Impact of nanoparticles on toxigenic fungi

Chapter 14

Impact of nanoparticles on toxigenic fungi Josef Jampı´lek1, 2, Katarı´na Kra´lova´3 1 Department of Analytical Chemistry, Faculty of Natural Sciences, Comenius University in Bratislava, Slovakia; 2Division of Biologically Active Complexes and Molecular Magnets, Regional Centre of Advanced Technologies and Materials, Faculty of Science, Palacky University, Olomouc, Czech Republic; 3Institute of Chemistry, Faculty of Natural Sciences, Comenius University, Bratislava, Slovakia

1. Introduction The most prevalent toxigenic fungi belonging to the genera Aspergillus, Fusarium, Alternaria, and Penicillium that grow on several crops and produce harmful toxins represent serious phytopathological and mycotoxicological risks at preharvest and postharvest stages and also in processed food products [1,2]. Except the serious crop yield losses caused by toxigenic fungi, the produced mycotoxins including aflatoxins, ergot alkaloids, fumonisins, deoxynivalenol, and other trichothecenes, ochratoxin A, patulin, zearalenone, and citrinin adversely affect human and animal health (e.g., Refs. [3e11]), and therefore it is most desirable to eliminate these fungi even at the field, postharvest management, and food processing and prevent the entry of mycotoxins in food and feed. Fungal diseases that result in considerable crop losses worldwide and show adverse effects on plant quality could be suppressed by effective fungicides that control fungal disease by specifically inhibiting or killing the harmful fungi [12]. Mycotoxins normally enter the human and animal dietary system by direct contamination, when the food or feed becomes infected with a toxigenic fungus with subsequent toxin formation or by indirect contamination, and when an ingredient participating in a process has previously become contaminated with toxin-producing fungi and the fungus was not killed/ removed during processing; thus, the mycotoxins that are generally quite resistant to most forms of food and feed processing remain in the final product [13]. Therefore, it is very important to apply proper fungicides combating fungi already in the field, while the mycotoxins are on average more than 200-fold more toxic than such fungicides having short half-live and Nanomycotoxicology. https://doi.org/10.1016/B978-0-12-817998-7.00014-8 Copyright © 2020 Elsevier Inc. All rights reserved.

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appropriate postharvest storage [14,15]. For this purpose, nanoformulations of effective fungicidal compounds such as essential oils (EOs) or metal nanoparticles (NPs) are favorable. The US National Nanotechnology Initiative [16] defined the nanotechnology in 2004 as “the understanding and control of matter at dimensions of roughly 1 to 100 nanometers, where unique phenomena enable novel applications.” According to the recommendation on the definition of a nanomaterials adopted by the European Commission in 2011, the term “nanomaterial” means “a natural, incidental or manufactured material containing particles, in an unbound state or as an aggregate or as an agglomerate and where, for 50% or more of the particles in the number size distribution, one or more external dimensions is in the size range 1e100 nm. In specific cases and where warranted by concerns for the environment, health, safety or competitiveness the number size distribution threshold of 50% may be replaced by a threshold between 1 and 50%. Also a material showing the specific surface area by volume of the material >60 m2 cm
3 could be considered as nanomaterial” [17]. It could be noted that nanomaterials showing the same chemical composition as microscale/bulk materials may demonstrate not only different physical and chemical properties but they could also have distinct impact on the living organisms. The ability of NPs “to permeate anywhere” connects primarily with their particle size and shape [18e21], small particles being more effective due to their high specific surface area. Applications of nanoformulations enable to increase the apparent solubility of poorly soluble active ingredients and thus to enhance their bioavailability, to protect the active ingredient against degradation, and to allow their controlled/ targeted delivery to the site of action. Besides widespread use of nanoscale formulations in pharmacy and medicine (e.g., Refs. [22e24]), recently rapid expansion of their applications in agriculture and food industry contributes to sustainable intensification of agricultural production, improving of existing crop management techniques, securing the rise of global food production, guaranteeing of enhanced food quality, and minimizing the waste [25e29]. NPs have found application as effective pesticides [30e34], growth-promoting compounds, and in delivery of nutrients [30,33e35], as well as in controlling plant diseases [32], whereby a lower amount of active compounds is sufficient to achieve the same effect as preparations with bulk compounds. This chapter summarizes recent findings related to the effects of nanoscale fungicides on growth and mycotoxins production of toxigenic fungi, with a main focus on Aspergillus sp., Fusarium sp., Alternaria sp., and Penicillium sp. Attention is devoted to effective fungicidal nanoformulations of encapsulated EOs, metal-based (Ag, Au, Cu, Zn, Ni, Fe, TiO2) and carbon-based NPs, and to nanoformulations of encapsulated organic fungicides and their mechanism of action in killing toxigenic fungi. Benefits of the applications of nanoscale fungicides in the field for preventing yield loss and in postharvest

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management as well as their potential in the prevention of cultural heritage are discussed.

2. Impact of essential oils on toxigenic fungi and production of toxins Although EOs in eukaryotic cells can act as prooxidants and affect inner cell membranes and organelles, such as mitochondria, depending on type and concentration, they could also be cytotoxic to living cells [36]. EOs comprise a large number of components, and their hydrophobicity enables them to partition in the lipids of the cell membrane and mitochondria, rendering them permeable and leading to leakage of cell contents, whereby the action of EOs could be improved by low pH, low temperature, and low oxygen levels [37]. Because of volatile nature of EOs, they may be used as plant-based fumigants for stored food commodities and contribute to overcoming storage losses and in enhancing food shelf life [38]. For example, widely consumed spices and herbs cultivated mainly in tropic and subtropic areas can be often exposed to contamination with toxigenic fungi and subsequently mycotoxins and the presence of fungi and mycotoxins in foods not only modify sensorial properties but it also represent a serious health risk for consumers [39,40]. A review paper focused on nonbiological postharvest procedures to decontaminate mycotoxins in foods and feeds was presented by Temba et al. [41]. Application of EOs can inhibit not only the growth of toxigenic fungi but also the production of their harmful metabolites adversely affecting animals and human health, and therefore EOs could be also used to control both the growth and production of toxic secondary metabolites of these fungi. The fennel EO applied at a dose 5 mL/mL reduced the ochratoxin A production by Aspergillus carbonarius up to 88.9% compared with the control, with only 13.8% of fungal growth reduction and downregulated levels of ackps gene responsible for the ochratoxin A biosynthesis by 99.2% [42]. Curcuma longa L. EO applied at doses 3500 and 3000 mg/mL, respectively, completely inhibited the growth and zearalenone production of Fusarium graminearum [43] and farnesol, occurring in many EOs, and strongly inhibited the growth of hyphae of Penicillium expansum by stimulating apoptosis via activation of metacaspase, production of reactive oxygen species (ROS), and disintegration of cellular ultrastructure [44]. Antifungal activities of C. longa L. against Aspergillus flavus were reported to be related to the disruption of fungal cell endomembrane system, including the plasma membrane and mitochondria, resulting in the inhibition of ergosterol synthesis, mitochondrial ATPase, malate dehydrogenase, and succinate dehydrogenase activities [45]. EOs of Rhanterium adpressum obtained separately by hydrodistillation of the aerial parts of plant (leaves and flowers) that was characterized with relatively high portion of oxygenated monoterpenes effectively inhibited production of type B trichothecenes in mycotoxigenic strains of the genus Fusarium [46].

