zn(CH3CO2)2	Hexagonal (average size of 63.3 nm)	[92]

). Mycogenic ZnO NPs are mostly spherical or hexagonal.

The formation of ZnO nanospheres with sizes ranging between 13 and 15 nm was studied by using an Acremonium potronii mycelial extract [74]. The obtained ZnO NPs showed high photocatalytic activity for the degradation of methylene blue dye. ZnO nanospheres with an average size of 14.48 nm were fabricated with an aqueous extract of Agarius bisporus as a reducing agent [75]. These NPs were effective inhibitors of microbially influenced corrosion.

The correlation between the zinc tolerance of soil fungi and their potential for the synthesis of ZnO NPs was examined with 19 fungal isolates from the rhizo-spheric soil of plants naturally growing at a zinc mine area [76]. The Aspergillus aeneus isolate had a high zinc tolerance and potential for the extracellular synthesis of ZnO NPs. The result was the synthesis of spherical NPs (100–140 nm) coated with proteins, which served as stabilizers.

Spherical 60–80-nm ZnO NPs synthesized with Aspergillus fumigatus culture liquid were an effective antimicrobial agent against Gram-negative and Gram-positive bacteria [77]. An A. fumigatus mycelial extract induced the formation of oblate spherical and hexagonal ZnO NPs (1.2–6.8 nm) with plant-growth-promoting properties [78]. Hexagonal ZnO NPs with an average size of 66 nm were synthesized by using crushed powder of A. niger [80]. Protein-capped ZnO nanospheres with a particle size of about 10–45 nm, possessing antibacterial activity, were obtained with an A. terreus mycelial extract [82]. Incubation of A. terreus culture liquid with ZnSO₄ yielded spherical ZnO NPs (28–63 nm) [81]. ZnO NPs with antioxidant and antimicrobial activities were also synthesized with the culture liquid of A. terreus and with ZnC₄H₆O₄ as a precursor [28,29].

Aqueous mycelial extracts of two fungi, A. niger and Fusarium keratoplasticum, were used to prepare ZnO NPs of different shapes [79]. A. niger synthesized ZnO nanorods (8–38 nm), and F. keratoplasticum synthesized hexagonal NPs (10–42 nm). The shape of the NPs greatly affected their multifunctional properties. Nanorods showed an enhanced antibacterial activity against pathogenic bacteria and a greater UV-protection index, as compared with hexagonal ZnO NPs. Treatment of textile fabrics with a safe dose of green ZnO NPs was potentially active against pathogenic bacteria and improved UV protection, as compared with untreated fabrics.

ZnO NPs obtained with an extract from the zinc-tolerant endophytic fungus Cochliobolus geniculatus were polydisperse, non-agglomerated quasi-spherical particles with a narrow range distribution (2–6 nm) [83]. Extracellular proteins involved in the synthesis of ZnO NPs and their capping were also characterized.

A fruit body extract from the medicinal mushroom Cordyceps militaris mediated the fabrication of ZnO NPs with an average size of 1.83 nm and with high antimicrobial, antidiabetic, and antioxidant potential [84]. ZnO NPs were also synthesized with a Daedalea sp. extract [85]. The NPs were irregularly shaped, had an average size of 14.58 nm, and showed a strong antibacterial and antifungal effect. A Lentinula edodes extract was used as a reducing agent involved in the myco-synthesis of ZnO NPs, coated with chitosan, which functions as a stabilizer [86]. The NPs were cubic and hexagonal and had dye-degrading and antibacterial properties.

Quasi-spherical ZnO NPs (16–78 nm) synthesized with a Periconium sp. mycelial extract showed good antioxidant properties, as well as excellent antimicrobial effect against fungi, Gram-positive and Gram-negative bacteria [87]. The ability of the yeast Pichia kudriavzevii to synthesize ZnO NPs was explored with a fungal extract [88]. The resulting NPs were found to have a hexagonal wurtzite structure with an average crystallite size of ~10–61 nm, and displayed antioxidant and antibacterial properties. The time of the reaction was found to play a critical part in the size, shape, and distribution of NPs. The ability to produce ZnO NPs was also reported for Pichia fermentans culture liquid [93].

ZnO NPs synthesized with a P. djamor fruit body extract were rod- and cluster-shaped with an average size of 70–80 nm and showed a wide range of biological activities, including larvicidal, antibacterial, antioxidant, and anticancer properties [64]. Semispherical ZnO NPs fabricated with P. florida bio-mass varied in size, depending on the precursors [36]. With ZnCl₂, their size was 21.27–118.36 nm, and with ZnSO₄, it was 9.36–58.13 nm. In another work, the culture liquid of Pleurotus floridanus was used for the synthesis of ZnO nanospheres, and the process parameters were optimized [89]. A Pleurotus ostreatus fruit body extract was used to synthesize small (average size of 7.50 nm), spherical, highly stable, agglomerated ZnO NPs with antibacterial and anticancer properties [90].

ZnO NPs with an unusual morphology (fan- and bouquetlike structures 27–40 nm in width and 134–200 nm in length) were fabricated with a T. harzianum mycelial extract [33]. In another study, ZnO nanospheres (average size of 30.34 nm) with antioxidant and antibacterial properties were produced with an extract from T. harzianum mycelium [91]. T. viride culture liquid was also used to synthesize ZnO NPs [92]. These NPs were hexagonal, had an average particle size of about 63.3 nm, and possessed dose-dependent antioxidant activity and appreciable antimicrobial effect against multidrug-resistant microorganisms.

2.5. Myco-Synthesis of Nanoparticles of Other Elements

Fungal cultures can form oxides of many elements other than copper, iron, titanium, and zinc. These include magnesium, manganese, cobalt, nickel, zirconium, selenium, tellurium, silicon, cerium, silver, aluminium, bismuth, antimony, gadolinium, and ruthenium (

Table 5. Myco-synthesis of nanoparticles of other elements.

NP	Species	Source	Precursors	Shape and Size	Reference
Al2O3	Colletotrichum sp.	Mycelial extract	AlCl3	Spherical (average size of 30 nm)	[94]
AgO	Aspergillus terreus	Culture liquid	AgNO3	Irregular spherical (60–100 nm)	[95]
Bi2O3	Fusarium oxysporum	Bio-mass	Bi(NO3)3	Quasi-spherical (5–8 nm)	[96]
CeO2	Aspergillus niger	Culture liquid	CeCl3	Spherical (5–20 nm)	[97]
CeO2	Aspergillus terreus	Mycelial extract	Ce(NO3)3	Spherical (average size of 28.5 nm)	[98]
CeO2	Fusarium solani	Culture liquid	CeCl3	Spherical (20–30 nm)	[99]
CeO2	Humicola sp.	Bio-mass	Ce(NO3)3	Spherical (12–20 nm)	[100]
CeO2	Talaromyces prupureogenus	Mycelial extract	Ce(NO3)3	Nano-sponges (average size of 21.4 nm)	[98]
Co3O4	Aspergillus brasiliensis	Mycelial extract	CoSO4	Quasi-spherical (20–27 nm)	[101]
Co3O4	Aspergillus nidulans	Bio-mass	Co(C5H7O2)2	Spherical (average size of 20.29 nm)	[102]
Co3O4	Aspergillus terreus	Culture liquid	CoSO4	Spherical	[28,29]
Gd2O3	Humicola sp.	Bio-mass	GdCl3	Quasi-spherical (3–8 nm)	[103]
MgO	Agaricus bisporus	Fruit body extract	Mg(CH3COO)2	29.6–38.6 nm	[104]
MgO	Aspergillus niger	Culture liquid	MgCl2	Spherical (40–95 nm)	[105]
MgO	Aspergillus tubingensis	Mycelial extract	Mg(NO3)2	Spherical (average size of 5.8 nm)	[106]
MgO	Trichoderma viride	Culture liquid	MgCl2	45.12–95.37 nm	[107]
MnxOy	Cladosporium halotolerans	Living culture	MnCl2	Needle-like (2–6 nm in diameter, 0.1–1 μm in length)	[108]
Mn5O8	Fusarium oxysporum	Bio-mass	(CH3CO2)2Mn·	Quasi-spherical (8–13 nm)	[109]
NiO	Aspergillus aculeatus	Dead bio-mass	NiCl2	Spherical (average size of 5.89 nm)	[110]
NiO	Aspergillus terreus	Culture liquid	NiSO4	Spherical	[28,29]
NiO	Hypocrea lixii	Dead bio-mass	NiCl2	Average size of 3.8 nm for extracellular and 1.25 nm for intracellular NPs	[111]
RuO2	Fusarium oxysporum	Bio-mass	RuCl3	Spherical (2–5 nm)	[112]
Sb2O3	Saccharomyces cerevisiae	Fungal culture	SbCl3	Spherical (2–10 nm)	[113]
SeO2	Trichoderma harzianum	Living culture	Na2SeO3	–	[114]
SiO2	Fusarium oxysporum	Bio-mass	K2SiF6	Quasi-spherical (5–15 nm)	[61]
SiO2	Fusarium oxysporum	Bio-mass	Amorphous silica present in rice husk	Quasi-spherical (2–6 nm)	[115]
SiO2	Saccharomyces cervisiae	Living culture	Sodium silicate	Spherical (40–70 nm)	[116]
TeO2	Mortierella humilis	Living culture	Na2TeO3	–	[114]
TeO2	Trichoderma harzianum	Living culture	Na2TeO3	–	[114]
ZrO2	Fusarium oxysporum	Bio-mass	K2ZrF6	Quasi-spherical (3–11 nm)	[117]
ZrO2	Fusarium solani	Culture liquid	zirconyl nitrate	Spherical (40–50 nm)	[118]
ZrO2	Penicillium aculeatum	Culture liquid	ZrCl4	Spherical (average size of 39.32 nm)	[119]
ZrO2	Penicillium notatum	Culture liquid	ZrCl4	Spherical (average size of 62.27 nm)	[119]
ZrO2	Penicillium purpurogenome	Culture liquid	ZrCl4	Spherical (average size of 53.60 nm)	[119]

). Many of these elements remain barely explored in terms of NP myco-synthesis, and their formation by fungal cultures has so far been described only in a few reports.

Several research groups were able to prepare mycogenic NPs of cerium oxide. CeO₂ nanospheres (5–20 nm) have been successfully obtained with an A. niger culture liquid filtrate [97]. The NPs showed a high antibacterial activity against pathogenic bacteria and larvicidal and pupicidal activity against mosquito vectors. Spherical 20–30-nm CeO₂ NPs obtained with F. solani culture liquid showed a good antibacterial and antibiofilm activity against Psedomonas aeriginosa, Klebsiella pneumoniae, Escherichia coli, and Staphylococcus aureus [99].