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Gaultheria fragrantissima Wall EO containing as the major component methyl salicylate notably inhibited growth and aflatoxin B1 production by toxigenic strain of A. flavus LHP (B)-7 at 1.0 and 0.7 mL/mL, respectively, while it did not adversely affect germination of millets [47]. Thymol exhibited potential antifungal activity against F. graminearum (the average EC50 value of 26.3 mg/ mL estimated for 59 F. graminearum isolates) due to the cell membrane damage originating from lipid peroxidation and the disturbance of ergosterol biosynthesis [48]. Cynara cardunculus L. extract was found to inhibit aflatoxin B1 production by Aspergillus parasiticus in Sesamum indicum L. seed paste and in yeast extract sucrose medium by 99.6% and 99.4%, respectively [49]. The in vitro antifungal activities of bergamot and lemon EOs and five natural compounds recurrent in EOs (citronellal, citral, cinnamaldehyde, cuminaldehyde, and limonene) against mycotoxigenic fungi Fusarium sporotrichioides, F. graminearum, and Fusarium langsethiae decreased as follows: cinnamaldehyde > cuminaldehyde > citral > citronellal > bergamot oil > limonene > lemon oil; however by the application of sublethal concentrations of some natural products, mycotoxin production could be enhanced [50]. In addition, cinnamaldehyde at a concentration of 104 mg/L completely inhibited fungal growth and aflatoxin B1 production in A. flavus, affected the morphology and ultrastructure of mycelium, and its inhibitory effect could be attributed to oxidative stress alleviation possibly induced by modifications of cellular structure and redox status [51]. The antifungal activity of cinnamon oil against Fusarium verticillioides was proportional to its cinnamaldehyde concentration, which at the concentration corresponding to its minimum inhibitory concentration (MIC) caused irreversible deleterious morphological and ultrastructural alterations including lack of cytoplasmic contents, loss of integrity and rigidity of the cell wall, plasma membrane disruption, mitochondrial destruction, and folding of the cell, whereby the interference of this active ingredient with enzymatic reactions of cell wall synthesis adversely affected the morphogenesis and growth of the fungus [52]. The antifungal activity of the EO extracted from the seeds of dill (Anethum graveolens L.) against A. flavus was connected with disruption of the permeability barrier of the plasma membrane and the mitochondrial dysfunction-induced ROS accumulation in the fungus, whereby besides the morphological changes in the cells of A. flavus caused by EO also a reduction in the ergosterol quantity was observed [53]. Increased antifungal effects against mycelium growth of Aspergillus niger were estimated also by incorporation of Mentha longifolia extract into chitosan (CS) NPs [54]. Eugenol oil nanoemulsion showed antifungal activity against Fusarium oxysporum f. sp. vasinfectum and could be used for protecting cotton seed from Fusarium wilt infection [55]. A combined formulation of oregano and thyme EOs resulted in a synergistic effect, showing enhanced efficiency against A. flavus, A. parasiticus, and Penicillium chrysogenum, while mixtures of peppermint and tea tree EOs produced synergistic effect against A. niger [56].

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Ozcakmak et al. [57] estimated that ochratoxin A production in ochratoxigenic Penicillium verrucosum could be considerably reduced by Salvia officinalis and Mentha piperita EOs, while it can be completely prevented by treatment with garlic and wild oregano EOs applied at doses of 0.5% and 0.25%. The gum of Pistacia atlantica subsp. kurdica dissolved in water and applied at a dose 125 mg/mL pronouncedly decreased aflatoxin production in A. parasiticus, aflatoxin B1 production being entirely inhibited and notable reduction of aflR gene expression in treated fungi was observed as well [58]. Complete inhibition of ergosterol biosynthesis by Aspergillus ochraceus was observed at 100 mg/mL of natural cinnamaldehyde and at 200 mg/mL of citral, while total inhibition was not estimated at treatment with 200 mg/mL eugenol. On the other hand, citral and eugenol pronouncedly inhibited the ochratoxin A biosynthetic pathway resulting in the inhibition of ochratoxin A production at 75 and 150 mg/mL, respectively, while complete inhibition of ochratoxin A production by natural cinnamaldehyde was not estimated at 200 mg/mL, which was connected with the conversion of active cinnamaldehyde to cinnamic alcohol by A. ochraceus [59]. The degradation of fumonisin B1 by six tested EOs decreased as follows: cinnamon EO, citral, eugenol oil, eucalyptus oil, anise oil, and camphor oil, and under optimal condition (exposure to 280 mg/mL for 120 h at 30 C), cinnamon EO reduced fumonisin B1 from 15.03 to 0.89 mg/mL (94.06%) [60]. Application of ethanolic and chloroformic fractions of Eucalyptus globulus at 2500 mg/g effectively reduced growth of Alternaria alternata by 66%e74% and Alternaria arborescens by 86%e88%, respectively; it caused 89% reduction of tenuazonic acid and 75%e94% reduction of alternariol as well as almost complete inhibition of alternariol monomethyl ether; and these extracts were able completely inhibit growth of both fungi on unwounded tomato fruits and considerably reduced their aggressiveness on wounded fruit [61]. Among Cymbopogon citratus, E. globulus, Origanum vulgare, Ruta graveolens, S. officinalis, and Satureja montana EOs, S. montana EO prevented most effectively the growth of A. parasiticus, while R. graveolens EO inhibited most of the aflatoxin production even though growth inhibition was low and at treatment with C. citratus EO trace levels of aflatoxins were detected. As most effective inhibitors of fungal growth EOs containing carvacrol and/or thymol (S. montana and O. vulgare) were estimated, while synthesis of aflatoxins was inhibited with EO containing 2-undecanone and 8-phenyl-2-octanone (R. graveolens) [62]. Beside plants EOs also Shewanella algae strain YM8 producing volatiles with strong antifungal activity against Aspergillus pathogens inhibited Aspergillus growth and aflatoxin biosynthesis in maize and peanut samples stored at different water activity levels, caused severe damage to conidia and a complete lack of mycelium development and conidiogenesis, and was effective also to some other phytopathogenic fungi, including A. parasiticus,

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A, niger, A. alternata, Botrytis cinerea, F. graminearum, F. oxysporum, Monilinia fructicola, and Sclerotinia sclerotiorum [63]. The effects of plant extracts on mycotoxin biosynthesis were variable and strain dependent. The MIC and minimum fungicidal concentration (MFC) values estimated for antimycotoxigenic activities of Boswellia serrata EO tested in vitro against 15 different field and storage fungi ranged between 0.039e0.625 and 2.5e10.0 mL/mL, respectively, and a dose 6 mL/mL completely inhibited the production of aflatoxin B1 and fumonisin B1, and strong decrease of the ergosterol content with the increasing concentration of EO was observed as well. Moreover, in viable maize model the contents of aflatoxin B1 and fumonisin B1 were pronouncedly inhibited with increasing seedling vigor of maize [64]. Lemon, grapefruit, eucalyptus, and palmarosa EOs caused degradation of zearalenone in vitro, and application of palmarosa EO at pH 6 and 4 or 20  C resulted in toxin degradation rate >99% [65].

2.1 Nanoformulations improving impact of essential oils on toxigenic fungi The oxidative stability, thermostability, shelf life, and biological activity of EOs could be improved by microencapsulation because due to functional barrier between the core and wall material, chemical and physical reactions could be avoided, volatility of EOs is reduced, and the biological, functional, and physicochemical properties of EO representing core materials are maintained [66]. Mode of action, synergies, and interactions of EOs with food matrix components focused on EOs applied in food preservation was overviewed by Hyldgaard et al. [67]. EOs play a fundamental role in protecting the plant from biotic and abiotic attacks to which it may be subjected. Nazzaro et al. [68] overviewed antifungal activity of EOs and their role in blocking cell communication mechanisms, fungal biofilm formation, and mycotoxin production. Smaller amounts of EOs in the packaging material are preferable, and a combination of EOs with other antimicrobial compounds can decrease the required dose of EOs while maintaining the appropriate antimicrobial activity. In experiments preformed on Sabouraud Dextrose culture the nanodispersed cinnamaldehyde showed not only a lower MIC value against A. flavus (0.8 mM) than free cinnamaldehyde but also improved activity against aflatoxin production without the promotion at lower dose. Moreover, in an experiment performed in peanut butter, where antifungal activity of free cinnamaldehyde was negatively affected and at the concentration of 0.25 mM, free cinnamaldehyde stimulated aflatoxin B1 production, the nanodispersed cinnamaldehyde exhibited more than twofold improved activity against the growth of A. flavus and more efficient inhibition of aflatoxin B1 production as well [69].

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Differences in the impact of tested EOs encapsulated in nanoemulsions on antifungal activity against A. niger were estimated: while the encapsulation of cinnamon leaf EO strongly enhanced the inhibiting effect against A. niger mycelial growth and spore germination compared to the free EO, for encapsulated citrus EOs, decreased antifungal activity was observed likely because of the nanoemulsion acted as a hydrophobic sink for the main constituents of citrus EOs. Moreover, the resulting antifungal activity was pronouncedly affected by the applied emulsifier; anionic whey protein isolateebased nanoemulsions are more effective in inhibiting the mycelial growth and the spore germination of A. niger than nanoemulsions prepared using nonionic surfactant Tween 80 [70]. Illicium verum Hook. f. EO with anethole (anise camphor) as major compound followed by estragole (89.12% and 4.86%, respectively) showing MIC and minimum aflatoxin B1 inhibitory concentration against aflatoxigenic strain A. flavus LHP-PV-1 of 0.7 and 0.5 mL/mL, respectively, caused reduction in ergosterol content and enhanced leakage of Ca2þ, Kþ, and Mg2þ ions (denoting fungal cell membrane as a site of action), and this EO was found to exhibit notable protection of Pistacia vera from aflatoxin B1 contamination in storage containers. Enhanced efficacy as fungal inhibitor and aflatoxin suppressor also exhibited its nanoencapsulated formulation in gel form and lyophilized form, which could be used in industry as shelf life enhancer of food items [71]. Raphael and Meimandipour [72] investigated the antimicrobial activity of CS film forming solution incorporated with EOs against A. niger and A. alternata and found that these formulations showed higher antifungal activity than free EOs and CS film solution, whereby the increase of the concentration of EOs in the film resulted in improved antifungal activity of CS, and CSeEOs complexes were evaluated as promising candidates for novel contact antimicrobial agents that can be used in animal feeds. Encapsulation of M. piperita EO in CSecinnamic acid nanogel enhanced not only the stability of EO but also its antifungal activity against A. flavus compared with free EO (MIC 500 and 2100 ppm, respectively, under sealed condition), and it could be noted that the formulation of encapsulated EO performed better (800 ppm) also in tests at nonsealed condition, while the free oils did not cause complete inhibition neither at a dose of 3000 ppm [73]. Gaultheria procumbens EO with major component methyl salicylate (96.25%) encapsulated in CSecinnamic acid microgel showing spherical shape and particle sizes 7.00e90.0 mm was found to be more efficient as antifungal agent and aflatoxin B1 suppressor compared with its uncapsulated application; encapsulated EO completely inhibited growth and toxin production at 1.00 mL/mL by targeting ergosterol content in the cell membrane, thereby causing the release of cellular ion contents and morphological alteration in A. flavus [74]. To reduce the volatility and instability of free thyme EO and increase halflife and the antifungal properties of this EO, Khalili et al. [75] encapsulated it