Electrochemical analysis shows that mycogenic NPs can be used in applications such as sensors, batteries, and supercapacitors. The bio-mass of the fungus Humicola sp. was able to extracellularly form highly stable, water-dispersible, and highly fluorescent CeO₂ NPs [100]. These NPs were spherical, were 12–20 nm in diameter, and were naturally capped by proteins secreted by the fungus. Komal et al. synthesized morphologically different CeO₂ NPs with mycelial extracts from two fungi, A. terreus and Talaromyces prupureogenus [98]. Pure CeO₂ NPs synthesized with A. terreus were spherical, with an average size of 28.5 nm. CeO₂ NPs formed by T. pupureogenus had a unique nano-sponge morphology and an average size of 21.4 nm. The nano-sponges were more active against Candida albicans than were spherical CeO₂ NPs.

Cobalt oxide NPs have so far been synthesized with several Aspergillus species. A cell-free mycelial extract of Aspergillus brasiliensis was used to make quasi-spherical monodispersed Co₃O₄ NPs of 20–27-nm [101]. The NPs have excellent magnetic properties and show good antimicrobial activity against pathogenic microorganisms. Four fungi were tested by Vijayanandan and colleagues to find a fungus suitable for the synthesis of cobalt oxide NPs [102]. Fluorescent Co₃O₄ nanospheres capped with sulfur-bearing proteins were successfully synthesized with Aspergillus nidulans bio-mass. Optimization of the fermentation conditions for the enhanced production of Co₃O₄ and other NPs with A. terreus culture liquid was studied by El-Sayed et al. [29].

Al₂O₃ nano-speres with an average size of 30 nm were synthesized with a Colletotrichum sp. mycelial extract [94]. Al₂O₃ NPs showed a strong antimicrobial activity against food-borne pathogens. Nano-functionalized oil was formulated by combining essential oils from the leaves of Eucalyptus globulus and Citrus medica with NPs. The combination showed higher antimicrobial activity than did NPs and the essential oils tested separately. Moreover, the activity of commercially available antibiotics increased in combination with mycogenic Al₂O₃ NPs.

Irregular silver oxide (AgO) nanospheres of 60–100 nm were synthesized with A. terreus culture liquid [95]. The nanospheres had antimicrobial, antioxidant, and antiangiogenic properties. Quasi-spherical bismuth oxide (Bi₂O₃) NPs of 5–8 nm were fabricated with F. oxysporum bio-mass [96]. Protein-capped, highly stable, and well-dispersed quasi-spherical gadolinium oxide (Gd₂O₃) NPs of 3–8 nm were synthesized extracellularly with Humicola sp. mycelial bio-mass [103]. These NPs were bio-conjugated with the chemically modified anticancer drug taxol, which may make it more efficient in killing tumor/cancer cells.

Recently, an effective method was described for the fungi-mediated production of fluorescent ruthenium oxide (RuO₂) QDs by F. oxysporum bio-mass [112]. The biosynthesis was conducted under ambient pressure at room temperature, which offers advantages over the previously used chemical and physical methods for RuO₂ synthesis, requiring highly elevated temperature and pressure. The QDs were monodisperse, non-flocculating, protein capped, and highly stable even months after synthesis. Biosynthesis of antimony trioxide (Sb₂O₃) NPs mediated by S. cerevisiae was reported by Jha et al. [113].

MgO NPs synthesized with A. niger culture liquid were nanospheres of 40–95 nm [105]. Their antibacterial activity was stronger against Gram-positive bacteria then it was against Gram-negative ones. Small MgO nanospheres with an average size of 5.8 nm were prepared with an A. tubingensis mycelial extract [106]. Larger NPs, of 45.12–95.37 nm, were synthesized with T. viride culture liquid and were found to be an effective antibacterial agent [107]. A white button mushroom extract was used to make MgO NPs with an average size of 29.6–38.6 nm [104]. The researchers showed that 16.5- and 15-nm MgO NPs may promote root development in peanut plants.

Quasi-spherical Mn₅O₈ NPs of 8–13 nm were obtained with F. oxysporum bio-mass [109]. These particles were highly stable, water dispersible, and naturally capped by the fungus-secreted proteins. The Mn-oxidizing fungus Cladosporium halotolerans with a strong ability to remove and oxidize Mn (II) was studied by Wang et al. [108]. The C. halotolerans culture formed particles with a needlelike or wrinkle-like morphology in the cross section, 2–6 nm in diameter, and 0.1–1 μm in length. The obtained nanowires showed excellent Cd (II) adsorption and had potential anti-pollutant application prospects.

NiO NP synthesis with A. terreus culture liquid was optimized for higher NP yield by El-Sayed et al. [29]. The dead bio-mass of the fungus Hypocrea lixii was also successfully used to convert nickel ions into NiO NPs in aqueous solution [111]. H. lixii–mediated NPs were predominantly spherical and were formed extra- and intracellularly. The NPs formed inside the fungal cells were smaller than those produced extracellularly. The average particle sizes were 3.8 nm for extracellular NPs and 1.25 nm for intracellular NPs. The dead bio-mass of Aspergillus aculeatus synthesized spherical NiO NPs in film form [110]. The NPs had a size of about 5.89 nm and were involved in a protein matrix, which probably permitted their organization in film form.