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in CS and benzoic acidemade nanogel, and this nanoformulation showed MIC of 300 mg/L against A. flavus at sealed condition compared with 400 mg/L estimated for free EO, and also under nonsealed condition, the nanoformulation completely inhibited fungal growth at 500 mg/L, which did not prove neither a double dose of free EO. Incorporation of thymol into a low-surfactant submicron emulsion with and without a carrier oil resulted in the MFC of 0.02% against F. graminearum and thymol emulsions applied at a dose >006% inactivated F. graminearum in 10 s. Spraying the thymol emulsions (approximately 0.1%) on the wheat variety, Bobwhite resulted in considerable reduction of number of infected spikelets, and it was found that the mechanism of antifungal action was membrane mediated and thymol caused complete organelle disorganization and lipid emulsification in exposed conidia [76]. Microparticles of cinnamon, clove, and thyme EOs encapsulated in CS with average size approximately 750 nm inhibited radial growth and spore germination of F. verticillioides and A. parasiticus better than unencapsulated EOs and also reduced mycotoxin production suggesting their fungistatic effect [77]. Cymbopogon martinii EO encapsulated in CS NPs showing spherical morphology with zeta potential of 39.3e37.2 mV and particle sizes 455e480 nm was characterized by gradual release of antifungal constituents resulting in an increase of the lifetime antifungal activity of EO in vitro and showed enhanced antifungal and antimycotoxin activities against F. graminearum compared to free EO also in a test performed with maize grains under laboratory conditions over a storage period of 28 days. Macroconidia exposed to this EO were adversely affected, and death of fungi caused by enhanced intracellular ROS levels and lipid peroxidation as well as reduction of ergosterol content was observed [78]. A CS coating containing O. vulgare L. EO reduced the incidence of black mold caused by A. niger in artificially contaminated cherry tomato fruit during storage at 25 and 12  C, respectively, delayed the reduction in lycopene, ascorbic citric acid, glucose, and fructose levels during the storage time assessed at room or cold temperatures, and showed increased catechin, myricetin, caffeic, and syringic acids contents compared to uncoated fruit during the storage at both tested temperatures [79]. The optimized CS/citral nanoemulsion with particle sizes 27e1283 nm showed antifungal activity against A. niger with EC50 of 278 mg/ L [80]. Fabra et al. [81] reported that nanolaminated films prepared by the layerby-layer deposition method with alternating layers of alginate and zein-carvacrol nanocapsules (enabling the controlled release of the active agent, carvacrol, from the nanocapsules) on an aminolysed/charged polyethylene terephthalate film showing antifungal activity against Alternaria sp. and Rhizopus stolonifer could be considered to improve the shelf life of foodstuffs. Optimized alginate microspheres prepared using emulsion extrusion method and hardened with a cross-linking agent CaCl2, in which

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EOs were encapsulated, showed depending on type of EO the loading capacity of 22%e24% and encapsulation efficiency (EE) of 90%e94% and effectively reduced the evaporation rate of EOs. They were characterized with a sustained in vitro release profile and maintained 50% of the antifungal activity against A. niger and F. verticillioides at the eighth day of the study [82]. EO of Lippia turbinata microencapsulated in gelatin/gum arabic system allowing its controlled release showed considerable antifungal effect on peanut mycoflora (59%e77% reductions), treated peanut seeds showed lesser extent of the prevalence of Penicillium and Aspergillus throughout the storage period, and the microencapsulated preparation was able to cause complete inhibition of peanut seed germination [83]. Active films based on cellulose acetate incorporating different concentrations of oregano EO and organophilic montmorillonite clay showed high antifungal activity against A. alternata and have potential to be used to control the growth of phytopathogenic fungi [84]. EO components (carvacrol, cinnamaldehyde, eugenol, and thymol) encapsulated into silica mesoporous support MCM-41 exhibited sustained antifungal effects against A. niger in vitro [85]. Long-term antifungal activity of volatile EO components released from mesoporous silica materials, MCM-41, against A. niger was reported also by Janatova et al. [86]. EOs that were extracted from the leaves of E. globulus and Citrus media and nanofunctionalized with mycosynthesized sulfur and aluminum oxide NPs were recommended to be used as novel antimicrobial agents to prevent food spoilage caused by food-borne pathogens [87]. Zataria multiflora EOeloaded solid lipid NPs with particle size approximately 255 nm, polydispersity index of 0.369  0.05, zeta potential approximately
37.8  0.8 mV, and EE of 84  0.92% also showed lower MIC values under in vitro conditions against A. ochraceus, A. niger, A. flavus and Alternaria solani (200, 200, 200, and 100 ppm) than EO alone (300, 200, 300, and 200 ppm) [88]. The physical properties and antifungal and mycotoxin inhibitory activity of clove oil-in-water nanoemulsions with mean diameters of <150 nm showing high physical stability over 30 days storage were found to be affected by oil composition. Under the same clove oil concentration in oil phase, the presence of medium chain triacylglycerol as ripening inhibitor decreased the antifungal and mycotoxin inhibitory activity of clove oil against F. graminearum isolates more than corn oil. However, encapsulation in nanoemulsions considerably enhanced the mycotoxin inhibitory activity of clove oil [89]. Aspergillus steynii and Aspergillus tubingensis belong to the main ochratoxin Aeproducing species in Aspergillus. Tarazona et al. [90] tested bioactive ethylene-vinyl alcohol copolymer (EVOH) films containing selected components of some plant EOs (cinnamaldehyde, linalool, isoeugenol, or citral) against A. steynii and A. tubingensis growth and ochratoxin A production in partly milled maize grains and found that the most effective films against both

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species were those containing cinnamaldehyde, and A. tubingensis was generally less sensitive to treatments than A. steynii. Based on the obtained results, the EVOH films containing cinnamaldehyde, isoeugenol, and citral applied in vapor phase could be used as potent antifungal agents against A. steynii and A. tubingensis and strong inhibitors of ochratoxin A biosynthesis in maize grains at very low doses. The incorporation of an EO such as anise, orange, and cinnamon in the formulation of edible films was found to improve not only their physical properties (e.g., vapor permeability and hardness) but also antifungal efficiency against Penicillium sp. and Rhizopus sp., suggesting that similar preparations could represent an alternative use as coatings to enhance the shelf life of food products [91].

3. Impact of metal nanoparticles on toxigenic fungi 3.1 Silver nanoparticles Ismaiel and Tharwat [92] tested the antifungal activity of Agþ ion from AgNO3 solution against two pathogenic and toxigenic fungal strains, A. flavus OC1, a clinical aflatoxigenic strain causing fungal keratitis, and Penicillium vulpinum CM1, a maize-pathogenic strain that is positive for patulin producing ability, using agar well diffusion assays on yeast sucrose agar and filter- or autoclaved-sterilized Agþ ions. The MIC values of the filter-sterilized Agþ ions against A. flavus OC1 and P. vulpinum CM1 were 70 and 60 mg/mL, respectively, while the corresponding MFC values were 120 and 80 mg/mL, respectively. Notable changes in the nature of cell membranes and cytoplasmic organelles in hyphal cells exposed to Agþ ions were estimated, and application of Agþ to yeast sucrose broth resulted in the inhibition of mycelial growth and aflatoxin B1 and patulin formation of both strains. In the study focused on in vitro fungistatic activity of colloidal silver against selected fungi following EC50 values related to the inhibition of mycelial growth were estimated: 3.69 ppm for Alternaria brassicicola, 7.32 ppm for B. cinerea, 18.21 ppm for A. flavus, 10.43 ppm for A. niger, 11.99 ppm for Fusarium culmorum, 12.27 ppm for F. oxysporum, 10.82 ppm for Penicillium digitatum, and 6.34 ppm for Sclerotinia [93]. AgNPs were found to decrease the mycotoxin production of Aspergillus sp. (81%e96%) and reduce mold cytotoxicity (50%e75%); they affected the organic acid production of A. niger and P. chrysogenum by decreasing their concentration (especially of the oxalic and citric acid) and modified the extracellular enzyme profile of both pathogenic fungi, although the total enzymatic activity was increased [94]. A dose of 100 ppm AgNPs led to 92.2% inhibition of A. brassicicola grown on potato dextrose agar suggesting that AgNPs effectively inhibited the growth of this toxicogenic fungus and could be used as fungicide in the management of black spot of cauliflower, radish,

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and cabbage causing severe agricultural loss [95]. Alananbeh et al. [96] tested antifungal activity of uncoated rod- and cube-shaped AgNPs against Aspergillus sp., i.e., A. niger and Aspergillus terreus fungi isolated from waste water of different sources in Madinah, Saudi Arabia. A. terreus was found to be more sensitive to AgNPs than A. niger, although no notable differences were found among applied doses of 1, 10, and 100 mg/mL, and the rod-shaped NPs inhibited growth of fungi more efficiently than the cube-shaped NPs. Spherical AgNPs with particle sizes ranging from 5 to 30 nm that were biosynthesized using A. terreus KC462061, when applied at a dose of 150 ppm, caused 71.1%
86.3% growth inhibition and 100% inhibition of aflatoxin production in five A. flavus isolates. At application of 50 ppm AgNPs, the inhibition of aflatoxin production ranged from 48.2% to 61.8%, and at exposure to 100 ppm, it ranged from 46.1% to 82.2% [97]. Application of AgNPs with an average size of 4.5 nm at a dose of 5 mg/mL notably decreased secretion of aflatoxin B1 from A. flavus, and it was demonstrated that AgNPs could trigger the release of O2
from fungal mycelia, and thus a mechanism involving O2
release was proposed to explain reduction of aflatoxin production from A. flavus by AgNPs [98]. Green synthesized AgNPs using pomegranate peel with particle sizes 5e50 nm decreased aflatoxin production in A. flavus isolated from hazelnut with increasing AgNPs concentration, with maximum suppression of aflatoxin production being observed at a dose of 150 ppm [99]. Significant inhibitory effect against A. flavus and A. terreus also exhibited spherical AgNPs with mean size of 29 nm and zeta potential of þ0.6 mV, which were synthesized using pelargonium/geranium leaf extract via a hydrothermal method [100]. Among AgNPs biosynthesized using 10 different plants extracts that were found to inhibit fungal growth of Aspergillus spp. isolated from infected peanuts, the most effective antifungal activity showed C. citratus leaf extract mediated AgNPs with MIC 20 mg/mL [101]. Using Cassia roxburghii aqueous leaf extract, highly efficient and stable AgNPs with mean size of 35 nm and the zeta potential of
18.3 mV were prepared, which exhibited higher antifungal activity against tested human fungal pathogens including A. niger, Aspergillus fumigatus, A. flavus, Penicillium sp., and F. oxysporum than the conventional antifungal drug amphotericin B [102]. AgNPs green synthesized using the flower bud’s aqueous extracts of Brassica oleracea (broccoli) acting as antimicrobial agents against human pathogenic bacteria and fungi with NPs sizes of 12e22 nm showed better antifungal activity against A. flavus, A. niger and Candida albicans than fluconazole [103]. The antifungal activity of spherical-shaped AgNPs with particle sizes 20e35 nm biosynthesized from aqueous stem bark extract of the medicinal plant Cochlospermum religiosum that was tested against various fungal species decreased as follows: A. flavus > Rhizopus > Fusarium > Curvularia > A. niger [104]. Antimycotic activity of AgNPs biosynthesized using Thuja occidentalis L. leaf extract with particle sizes <30 nm against A. niger, Fusarium spp., and A.

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alternata increased with increasing NPs concentration in the growth media, and even a 10 ppm solution of AgNPs was found to be detrimental to fungal growth [105]. The potential of AgNPs biosynthesized using leaf aqueous extracts from two plants species (Foeniculum vulgare and Tecoma stans) as preventive/corrective treatments to protect stucco materials from biodeterioration, as well as the microbial inhibition on three stone materials (stucco, basalt and calcite), was analyzed by Carrillo-Gonzalez et al. [106]. The researchers isolated 23 bacterial species belonging to 8 genera and 14 fungal species belonging to 7 genera (including A. alternata) from colored stains, patinas, and biofilms produced on the surfaces of archaeological walls from the pre-Hispanic city, Teotihuacan, and proved that a preventive or corrective treatment with AgNPs resulted in a decrease of microbial colonization in three kinds of stone used in historical walls. AgNPs prepared using Plectranthus amboinicus leaf extract acting as both reducing and capping agent showed strong antifungal activity against Penicillium spp. [107]. AgNPs with particle sizes 25e55 nm prepared using a warm water extract of Chroococcus dispersus and Chlorella vulgaris algae showed high antifungal activity against Fusarium solani, Fusarium oxysporum, Rhizoctonia solani, Helminthosporium sp., A. alternata, and S. sclerotiorum fungi ninefold exceeding that of the generic antibiotics (ampicillin, gentamycin, and streptomycin) [108]. AgNPs synthesized using Penicillium citrinum were found to inhibit the growth of aflatoxigenic A. flavus var. columnaris isolated from sorghum grains in vitro [109]. Spherical and monodispersed AgNPs with an average size of 14.8  1.2 nm mycosynthesized using an aqueous extract of endophytic nonpathogenic fungus A. solani F10 (KT721914) showed strong antifungal activity against different pathogenic isolates of the same A. solani fungus, whereby treated fungal hyphae showed formation of pits and pores suggesting that AgNPs were able to pass and distribute throughout the fungal cell area and interact with the cell components [110]. AgNPs of 45 ppm present in the environment was found to decrease fungal numbers (33%e85%) and eliminate fungal strains A. alternata and Cryptococcus laurentii. Based on the biomass growth of A. niger and P. chrysogenum in environmental samples containing AgNPs, it was observed that environment can enhance (soil extract) or inhibit (sewage) antifungal activity of AgNPs [111]. Considerable reduction in mycelial growth was observed for spores of F. culmorum incubated with AgNPs, which depended on the incubation time and type of growth medium but did not depend significantly on the AgNPs concentration up to 2.5 ppm. The number of spores formed by mycelia increased in the culture after contact with AgNPs, in particular, on the nutrient-poor potato dextrose medium, and 24 h incubation of spores with a 2.5 ppm solution AgNPs resulted in great reduction of the number of germinating fragments and sprout length relative to the control [112]. Kotzybik et al. [113] investigated the impact of AgNPs (0.65e200 nm) on the physiology of the mycotoxigenic filamentous fungus P. verrucosum and found that NPs

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significantly affected the growth and mycotoxin biosynthesis, attached to the mycelial surface and AgNPs with sizes 0.65 and 5 nm, respectively, were internalized within the cell, formed agglomerates in the cytoplasm, and associated to cell organelles. Xu et al. [114] compared the antifungal activity of AgNPs and natamycin against ocular pathogenic filamentous fungi in vitro by testing their impact on 216 strains of fungi isolated from patients with fungal keratitis, whereby the isolates included 112 Fusarium isolates (82 F. solani species complex, 20 F. verticillioides species complex, and 10 F. oxysporum species complex), 94 Aspergillus isolates (61 A. flavus species complex, 11 A. fumigatus species complex, 12 Aspergillus versicolor species complex, 10 A. niger species complex), and 10 A. alternata isolates. The estimated MIC50 values of AgNPs/ natamycin were 1/4, 0.5/32, and 0.5/4 mg/mL for Fusarium spp., Aspergillus spp., and A. alternata, respectively, while the corresponding MIC90 were 1/8, 1/32, and 1/4 mg/mL, respectively, suggesting better in vitro activity of AgNPs against ocular pathogenic filamentous fungi than natamycin. According to the results of microbial contamination analysis of air and surfaces in six different museums and archives in Poland, among fungi contaminating museums and archives, some potentially allergenic and toxic species such as A. fumigatus, A. flavus, A. ochraceus, A. parasiticus, and A. versicolor were estimated, and it was found that treatment with AgNPs (10e100 nm) at a dose 90 ppm effectively removed the microorganisms present on the surface of objects, while by using a half dose of AgNPs (45 ppm), 94% of all microorganisms could be removed [115]. Disinfection of archaeological textiles made of wool, cotton, and sisal with AgNPs misting was reported to reduce the number of microorganisms, depending on the qualitative microbial contamination by 30.8%e99.9%, and in such way prevent biodeterioration of archaeological materials [116]. On the other hand, Villamizar-Gallardo et al. [117] evaluated microbicidal effect of chemically synthesized AgNPs on potentially toxigenic fungi affecting cocoa (Theobroma cacao) crops isolated from diseased cocoa pods showing high prevalence of two potentially toxigenic fungi, A. flavus and F. solani, respectively. While in liquid and solid synthetic culture media the AgNPs did not considerably affect the growth of these fungi, even at a dose of 100 ppm, positive inhibitory effect in plant tissues infected with A. flavus was observed. For example, for complete inhibition of fungal growth in the cortex, application of 80 ppm was sufficient, suggesting that microbicidal effect of AgNPs is greater in plant tissues than in culture media. However, once fungi have penetrated inside the pods, their growth was unavoidable and AgNPs effect was lower. Ogar et al. [118] tested antifungal properties of AgNPs against common indoor mold species Penicillium brevicompactum, A. fumigatus, Cladosporium cladosporioides, Chaetomium globosum, and Stachybotrys chartarum cultured on agar media as well as antifungal activity of AgNPs in relation to