Bansal et al. obtained small quasi-spherical silica NPs with F. oxysporum bio-mass. NPs of 5–15 nm were synthesized with K₂TiF₆ as a precursor [61]. Moreover, F. oxysporum was able to bio-transform naturally occurring amorphous plant bio-silica into crystalline silica and leach out silica extracellularly as 2–6 nm NPs [115]. Spherical silica NPs (40–70 nm) were fabricated extracellularly by an S. cervisiae culture [116].

Liang et al. studied the formation of Se- and Te-containing NPs by several fungal species during growth on Se- and Te-containing media [114]. Besides the formation of elementary selenium, selenium oxide was also found after T. harzianum had been grown with selenite. Tellurium oxide was detected in the particles generated by T. harzianum and Mortierella humilis grown with tellurite.

Zirconium oxide (ZrO₂) nanospheres (40–50 nm in diameter) were fabricated with F. solani culture liquid as a reducing and stabilization agent [118]. F. oxysporum bio-mass formed quasi-spherical ZrO₂ NPs (3–11 nm) [117]. Ghomi et al. studied culture liquids of three Penicillium species (Penicillium aculeatum, Penicillium notatum, Penicillium purpurogenome) and reported their ability to form ZrO₂ NPs [119]. All the species studied formed spherical NPs with a size below 100 nm. Penicillium-mediated ZrO₂ NPs showed considerable antibacterial potential against Gram-negative bacteria.

3. Myco-Synthesis of Chalcogenide Nanoparticles

Chalcogens are chemical elements from group 16 of the periodic table: oxygen, sulfur, selenium, tellurium, polonium, and livemorioum. Oxygen is often treated separately from the other group 16 elements, or even excluded from the scope of the term “chalcogen”, owing to its very different chemical behavior from the other chalcogens [120]. Chemical compounds consisting of at least one chalcogen anion and at least one more electropositive element are called chalcogenides. The three most important groups of chalcogenides are sulfides, selenides, and tellurides. In recent years, fungi-assisted synthesis of chalcogenide NPs and nanomaterials has become of interest.

3.1. Myco-Synthesis of Sulfide Nanoparticles

Fungi-mediated synthesized sulfide NPs are the most commonly studied of all chalcogenides. One of the most important types of semiconductor nanomaterials with a wide band gap and with stability than that of the other chalcogenide NPs, sulfide NPs are more suitable for industrial applications, including high temperature operations, high voltage optoelectronic devices, and as high efficiency electric energy transformers and generators [13].

According to the data so far, fungal cultures can synthesize cadmium, zinc, and lead sulfide NPs. Several researchers have also found that some fungi can produce gold, silver, and copper sulfide NPs (

Table 6. Myco-synthesis of sulfide nanoparticles.

NP	Species	Source	Precursors	Shape and Size	Reference
α-Ag2S	Humicola sp.	Mycelial bio-mass	AgNO3, Na2SO3	Spherical (15–40 nm)	[121]
Au2S	Humicola sp.	Mycelial bio-mass	HAuCl4, Na2SO3	Spherical (20–30 nm)	[122]
CdS	Aspergillus niger	Mycelial bio-mass	CdCl2, Na2S	Spherical (2.7–7.5 nm)	[123]
CdS	Candida glabrata	Living culture	Cd(NO3)2	–	[124]
CdS	Fusarium oxysporum	Living culture	CdSO4	5–20 nm	[125]
CdS	Fusarium oxysporum	Mycelial bio-mass	Cd(NO3)2, sulfur waste	Spherical (average size of 6 nm)	[126]
CdS	Fusarium sp.	Mycelial bio-mass	CdSO4	Spherical (80–120 nm)	[127]
CdS	Phanerochaete chrysosporium	Living culture	Cd(NO3)2	Average size of 2.56 nm	[128]
CdS	Pleurotus ostreatus	Mycelial bio-mass	CdSO4, Na2S	Spherical (4–5 nm)	[129]
CdS	Rhizopus stolonifer	Mycelial bio-mass	CdCl2, ZnS	Average size of 8.8 nm	[130]
CdS	Saccharomyces cerevisiae	Living culture	CdS solution	Spherical (average size of 3.57 nm)	[131]
CdS	Saccharomyces cerevisiae	Bio-mass	CdCl2, Na2S	Spherical (average size of 2 nm)	[132]
CdS	Schizosaccharo-myces pombe	Living culture	CdSO4	Average size of 1.8 nm	[133]
CdS	Schizosaccharo-myces pombe	Living culture	CdSO4	1–1.5 nm	[134]
CdS	Schizosaccharo-myces pombe	Living culture	Cd(NO3)2	–	[124]
CdS	Termitomyces heimii	Fruit body extract	Cd(NO3)2, Na2S	Spherical (3–5 nm)	[135]
CdS	Trametes versicolor	Living culture	Cd(NO3)2	Spherical (average size of 6 nm)	[136]
CdS	Trichoderma harzianum	Mycelial bio-mass	CdCl2, Na2S	Spherical (3–8 nm)	[137]
CdS	Trichosporon jirovecii	Living culture	CdCl2	Spherical (6–15 nm)	[138]
CuS	Fusarium oxysporum	Mycelial bio-mass	CuSO4	Spherical (2–5 nm)	[139]
CuS	Fusarium oxysporum	Mycelial bio-mass	Copper mine wastewaters	10–40 nm	[140]
PbS	Aspergillus flavus	Living culture	Pb(C2H3O2)2, Na2S	35–100 nm	[141]
PbS	Rhodosporidium diobovatum	Bio-mass	Pb(NO3)2	Spherical (2–5 nm)	[142]
PbS	Saccharomyces cerevisiae	Living culture	Pb(C2H3O2)2, Na2S	Spherical (0.667–6.95 nm)	[143]
PbS	Torulopsis sp.	Living culture	Pb(NO3)2	2–5 nm	[144]
ZnS	Agaricus bisporus	Fruit body extract	ZnCl2, Na2S	Almost spherical (2.1–3.5 nm)	[145]
ZnS	Aspergillus flavus	Mycelial bio-mass	ZnSO4	Spherical (average size of 18 nm)	[146,147]
ZnS:Gd	Aspergillus flavus	Mycelial bio-mass	ZnSO4, Gd(NO3)2	Spherical (10–18 nm)	[148]
ZnS	Aspergillus sp.	Mycelial bio-mass	ZnSO4	Spherical (average size of 11.08 nm)	[149]
ZnS	Fusarium oxysporum	Mycelial bio-mass	ZnSO4	Spherical (average size of 42 nm)	[150]
ZnS	Penicillium sp.	Mycelial bio-mass	ZnSO4	Spherical (average size of 6.3 nm)	[151]
ZnS	Pleurotus ostreatu	Fruit body extract	ZnCl2, Na2S	Almost spherical (2.1–3.5 nm)	[152]
ZnS	Saccharomyces cerevisiae	Bio-mass	ZnSO4	Spherical (30–40 nm)	[153]

).

Among mycogenic sulfide NPs, the best studied are cadmium sulfide (CdS) NPs. These were first obtained with the use of fungal cultures in the 1980s, when Dameron and colleagues synthesized quantum CdS nano-crystallites with the yeasts Candida glabrata and Schizosaccharomyces pombe [154]. Short chelating peptides of general structure (γ-Glu-Cys)_n-Gly control the nucleation and growth of CdS crystallites to peptide-capped intracellular particles of diameter 20 Å (2 nm). Both yeasts also produce larger, extracellular CdS NPs with an uncharacterized coating, 29 Å (2.9 nm) in diameter. Later, the S. pombe–mediated synthesis of CdS NPs was studied by Williams et al. [133]. It was found that intracellular CdS quantum semiconductor crystallites approximately 1.8 nm in diameter can be selectively released from S. pombe cells by freezing–thawing. S. pombe and C. glabrata also formed CdS NPs in their cytoplasm when yeasts were grown in a fed-batch process at high Cd concentrations [124].

A. niger bio-mass challenged with precursors produced highly stable poly-dispersed CdS nanospheres with a size ranging from 2.7 to 7.5 nm; these particles were found to have antimicrobial and anticancer abilities [123]. The bio-mass of F. oxysporum produced extracellular biocompatible CdS QDs from sulfur waste and Cd(NO₃)₂ [126]. These QDs were circular with a diameter of about 6 nm and had a wurtzite crystalline structure. F. oxysporum incubated with CdSO₄ formed CdS NPs in the size range 5–20 nm [125]. Fusarium sp. bio-mass, after being exposed to a CdSO₄ solution, formed spherical CdS NPs with an average particle size of 80 to 120 nm and agglomerates with a size of 350 to 390 nm [127]. CdS QDs synthesized by the fungus Phanerochaete chrysosporium had an average size of 2.56 nm [128]. The synthesis of cysteine and proteins was found to play an important part in the formation and stabilization of CdS QDs. CdS QDs with an average size of 8.8 nm formed by Rhizopus stolonifer mycelial bio-mass [130]. Luminescent CdS QDs synthesized with P. ostreatus mycelium were spherical, were predominantly 4 to 5 nm in size [129], and had anticancer properties [155].

S. cerevisiae–mediated synthesis of CdS NPs was reported by Prasad and Jha [131]. The NPs were almost spherical, with an average size of 3.57 nm. Another study described the production of CdS nanospheres (average size of 2 nm) with S. cerevisiae bio-mass [132]. Cds NPs were formed intracellularly by an S. pombe strain [134]. The NPs had a wurtzite (Cd₁₆S₂₀)-type structure and were mostly in the size range 1–1.5 nm. By using S. pombe–mediated CdS NPs, a polymer/nanoparticle diode with a low operating voltage and a high forward current was fabricated. Wurtzite CdS NPs of 3–5 nm were synthesized with a Termitomyces heimii mushroom extract [135]. The volume of extract used for the synthesis affected the particle size. A Trametes versicolor culture synthesized spherical extracellular CdS QDs with an average size of 6 nm [136]. T. harzianum bio-mass formed spherical CdS NPs (3–8 nm) with photocatalytic activity, which was determined upon degradation of methylene blue dye [137]. CdS nanospheres with a size range of about 6–15 nm were formed with the yeast Trichosporon jirovecii [138].

Silver sulfide (α-Ag₂S) NPs were produced with Humicola sp. mycelium [121]. These NPs were nanospheres of 15–40 nm and had strong antimicrobial, anticancer, and anti-leishmania activities.