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C. globosum and S. chartarum grown on the surface of gypsum drywall and found that a dose of 30e200 mg/L AgNPs considerably inhibited the growth of fungi, and treatment with AgNPs also pronouncedly affected the parameters of conidiophores/sporangiophores. Citrate-coated AgNPs (20 nm) applied at appropriate nonlethal dose can cause more than twofold inhibition of biosynthesis of the carcinogenic mycotoxin and secondary metabolite, aflatoxin B1 by A. parasiticus, without inhibiting fungal growth, and this inhibition was connected with the mycelial uptake of AgNPs. Application of AgNPs resulted in considerable decrease in transcript levels of five aflatoxin genes and at least two key global regulators of secondary metabolism, laeA and veA, and total ROS reduction. However, aflatoxin biosynthesis could be completely restored as a result of AgNPs depletion in the growth medium [119]. AgNPs incorporated on cellulose acetate nanofibers prepared by electrospinning technique exhibited strong inhibitory activity against A. flavus [120]. AgNPs prepared using gum kondagogu (Cochlospermum gossypium) with particle sizes 3.6  2.2 nm showed antifungal activity against A. parasiticus NRRL-2999 and A. flavus NRRL-6513 with MICs and MFCs ranging from 3.5 to 6.5 mg/mL and caused morphological changes such as deformation, shrunken, and ruptured mycelium of the fungi. Increased oxidative stress caused by AgNPs resulted in outer membrane damage and higher levels of Kþ release from the fungi [121]. AgNPs-encapsulated CS functionalized with 4-[(E)-2-(3-hydroxynaphth alen-2-yl)diazen-1-yl]benzoic acid was reported to be suitable for antifungal applications against A flavus and A. terreus [122]. Spherical AgNPs in CS stabilizer were synthesized using electron beam irradiation with particle sizes 5e20 nm, and their application in CS solution effectively inhibited the growth of several fungi, i.e., Curvularia lunata, Trichoderma sp., Penicillium sp., and A. niger, commonly found on the building surface [123]. Poly(vinyl alcohol) capped spherical AgNPs synthesized at various pH conditions were reported to exhibit strong antifungal activity against A. niger and Penicillium sp., particles with smaller size being more efficient [124]. Racova and Ryparova [125] studied inhibitory effects of AgNPs and Agþ ions on mold growth on surfaces of building materials used for construction of crawl space, all of them being board materials (one group was plaster based and the second group was wooden based) that were exposed to ideal condition for mold growth and found that protection against mold (consisting of typical mold mixture including Trichoderma, Penicillium, Alternaria, Paecilomyces) by AgNPs and Agþ ions was not universally applicable protection for all tested materials, and it would be desirable to find ideal concentration for different material as well as to find better application than painting. At investigation of the mechanism of action of AgNPs on molds, Pietrzak et al. [126] found that treatment with 15 ppm AgNPs resulted in the downregulation of 162 metabolites of A. niger and 19 metabolites of P. chrysogenum, while at treatment

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with higher concentration (62 ppm) the number of downregulated metabolites was 284 (A. niger) and 29 (P. chrysogenum), respectively. In the mold mycelium accumulated Agþ ions and their clusters (Ag, Ag2, and Ag3) as well as Agþ ion adducts with nucleotide derivatives, amino acids, peptides, and lipids were observed. AgNPs treatment also caused shortening and condensation of hyphae, ultrastructural reorganization, cell plasmolysis, increased vacuolization, collapsed cytoplasm, accumulation of lipid material, condensed mitochondria, disintegration of organelles, nuclear deformation, condensation and fragmentation of chromatin, creation of apoptotic bodies, and a new inside cell wall in P. chrysogenum. Spherical shaped and monodispersive Ag2O/Ag NPs with particle sizes ranging from 20 to 60 nm biosynthesized using the culture filtrate of marine Streptomyces sp. VITSTK7 showed antifungal activity against medically important pathogenic A. niger, A. flavus, and A. fumigatus with antifungal index ranging from 62% to 75% [127]. The AgNPs and CuO NPs showed considerably higher antifungal activity against A. niger, A. flavus, and A. fumigatus and antibacterial activity against bacterial strain of Bacillus alvei, the short Bacilli, and the Bacilli spore former than TiO2 NPs. AgNPs were also applied for treatment and conservation of three ancient Egyptian funeral masks in Saqqara, Egypt, because they were able to inhibit the growth of both fungi and bacteria safely, without any effect on the colors of funeral masks, while CuO NPs may be refused for these purposes due to the probability of changing colors of artifacts [128]. A. flavus and P. chrysogenum, similar to bacteria Escherichia coli and Staphylococcus aureus, showed clear hypersensitivity to AgNPs biosynthesized using Althaea officinalis, Thymus vulgaris L., and Mentha pulegium L. leaf extracts as well as to CuNPs prepared by reduction of CuCl2 with L-ascorbic acid, whereby the inhibitory activity of NPs was pronouncedly greater than that of AgNO3 and CuCl2 and the effectiveness of AgNPs was considerably higher than that of CuNPs [129].

3.2 Gold nanoparticles AuNPs biosynthesized using Aspalathus linearis tea leaves with mean particle size about 41  1 nm attached onto commercial antifungal discs (e.g., amphotericin B, fluconazole, clotrimazole, econazole, flucytosine, ketoconazole, miconazole, and nystatin) notably improved the antifungal activity of antibiotic discs against four Aspergillus spp., AuNPs-coated econazole being the most efficient [130]. Triangular and spherical-like AuNPs with sizes 5e20 nm biosynthesized using Punica granatum fruit extract showed excellent antifungal activity against nontoxigenic A. flavus ATCC 10124 [131]. Spherical AuNPs prepared using aqueous extract of Abelmoschus esculentus with particle sizes ranging from 45 to 75 nm showed high antifungal efficacy against

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A. flavus and A. niger reflected in inhibition zone of 16  0.5 and 15  1.5 mm, respectively, estimated by well diffusion method at treatment with 50 mL AuNPs [132]. Afifi et al. [133] investigated antifungal activities of three shapes (rods, spheres, and prisms) of AuNPs on deterioration of archeological gilded painted cartonnage, late period, Saqqara, Egypt. Among four isolated fungal species (A. flavus, B. cinerea, Fusarium moniliforme, and Verticillium albo-atrum), a 9 cm inhibition zone was estimated against the most sensitive fungal species A. flavus, and exposure to AuNPs was accompanied with leakage of proteins, nucleic acids, sugars, and electrolytes. Zone of inhibition estimated for antifungal activity of fluconazole coated with 40 mL AuNPs against A. niger and A. flavus was found to be 13 and 12 mm, respectively, and MIC values of fluconazole coated with AuNPs represented only a half of corresponding MIC values of AuNPs estimated against A. niger and A. flavus [134]. At evaluation of the antifungal efficiency of AuNPs against P. citrinum, F. verticillioides, and A. flavus, neither treatment with 0.2 mg/L in potato dextrose agar was able to cause complete inhibition of fungal growth; however, in contrast to fungi grown in control medium, damaged hyphae and unusual bulges were observed in AuNPs-treated fungi, resulting in reduced growth which could affect the toxins production by these fungi [135].