Gold sulfide (Au₂S) nanospheres with a size of 20–30 nm were synthesized with Humicola sp mycelium [122]. The prepared particles were shown to be nontoxic to humans and, therefore, can be proposed for use in leishmania treatment, nano-diagnostics, and drug carrier applications.

Copper sulfide (CuS) NPs were synthesized with F. oxysporum mycelium and with CuSO₄ as a precursor [139]. The formed spherical particles with a size of 2–5 nm were enclosed in spherical peptide shells about 20 nm in diameter. Later, the same authors obtained CuS NPs by incubating F. oxysporum mycelium with copper mine wastewater [140]. The results showed that the produced NPs had a covelite composition and that their size was about 10–40 nm.

Lead sulfide (PbS) NPs with quantum semiconductor properties were first synthesized with Torulopsis sp. [144]. Seshadri et al. reported the intracellular synthesis of stable PbS NPs by the marine yeast Rhodosporidium diobovatum [142]. The NPs, of 2–5 nm, were spherical and well dispersed. S. cerevisiae produced PbS nanospheres 0.667–6.95 nm in size [143]. Synthesis of PbS NPs with A. flavus yielded 35–100-nm particles that had the potential for the detection of arsenic in aqueous solution [141].

ZnS NPs was synthesized with an extract of the edible mushroom A. bisporus [145]. The agglomeration and size of the NPs decreased along with increasing the A. bisporus extract volume used for the myco-synthesis. With a high extract volume, the NPs were almost spherical and the average particle size varied from 2.1 to 3.5 nm. The same authors also synthesized ZnS NPs with a P. ostreatus fruit body extract [152]. In that case, the agglomeration of the particles and their size also decreased as the amount of the mushroom extract was increased. With the use of a P. ostreatus extract, a large quantity of spherical NPs of 4.04 to 2.30 nm was formed. The authors attribute the smaller size of the ZnS NPs obtained with A. bisporus to the higher protein content of this mushroom’s fruit bodies [145].

Spherical ZnS QDs (average size of 18 nm) were obtained with A. flavus bio-mass [146,147]. Later, the same researchers utilized A. flavus bio-mass to synthesize gadolinium-doped ZnS (ZnS:Gd) [148]. The fluorescence intensity of the biogenic ZnS:Gd NPs increased in comparison to ZnS NPs, which makes them a reliable fluorescent sensing tool. Jacob and colleagues studied ZnS QD production with bio-mass of two micro-mycetes, Aspergillus sp. and Penicillium sp. In both cases, the mycogenic NPs were spherical and their average size was 11.08 nm for Aspergillus [149] and 6.3 nm for Penicillium [151]. Aspergillus-mediated ZnS QDs showed excellent antibacterial and dye-degrading activities. The QDs synthesized by Penicillium sp. were effective in the photodegradation of methylene blue dye. F. oxysporum mycelial bio-mass was used to synthesize spherical ZnS NPs with an mean size of 42 nm [150]. S. cerevisiae bio-mass formed 30–40-nm ZnS nanospheres [153].

3.2. Myco-Synthesis of Selenide Nanoparticles

Selenides are another important class of chalcogenide semiconductors. Their potential applications include photocatalysis, bioimaging and biolabeling, and nanomedicine [156]. Mycogenic selenide NPs obtained by bio-nanotechnologists so far include cadmium, lead, silver, gold, indium, and neodymium selenides. To date, they have been obtained mostly with fungal bio-mass or living cultures (

Table 7. Myco-synthesis of selenide nanoparticles.

NP	Species	Source	Precursors	Shape and Size	Reference
Ag2Se	Saccharomyces cerevisiae	Living culture	AgNO3, Na2SeO3	Average size of 3.9 nm	[157]
AuSe	Fusarium oxysporum	Mycelial bio-mass	HAuCl4, SeCl4	Spherical (average size of 52 nm)	[158]
CdSe	Candida utilis	Living culture	CdCl2, Na2SeO3	Average size of 4.38 nm	[159]
CdSe	Fusarium oxysporum	Mycelial bio-mass	CdCl2, SeCl4	Average size of 11 nm	[160]
CdSe	Helminthosporum solani	Mycelial bio-mass	CdCl2, SeCl4	Spherical, cubic (average size of 5.5 nm)	[161]
CdSe	Rhodotorula mucilaginosa	Bio-mass	CdCl2, Na2SeO3	Average size of 3.2 nm	[162]
CdSe	Saccharomyces cerevisiae	Living culture	CdCl2, Na2SeO3	15–20 nm	[163]
CdSe	Saccharomyces cerevisiae	Living culture	CdCl2, Na2SeO3	Average size of 2.8 nm	[164]
CdSe	Saccharomyces cerevisiae	Bio-mass	CdCl2, Na2SeO3	–	[165]
InSe	Aspergillus niger	Living culture	InCl3, Na2SeO3	<10 nm	[166]
Nd2Se3	Fusarium oxysporum	Fungal nitrate-dependent reductase	NdCl2, SeCl4	Spherical (average size of 18 nm)	[167]
PbSe	Aspergillus terreus	–	–	Nanorods (average size of 59 nm)	[168]
PbSe	Trichoderma sp.	Mycelial bio-mass	Pb(NO3)2, SeO2	Cubic (10–30 nm)	[169]

).

The most widely studied mycogenic selenide NPs are cadmium selenide (CdSe) NPs, and their synthesis with yeasts is the best studied so far [159,162,163,164,165,170]. Various conditions for CdSe QD synthesis with S. cerevisiae were investigated and optimized to obtain particles with a controllable size and with tunable fluorescence emission [163]. Brooks and Lefebvre examined the ability of S. cerevisiae sequentially treated with sodium selenite and cadmium chloride to synthesize CdSe QDs in the cytoplasm [164]. They optimized biosynthesis conditions for the highest yield of QDs, and through the optimized method they obtained fluorescent QDs with an average particle diameter of 2.8 nm. Shao et al. studied Se precursors and Se metabolic flux in the synthesis of CdSe QDs in S. cerevisiae and improved their ability to synthesize CdSe QDs through gene modification [165]. They identified selenocysteine as the primary Se precursor in the intracellular biosynthesis of CdSe QDs. Further studies showed that the seleno-methionine-to-selenocysteine pathway regulates CdSe QD biosynthesis. Seleno-methionine synthesis was enhanced by overexpression of the MET6 gene, and the yield of CdSe QDs in the engineered cells was increased.

CdSe QDs (average size of 4.38 nm) were also fabricated in vivo with Candida utilis [159]. Higher Cd and lower Se contents favored the formation of QDs with a higher fluorescence intensity and better stability, implying a possibility of tuning the fluorescence properties of these QDs. Candida-mediated CdSe QDs were directly used in live-cell imaging without further surface modification. Cao et al. synthesized CdSe QDs with bio-mass of the yeast Rhodotorula mucilaginosa [162]. The synthesis was regulated by changing the concentration of precursors and the pH of the medium, and it was found that the concentration of cadmium ions, rather than that of selenium ions, determined the synthesis of CdSe QDs. The synthesized CdSe QDs had a narrow size distribution (3.2 ± 0.4 nm) and great photocatalytic activity toward malachite green dye under ultraviolet and visible light.

Besides various yeasts, other micro-mycetes are also able to form CdSe QDs. F. oxysporum bio-mass was used for the synthesis of highly stable semiconductor CdSe QDs (average size of about 11 nm) with a broad fluorescent spectrum [160]. Helminthosporum solani mycelial bio-mass induced the synthesis of small monodisperse luminescent CdSe QDs with a mean size of 5.5 nm [161]. Most of these NPs were spherical, and a few cubelike particles were present.

Ag₂Se QDs with a uniform size of 3.9 nm were obtained with living S. cerevisiae yeast [157]. The authors showed that selenocysteine was the primary Se precursor, and the ability to synthesize Ag₂Se QDs was improved by the construction of engineering strains. Ag₂Se synthesized with S. cerevisiae were weakly toxic and could be used for in vivo imaging.

AuSe nanospheres with an average particle size of 52 nm were synthesized by incubating F. oxysporum mycelium with SeCl₄ and HAuCl₄ [158]. First, SeCl₄ was reduced into Se NPs, and then these NPs were reacted with HAuCl₄ and formed AuSe NPs. In the absence of an Se intermediate, HAuCl₄ was reduced to Au NPs by fungal biomolecules. AuSe NPs effectively inhibited conidiophores, conidiation, and sporulation in the fungus A. niger.

Sinharoy and Lens studied the simultaneous removal of indium, selenium, and tellurium by A. niger from media by using different precursor concentrations [166]. Characterization of the fungal bio-mass showed accumulation mostly of elementary Se NPs within mycelial pellets, and, in addition, the formation of indium selenide (InSe) during their simultaneous removal. The NPs were <10 nm in size. Biomimetic fabrication of neodymium selenide (Nd₂Se₃) NPs was conducted with a nitrate-dependent reductase from the fungus F. oxysporum as a reducing agent and with a synthetic peptide as a capping molecule [167]. Nd₂Se₃ NPs were spherical, with an average size of 18 nm.

Fluorescent, semiconductor lead selenide (PbSe) quantum rods were synthesized with the Pb- and Se-tolerant marine fungus A. terreus [168]. Semiconductor PbSe NPs were also obtained with Trichoderma sp. bio-mass [169]. The optimal ratio between precursors was 1:1 mM SeO₂:Pb(NO₃)₂. The NPs were 10–30-nm cubic face-centered protein-capped particles, which showed a strong antioxidant activity and photocatalytic activity in degrading rhodamine B dye.

3.3. Myco-Synthesis of Telluride Nanoparticles

Yet another group of chalcogenides consists of the tellurides, which also show outstanding properties and potential applications in optical, electronic, thermoelectrical, energy storing, catalytic, magnetic, and biological fields [171,172]. Their antimicrobial and anticancer properties allow them to be used in nanomedicine [173]. The fungal synthesis of NPs of these compounds has been poorly studied and has been described by only a few researchers (

Table 8. Myco-synthesis of telluride nanoparticles.

NP	Species	Source	Precursors	Shape and Size	Reference
CdTe	Fusarium oxysporum	Mycelial bio-mass	CdCl2, TeCl4	Spherical (15–20 nm)	[174]
CdTe	Rhizopus stolonifer	Mycelial bio-mass	CdCl2, TeCl4	QDs (average size of 7.6 nm)	[133]
CdTe	Saccharomyces cerevisiae	Living culture	CdCl2, Na2TeO3	QDs (2.0–3.6 nm)	[175]
InTe	Aspergillus niger	Living culture	InCl3, K2TeO3	<10 nm	[166]

).