3.3 Copper nanoparticles CuNPs were reported as efficient inhibitors of fungal growth and treatment with 250 mg/mL CuNPs completely suppressed fungal growth (assayed as biomass dry weight) of A. niger, F. solani, and A. solani, while application of 200 mg/mL inhibited the growth of these fungi by 95.7%, 95.2%, and 97.4%, respectively, and their inhibitory effectiveness exceeded that of CuSO4. Exposure of fungi to 200 mg/mL CuNPs on potato dextrose agar resulted in fungal growth reduction of 67.7% for A. flavus, 64.3% for F. solani, and 60.7% for A. niger [136]. The MIC values of CuNPs (8 nm) estimated by agar dilution method were 40 mg/L for P. chrysogenum, 60 mg/L for A. alternata, 60 mg/L for F. solani, and 80 mg/L for A. flavus and also MIC values observed using XTT reduction assay ranged from 40 to 80 mg/L [137]. CuNPs applied at low concentrations stimulated the growth of the plant pathogenic fungi Botrytis fabae, F. oxysporum f. sp. ciceris, F. oxysporum f. sp. melonis, A. alternata, and Pseudomonas syringae and showed synergistic inhibitory effect with bulk copper such as Cu2(OH)3Cl on mycelial growth and sporulation of A. alternata [138]. The sensitivity of plant pathogenic fungi against biogenic CuNPs prepared using citron juice (Citrus medica L.) with particle sizes ranging from 10 to 60 nm decreased as follows: F. culmorum > F. oxysporum > F. graminearum [139].

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Flower-shaped CuNPs with particle sizes 100e500 nm and zeta potential of 35 mV showed notable antifungal activity against the plant pathogenic fungi A. niger, F. moniliforme, F. culmorum, F. oxysporum, and Fusarium tricinctum, which decreased as follows: A. niger > F. moniliforme > F. oxysporum > F. culmorum, and in combination with commercial antifungal agent (ketoconazole) enhanced its antifungal activity [140]. Copper nano-/microparticles prepared in the presence of 2,20 ,200 ,2000 (ethane-1,2-diylbis(azanetriyl))tetraacetohydrazide as a capping and reducing agent under hydrothermal conditions were found to be more effective than Bordeaux mixture in killing phytopathogenic fungi in vitro, but they did not exhibit fungicidal effect on the nonphytopathogenic fungus, Penicillium [141]. CuNPs synthesized by chemical reduction of Cu2þ in the presence of cetyltrimethylammonium bromide (CTAB) and isopropyl alcohol with particle sizes 3e10 nm were found to be coated by CTAB and showed notable antifungal activity against Phoma destructiva, C. lunata, A. alternata, and F. oxysporum, suggesting that they could be used as antifungal agents in agriculture to control the plant pathogenic fungi [142]. Spherical CuNPs synthesized by chemical reduction method with a support of CTAB reductive agent with particle sizes 20e50 nm applied at a dose 450 ppm in 9-day incubation showed 93.98% of growth inhibition of Fusarium sp. [143]. The zone of inhibition observed at exposure to stable CuNPs synthesized using CTAB was reported to be 25 mm for Fusarium equiseti, 20 mm for F. oxysporum, and 19 mm for F. culmorum [144]. Kasana et al. [145] summarized the findings related to the biological synthesis of CuNPs and CuO NPs using plant extracts and microorganisms and their antibacterial and antifungal activity, as well as the impact of these NPs on crops and pathogenic microorganisms. Small spherical CuO NPs (5e10 nm or with average size of 15 nm) were synthesized by using leaf extract or latex produced by plants, while CuNPs of various sizes (5e280 nm) were biosynthesized using extracts prepared from plants (e.g., Syzygium aromaticum, Vitis vinifera, Aloe vera, Cassia alata, C. medica) or using microorganisms (both bacteria and fungi). The Cu-based NPs were reported to show antifungal activity against the pathogenic fungi F. culmorum, F. oxysporum, F. graminearum, and Phytophthora infestans. Good antifungal activity against plant fungal pathogens F. culmorum and A. niger also exhibited spherical CuO NPs with mean diameter of 28  4 nm biosynthesized using Eichhornia crassipes [146]. Flower-shaped CuO nanostructures acting as an effective antifungal agent against pathogenic fungi A. niger, A. flavus, Penicillium notatum, and A. alternata were reported previously by Mageshwari et Sathyamoorthy [147]. Spherical CuO NPs with particle sizes 30  2 nm ecofriendly synthesized using Cissus quadrangularis plant extract exhibited better antifungal activity against A. flavus (81% and 85% inhibition at 500 and 1000 ppm, respectively) and A. niger (83% and 86% inhibition at 500

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and 1000 ppm, respectively) compared with standard carbendazim (methyl 1H-benzimidazol-2-ylcarbamate) [148]. Copper sulfide nanoaquaformulations showed multifold efficacy against A. alternata, Drechslera oryzae, and C. lunata in comparison to standard, and in vivo seed treatment with citrate capped copper sulfide nanoformulation on discolored paddy seeds (7 mg/mL for 2 h) considerably reduced seed rot and seedling blight and exhibited beneficial effect on germination and growth parameters [149].

3.4 Zinc nanoparticles Comparison of antifungal properties of Zn compounds (ZnO NPs, ZnO, ZnSO4, and Zn(ClO4)2) against toxigenic fungi F. graminearum, P. citrinum, and A. flavus and their effects on the production of corresponding mycotoxins deoxynivalenol, aflatoxins, and citrinin showed that ZnSO4 and Zn(ClO4)2 completely inhibited the fungal growth and their ability to produce mycotoxins, and treatment with Zn compounds resulted in ROS production, reduction of the conidia production of all fungi, and morphological alterations leading to hyphae damage [150]. The wheat plants that were inoculated with F. graminearum and treated with ZnSO4 and ZnO NPs (100 mM) onto spikelets at the anthesis stage were characterized with reduced number of colonies per gram compared with the control, and the toxin deoxynivalenol was reduced to nondetected levels in the treated group. Antifungal activity of ZnNPs and ZnO NPs against fungi such as Penicillium and Mucor species was also reported by Swain et al. [151]. ZnO NPs with sizes of 70  15 nm applied at a dose >3 mmol/L pronouncedly inhibited P. expansum, and they prevented the development of conidiophores and conidia, which eventually led to the death of fungal hyphae [152]. ZnO NPs strongly reduced F. graminearum and toxin formation in the grains at low concentration, and the treatment did not affect adversely the wheat grains [153]. The investigation of impact of ZnO NPs on the growth and mycotoxins production by mycotoxigenic molds A. flavus, A. ochraceus, and A. niger showed inhibition of the growth of aflatoxigenic molds and aflatoxins production at treatment with 8 mg/mL ZnO NPs, while ochratoxin A and fumonisin B1 producing molds and mycotoxins production were inhibited at 10 mg/mL ZnO NPs in tested medium, whereby the damage and rupture of fungal cell wall were detected in the area of surrounding growth media [154]. Decelis et al. [155] assessed the antifungal efficiency of filters coated with ZnO NPs using 0.012 and 0.12 M ZnO NPs to coat two types of filters (meltblown and needle-punched) for three different periods (0.5, 5, and 50 min) and R. stolonifer and P. expansum isolated from spoiled pears as test organisms. P. expansum was the more sensitive organism showing inhibition at 0.012 M at only 0.5 min coating time on the needle-punched filter, and prolongation of the coating time resulted in the more effective inhibition of both organisms.

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The coating showed less effect on Young’s modulus (measuring the stiffness of a solid material) of the needle-punched filters compared with melt-blown filters. Hexagonal wurtzite ZnO NPs prepared by emulsion (spherical NPs with sizes 60e250 nm), microemulsion (flower-like NPs with 20 nm in average thickness and 600 nm in average diameter), and direct precipitation (polygonalflake NPs with mean thickness of 50  2 nm and width ranging from 100 to 800 nm) were able to change the morphology of mycetes and inhibit the growth and the reproduction of Penicillium, Mucor, and Myxomycetes, ZnO NPs prepared by microemulsion method being the most effective [156]. Spherical and hexagonal ZnO NPs with particle sizes 27  5 nm and 84  2 nm, respectively, biosynthesized using leaf extract of Parthenium hysterophorus L. exhibited the size-dependent antifungal activity against plant fungal pathogens, smaller particles being more effective and highest zone of inhibition being estimated with spherical ZnO NPs applied at a dose of 50 mg/ mL in A. flavus (24.66  0.57 mm), while the lowest one in F. culmorum showing a diameter of zone of inhibition 14  0.57 mm [157]. Spherical ZnO NPs with mean particle size of 12  3 nm and of crystalline nature prepared using aqueous extract of Lantana aculeata L. leaf tested on antifungal activity showed, at a dose 100 mg/mL, that the maximum zone of inhibition in A. flavus and F. oxysporum was 21  1.0 mm and 19  1.0 mm, respectively [158]. Also spherical ZnO NPs prepared using reproducible bacteria Aeromonas hydrophila with hexagonal unit cell at crystalline level and mean size of 57.72 nm applied at a dose 25 mg/mL showed the maximum zone of inhibition in A. flavus (19  1.0 mm), and the estimated MIC values of these ZnO NPs for A. flavus and A. niger were 2.9  0.01 and 2.0  0.04 mg/mL, respectively [159]. Crystallite ZnO nano falcates of sickle shape synthesized from Prunus cerasifera pomological extract, exhibiting 4.93 nm average size loaded on discs and applied at a dose of 10 mL in standard KirbyeBauer disc diffusion assay, effectively inhibited pathogenic fungi with following zones of inhibition: 17.07 mm for A. niger, 20.05 mm for A. flavus, 18.05 mm for A. fumigatus, 15.01 mm for A. terreus, 22.07 mm for P. chrysogenum, 21.01 mm for F. solani, and 24.02 mm for Lasiodiplodia theobromae [160]. ZnO NPs fabricated on the surface of bamboo timber by a simple lowtemperature wet chemical method, which were immobilized on the bamboo timber surface through electrostatic and hydrogen bonding interactions, contributed to better resistance of bamboo timber against A. niger and P. citrinum [161]. ZnO NPs applied at concentration >6 mM reduced mycelium growth diameters of P. expansum, A. alternata, B. cinerea and R. stolonifer on potato dextrose agar plates, and treatment with ZnO NPs caused clear morphological aberrations in the fungal structures, whereas cotreatment with ethylenediaminetetraacetic acid reduced the antifungal activity of ZnO NPs [162]. Reinprecht et al. [163] reported that ZnO NPs added into melamine-ureaformaldehyde glue (2e24 wt%) contributed to higher biological resistance of

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laboratory-produced one-layer particleboards against the molds P. brevicompactum and A. niger by up to 50%e63%, causing a decrease of fungal growth intensities on the top surfaces of treated particleboards. Melamine-formaldehyde resin designed for the white decor paper impregnation modified with ZnO NPs (0.1e1.0 wt%) and pressed onto particleboards increased the anti-mold resistance of the intentionally contaminated laminated surfaces against A. niger and P. brevicompactum atmost by approximately 50%, whereby the presence of ZnO NPs practically did not affect the resistance of the laminated surfaces toward aggressive chemicals and dry heat (180  C), but abrasion resistance decreased atmost by about 17% [164]. Inclusion of the ZnO NPs in a mung bean broth agar and in sand resulted in considerable inhibition of F. graminearum growth, whereby nanoscale particles were more efficient than the microscale ones, and the inhibitory effect was connected with soluble Zn released from NPs [165]. Polyvinyl chlorideebased films coated with ZnO NPs (0.2 or 0.075 g/L) that showed antibacterial activity against both Gram-positive (S. aureus) and Gram-negative (E. coli) bacteria were inactive against pathogenic fungi A. flavus and P. citrinum [166]. Films with dispersed sphere-like and flowerlike ZnO NPs showed notably higher antifungal activity against A. flavus and C. albicans than the films containing rod-, sheet-, or needle-like ZnO NPs, which could be connected with higher specific surface area of these NPs (27.64 and 15.07 m2/g, respectively), enabling easier to contact and adsorb the fungi compared to sheet-like (11.369 m2/g), needle-like (9.909 m2/g), and short rod-like (9.47 m2/g) ZnO NPs. Treatment with films containing spherelike ZnO and flower-like ZnO NPs caused disruption of fungi, in which released Zn2þ ions were present and the small sizes of sphere-like ZnO NPs contributed to higher release of Zn2þ ions, which accumulated and adhered to the surface of cell membrane resulting in the denaturation of membrane proteins, modification of membrane permeability, and destroying the fungal cell membrane structure. However, the strong antifungal activity of films containing flower-like ZnO NPs could be attributed to their photocatalytic activity because under light irradiation, the electronehole pairs are generated that could react with OH
on the surface, generating ROS ( OH, O2, and H2O2), and negatively charged radicals OH
and O2 could not penetrate into the cell membrane and remain in direct contact with the outer surface of fungi causing strong damage to the cell membrane [167]. Four different NPs (mix metallic NPs containing several elements including Ag, Cu, and TiO2 NPs; AgNPs, AuNPs, and ZnO NPs) were tested for their antifungal activities against the mycotoxin-producing mold strains A. flavus and A. fumigatus. The MIC value of AgNPs determined in broth media for A. fumigatus was 10 mg/mL, whereas MIC values of ZnO NPs and metallic NPs for both strains were 20 and 100 mg/mL, respectively. Under illumination with ultraviolet light, TiO2 present in mix metallic NPs generates highly toxic free radicals. It is important to note that also Ag and Cu present in 







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these NPs contribute to ROS generation. The paint or coating formulations prepared using metallic and ZnO NPs could reduce the growth of molds on surfaces, specifically in humid and nonventilated environments with very few potential health concerns such as cytotoxicity and immunological responses [168]. Blend films of ZnO and AgNPs with spherical and granular morphology uniformly distributed within CS polymer were reported to have strong antifungal activity against Aspergillus sp [169]. Antimicrobial paints based on the aqueous acrylic dispersion and ZnO and TiO2 NPs were found to be effective in photocatalytic and hygienic coatings [170]. The suspensions of Ca(OH)2 particles, mixed with ZnO NPs, exhibited antifungal activity against Penicillium oxalicum and A. niger both in the dark and under illumination, and the coated nanosystems based on Ca(OH)2
50% ZnO and pure zincite nanoparticulate films were found to have promising performance on low porosity limestone used in construction and as materials for the restoration of historic buildings because they showed good antifungal properties against abovementioned fungi under simulated photoperiod conditions [171]. Zn-doped MgO (Mg1-xZnxO, x ¼ 0.096) NPs obtained by solegel method as antifungal coatings on dolomitic and calcitic limestones were investigated to develop effective protective coatings for stone heritage, and it was found that compared to the MgO and ZnO nanomaterials, the Mg1-xZnxO NPs showed higher photocatalytic activity and stronger antifungal activity against A. niger, P. oxalicum, Paraconiothyrium sp., and Pestalotiopsis maculans that are especially active in the bioweathering of stone, which could be attributed to the formation of crystal defects by the incorporation of Zn into MgO. Zn-doped MgO NPs applied as protective coatings on calcareous stones inhibited the epilithic and endolithic colonization of A. niger and P. oxalicum in both lithotypes, and they could be considered as highly efficient antifungal protection for calcareous stone heritage [172]. Evaluation of antifungal potential of ZnO and Fe2O3 NPs against A. ochraceus and A. niger strains showed that the diameters of inhibition zones induced by NPs for nonochratoxigenic strains were larger than that of ochratoxigenic strains and showed an increase with increasing concentration in the medium. The ochratoxin A production by ochratoxigenic strains in liquid medium or on yellow corn was significantly diminished simultaneously with the decline parameters in colony count of the treated ochratoxigenic strains [173]. The aflatoxin B1 production by aflatoxigenic strains of A. flavus in yeast sucrose agar or on yellow corn was also considerably diminished along with the decline parameters in colony count of the aflatoxigenic strains treated with ZnO and Fe2O3 NPs. However, it was found that antimycotoxins effect of these metal NPs was limited to their use as feed additives during manufacture and before exposure of feeds to fungal contamination [174]. Cerium-doped flower-shaped ZnO crystallites, in which increasing levels of the Ce doping element (>0.8%) result in decreased optical band gap (3.06 eV), showed enhanced antifungal activity against A. flavus (80%) and

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C. albicans (75%) under visible light sources [175]. Pure and Nd3þ (0.5e9 mol%)-doped ZnO nanophosphor superstructures in the nanolevel synthesized using A. vera gel as a biotemplate/surfactant via ultrasound method effectively inhibited the growth of A. alternata and F. oxysporum that were cultured on Sabouraud Dextrose Agar, and with an increase of the dose of ZnO:Nd3þ(1 mol%) from 100 to 700 mg/mL, the percentage of inhibition of colony growth diameters after 7 days of incubation increased from 11.26% to 92.95% for F. oxysporum and from 15.06% to 91.77% for A. alternata. It was assumed that ZnO:Nd3þ superstructures interwind the pores, resulting in the local perturbation of fungal cell membrane and in the leakage of electrolytes, and locally damage the cell membrane due to mechanical wrapping interactions between pathogens and the NPs, causing cell lysis. Such biocompatible ZnO:Nd3þ nanostructures also possess inhibitory activity against more multiresistant bacterial and fungal phytopathogens [176].