The ability to fabricate CdTe NPs has been found in several species of micro-mycetes. Highly fluorescent biocompatible CdTe QDs capped with proteins were synthesized with S. cerevisiae cells [175]. The synthesized QDs, obtained after 8 days of incubation, were well-dispersed particles with a uniform diameter of about 3.6 nm. When the incubation time was shortened to 2 days, the resulting CdTe QDs were smaller (about 2.2 nm). The CdTe QDs obtained with F. oxysporum mycelial bio-mass were also highly fluorescent and were stable and biocompatible [174]. These NPs were spherical, were 15–20 nm in diameter, and showed antibacterial activity against Gram-positive and Gram-negative bacteria. Biocompatible CdTe QDs with an average size of 7.6 nm were also obtained with R. stolonifer [133]. The study of the simultaneous removal of indium, selenium, and tellurium by A. niger from media showed accumulation of elementary Te NPs and indium telluride NPs within mycelial pellets [166].

4. Prospects of Mycogenic Oxide and Chalcogenide Nanoparticles Practical Application

Many researchers have identified a variety of activities in mycogenic oxide and chalcogenide NPs, determining their great potential for further practical employment in biomedicine, optics, agriculture, pollution control, and other fields of application (Figure 1).

One of the most important fields for use of these NPs is biomedicine. As described above, various biomedical activities were found in many oxide and chalcogenide NPs produced with fungi. Antibacterial, antifungal, antioxidant, anticancer, antidiabetic, and antileishmanial properties offer great prospects for their use in the treatment and prevention of various diseases. The larvicidal and pupicidal activities against human disease vectors, found in mycogenic TiO₂ [57], ZnO [64] and CeO₂ [97] NPs allow them to be used as agents of infection control. The prospects for fungi-derived NP use in agriculture are opened by CuO [33], ZnO [33] and Fe₂O₃ [37] NPs’ activity against bacterial and fungal crop pathogens and by TiO₂ NPs effect against insect pests [70]. Plant growth-promoting properties of TiO₂ [56] and MgO [104] myco-synthesized NPs enable their use as nano-fertilizers.

Another important characteristic of NPs is their photocatalytic properties, which determine their ability to degrade toxic dyes [176]. Dye-degrading ability was found in ZnO [74,86], ZnS [149,151], CdS [137], CdSe [162] and PbSe [169] mycogenic NPs. In addition, some fungi-derived NPs, such as Fe₂O₃ [42] and Fe₃O₄ [43], were found to be effective for metal ions removal. These properties allow the use of mycogenic oxide and chalcogenide NPs in the bioremediation of polluted areas and in the treatment of industrial and municipal wastewaters. Thanks to their unique physical and photochemical properties, chalcogenide NPs are actively used in various optical and data storage devices, sensors, batteries and solar cells [120]. Fungi-assisted biosynthesis of these NPs opens up opportunities for environmentally safe NP production for these applications.

5. Conclusions

As compared with the NPs of elementary metals and metalloids, the myco-synthesis of oxide and chalcogenide NPs is less widely studied, but in recent years, it has attracted increasing research attention. To date, the ability to form oxide and/or chalcogenide NPs has been found in about 70 species of fungi of different taxa, mainly in asco- and basidiomycetes. Fungal cultures can synthesize oxide, sulfide, selenide, and telluride NPs of many elements, which have diverse shapes and sizes (Figure 2).

The characteristics of NPs of the same chemical compound may vary greatly depending on the conditions of their production and are determined not only by the physical and chemical parameters of the reaction (precursors and their concentration, growth medium composition, pH, temperature, stirring rate, lighting, reaction time, and so on) but also by the characteristics of the fungal bio-object used (culture species, strain and age) and by the method of use of the fungus (as a living culture, filtered mycelial bio-mass, spores, extracts from the vegetative mycelium or fruit bodies, cell-free culture liquids, purified metabolites). The study of the influence of all these conditions on NP shape and size, their surface topography, dispersity, stability, aggregation resistance, formation rate, bioavailability, photoluminescent and magnetic properties, and biological activity is very important for selection of the most effective NP producers and optimization of the bio-nano-synthesis methods.

Micro-nano-synthesis of some oxides and chalcogenides, such as TiO2, ZnO, and CdS, has been well studied, but most of the NPs of these compounds remain virtually unexplored in terms of their fungi-mediated production. Fungal cultures are capable of forming NPs of highly diverse chemical compositions, including compounds that are not widely distributed and difficult to obtain, which have great potential for practical applications in various fields of science and technology. Therefore, important challenges facing nano-biotechnologists include:

• screening fungal cultures to identify NP producers of new, previously unexplored compounds;
• further enhancing the knowledge of already known mycogenic oxide and chalcogenide NPs;
• optimization of production methods and scaling up of processes for the biosynthesis of NPs with the required properties on an industrial scale;
• studying the possibilities of practical application of NPs and their introduction into practice.

The enormous potential of fungal cultures as NP producers of various oxides and chalcogenides, together with the extremely poor state of knowledge of the myco-nano-synthesis of the majority of these NPs, makes their further detailed and in-depth study, as objects for the biosynthesis of the oxide and chalcogenide NPs and nanomaterials based on them, a highly important task.