3.5 TiO2 nanoparticles Investigation of antifungal properties of anatase and rutile crystallites isolated from commercial titania P25 photocatalyst on mycelium growth of A. versicolor, A. flavus, S. chartarum, P. chrysogenum, and Aspergillus melleus isolated from air and from moisture condensed on walls in the dark and under indoor light showed that antifungal activities were affected not only by fungal structure but also by aggregation of TiO2 NPs and impurities adsorbed on their surface, whereby sporulation and mycotoxin generation were strongly inhibited by light and presence of TiO2 NPs [177]. Although the effect of TiO2 NPs on growth of toxigenic strains of A. flavus was lower than that against E. coli and S. aureus, with the increase in TiO2 NPs concentration and time of irradiation, a decrease in population of A. flavus was pronounced. Relative resistance of A. flavus to TiO2 NPs could be connected with the composition of its cell wall consisting of long carbohydrate layers, long chain of polysaccharides along with glycoproteins, and lipids; however, ROS generated during the photocatalytic process could overcome this resistance [178]. Visible lighteactivated palladium-modified nitrogen-doped TiO2 NPs photocatalyst was found to be a highly effective in photocatalytic disinfection of F. graminearum macroconidia under visible light illumination because NPs of opposite surface charges than F. graminearum macroconidium could be effectively adsorbed on the surface of macroconidium, contributing to photocatalytic disinfection of these macroconidia, which are exposed to the attack of ROS causing their cell wall/membrane damage [179].

3.6 Iron nanoparticles Fe2O3 NPs biosynthesized using tannic acid as reducing and capping agent with particle sizes ranging from 10 to 30 nm showed antifungal activity and inhibited spore germination, whereby zone of inhibition at treatment with

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Fe2O3 NPs decreased in following order: P. chrysogenum (28.67 mm) > A. niger (26.33 mm) > A. alternata (21.33 mm); the activity index at 0.5 mg/ mL was 0.84 for P. chrysogenum, 0.77 for A. niger, and 0.62 for A. alternata; and estimated MIC values of Fe2O3 NPs were 0.016 mg/mL for both P. chrysogenum and A. niger and 0.032 mg/mL for A. alternata [180]. Iron NP films used inside polyethylene/polyamide packages effectively inhibited the growth of A. flavus and also avoided the spore formation suggesting their potential to be used on food packaged to suppress fungal growth and thus contribute to the food safety. Considerable inhibition of colonies growing was connected with the reduction of O2 concentration inside the packages promoted by iron NPs [181]. MgO, FeO, and ZnO NPs notably inhibited the germination of spores of P. notatum, A. niger, and Nigrospora oryzae (Berk) in vitro, and their effectiveness decreased as follows: MgO NPs > FeO NPs > ZnO NPs [182].

4. Nonmetal nanoparticles The antifungal activity of clotrimazole against the five most common fungal species affecting paper collections decreased in the following order: C. globosum < C. cladosporioides < P. chrysogenum < A. niger < Penicillium corylophilum, and when applied with deacidifying agent Ca(OH)2 NPs, a multipurpose formulation was achieved suitable to protect the paper from acidification and loss of folding endurance in the long term that could be used as a nonaqueous alternative treatment for paper affected by fungi [183]. Curcumin NPs with particle sizes 2e40 nm that were freely dispersible in water in the absence of any surfactants showed much better antibacterial activity against S. aureus, Bacillus subtilis, E. coli, and Pseudomonas aeruginosa (being more pronounced against Gram-positive bacteria than Gram-negative bacteria) than antifungal activity against P. notatum and A. niger [184]. Antifungal effect of curcumin-loaded cylindrical and ultrafine electrospun zein nanofibers (<350 nm in diameter) against P. expansum was found to be twofold higher than that against B. cinerea, and visual inspections on uncoated apples and coated with this nanoformulation performed after 6 days of storage period at 23  C and 75% humidity revealed almost 50% reduction in lesion diameter measured on coated apples infected with P. expansum [185].

5. Carbon-based nanoparticles Graphene (GR), graphene oxide (GO), and reduced graphene oxide (rGO) elicit toxic effects both in vitro and in vivo, whereas surface modifications can significantly reduce their toxic interactions with living systems [186]. Findings related to nanotoxicity of GR and GO was summarized by Seabra et al. [187]. As main mechanism for toxicity of GR-family nanomaterials, generation of

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ROS in target cells could be considered, although the extremely high hydrophobic surface area of some of these nanomaterials may also lead to significant interactions with membrane lipids resulting in direct physical toxicity or adsorption of biological molecules [188]. For example, GR nanosheets were found to penetrate into and extract large amounts of phospholipids from the cell membranes of E. coli because of the strong dispersion interactions between GR and lipid molecules [189]. Recent findings related to antimicrobial effects of GR-based materials were summarized by Lukowiak et al. [190]. GO intertwinds fungal spores with a wide range of aggregated GO sheets, causing the local perturbation of their cell membrane and the leakage of electrolytes of fungal spores. GO repressed 80% macroconidia germination of F. graminearum and F. oxysporum along with partial cell swelling and lysis at 500 mg/mL. It could be assumed that GO interacts with the pathogens by mechanically wrapping and locally damaging the cell membrane and finally causing cell lysis, and it could be effective also against more multiresistant fungal phytopathogens [191]. rGO nanosheets inhibited the mycelial growth of F. oxysporum, A. niger, and Aspergillus oryzae showing IC50 values of 50, 100, and 100 mg/ mL, respectively, and the inhibitory activity of rGO could be connected with its sharp edges [192]. Kovac et al. [193] observed that at environmentally plausible concentrations of fullerene C60 (10e100 ng/mL), the growth of A. flavus was not strongly inhibited, but C60 NPs at doses of 10 and 100 ng/L showed antiaflatoxigenic effects, while application of 50 ng/mL enhanced aflatoxin production. It was found that 10 ng/mL fullerene C60 exhibited antioxidative action and reduced aflatoxin B1 production within fungal cells, while at a dose of 50 ng/mL prooxidative effects of C60 NPs surpassed cellular defences, which was reflected in enhanced aflatoxin B1 production, and at the highest tested C60 concentration 100 ng/L likely cytotoxic effects of C60 contributed to the inhibition of aflatoxin B1 production. Application of fullerol (C60(OH)24) NPs caused only slight reduction of mycelial biomass weight of aflatoxigenic strain of A. flavus (NRRL 3251) during 168 h of incubation in a liquid culture medium, while notably reduced aflatoxin concentration in media, and it was found that fullerol NPs hormetically reduced oxidative stress within fungal cells, in turn suppressing aflatoxin production [194]. Wang et al. [195] reported that antifungal activity of carbon-based nanomaterials against F. graminearum and Fusarium poae decreased in following order: single-walled carbon nanotubes (SWCNTs) > multi-walled carbon nanotubes (MWCNTs) > GO > rGO > fullerene (C60) > activated carbon, showing no significant antifungal activity; on targeting the spores by carbon-based nanomaterials deposition on the surface of the spores, inhibition of water uptake and induction of plasmolysis is accomplished.

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6. Conclusions Fungi are simple eukaryotic organisms that have colonized diverse environments around the planet. They are ubiquitous in nature and vital for recycling of nutrients contained in organic matter. The vast majority of the known fungal species are saprophytes, but some of them can attack plants, animals, and human. Primary pathogens can establish infections in normal hosts. Opportunistic pathogens cause disease in individuals with compromised host defense mechanisms. The primary pathogens have relatively well-defined geographic ranges; the opportunistic fungi are ubiquitous. Fungi, whether primary or opportunistic pathogens, can damage the affected organism by attack of living tissue or production of mycotoxins, or they can cause allergies. Especially mycotoxins are dangerous as they are not “visible” (they are detectable by special equipment), and they are highly toxic not only for plants but especially in high doses or at long-term exposure for animals and humans, as mentioned above. Therefore, detection by application of various sensors and especially the fight against mycotoxin producers and perhaps even the destruction of these mycotoxins is very important. Nanoscale science and nanotechnology have unambiguously demonstrated to have a great potential in providing novel and improved solutions. As it was discussed in this chapter, NPs/nanomaterials/nanoformulations provide enormous potential for their applications against diverse fungal species in medicine, agriculture, and food industry, and thus biologically effective antifungal nanomaterials can be used in improved protection of plants, agricultural crops, foodstuffs, and human health. On the other hand, increased nanosize-based toxicity effects (e.g., surface reactivity of NPs) of new materials are not selective on fungal cells, but frequently they can demonstrate unspecified toxicity also against living organisms, which they should protect. These new nanoscale materials should be used advisedly and especially after in-depth investigation of cytotoxicity. Thus, an increased attention must be devoted to the impact of risk factors associated with their usage on the environment and possible adverse/ hazardous effects on all organisms and humans.

Acknowledgments This study was supported by the Slovak Research and Development Agency (projects APVV-17-0373 and APVV-17-0318) and by the Ministry of Education of the Czech Republic (LO1305).

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