Nanotechnological Applications of Fusarium oxysporum: Comparison
Please note this is a comparison between Version 1 by Sabrin R. M. Ibrahim and Version 2 by Camila Xu.

Fusarium oxysporum is the most encountered and economically important species of this genus. It includes pathogenic (plant, human, and animal) and non-pathogenic strains that even possess bio-control activity against fungal pests and some insects. It is one of the soil-borne pathogens that causes vascular wilt on many plants, which is characterized by various symptoms, including leaf epinasty, vascular browning, progressive wilting, defoliation, stunting, and plant death. Its species complex consists of several formae speciales (f. sp.) that collectively infect more than one hundred hosts, leading to serious losses in crops such as tomato, melon, banana, and cotton.

  • Fusarium oxysporum
  • fungi
  • metabolites
  • bioactivities

1. Introduction

Fungi are eukaryotic microorganisms that settled mostly in all kinds of environments and have fundamental roles in maintaining the environmental balance [1][2][1,2]. It has been stated that only about 5% of 2.2 to 3.8 million different fungal species on earth have been taxonomically characterized [3][4][3,4]. Fungi have been considered as one of the wealthiest pools of natural metabolites with unique structural features and biodiversity that have a remarkable role in developing new drugs [1][2][3][5][6][7][8][9][10][1,2,3,5,6,7,8,9,10]. Some fungal metabolites are also highly toxic such as Aspergillus mycotoxin and aflatoxin B1, which affect human health when occurring in food products [8][9][11][8,9,11]. Therefore, it is important to unravel the metabolites of fungal species to prevent health risks, as well as to identify new potential bioactive compounds. Fusarium is a genus of filamentous fungi that includes many mycotoxin producers, agronomically important plant pathogens, and opportunistic human pathogens [12]. Its species are a widespread cosmopolitan group of fungi that are found in various habitats such as water, soil, or associated with plants [13][14][13,14]. They commonly colonize subterranean and aerial plant parts, either as primary or secondary invaders [15]. Many Fusarium species are spread out pathogens on crops in temperate and semi-tropical regions that produce a variety of mycotoxins, causing a reduction in yield and quality of crops, as well as animal and human health risks [16]. On the other hand, some species have the potential capacity to produce a great number of metabolites with remarkable chemical diversity and significant bioactivities [11][17][18][19][20][21][22][23][24][25][26][11,17,18,19,20,21,22,23,24,25,26]. Fusarium oxysporum is the most encountered and economically important species of this genus. It includes pathogenic (plant, human, and animal) and non-pathogenic strains that even possess bio-control activity against fungal pests and some insects [27]. It is one of the soil-borne pathogens that causes vascular wilt on many plants, which is characterized by various symptoms, including leaf epinasty, vascular browning, progressive wilting, defoliation, stunting, and plant death [28]. Its species complex consists of several formae speciales (f. sp.) that collectively infect more than one hundred hosts, leading to serious losses in crops such as tomato, melon, banana, and cotton [29]. In humans, F. oxysporum causes invasive infections in immuno-compromised patients and it is commonly found in onychomycosis [30][31][30,31]. Many studies revealed that F. oxysporum showed a remarkable capacity to yield diverse classes of secondary metabolites such as alkaloids, jasmonates, anthranilates, cyclic peptides, cyclic depsipeptides, xanthones, quinones, and terpenoids with various activities such as phytotoxicity, antimicrobial, cytotoxicity, insecticidal, antioxidant, and antiangiogenic. Additionally, F. oxysporum possessed significant industrial and biotechnological values as a wealthy source of diverse enzymes with wide applications such as cutinases, nitrilases, glycoside hydrolases (e.g., fucosidase, α-galactopyranosidases, and xylanases), fructosyl amino acid oxidase, laccases, lipoxygenase, nitric oxide reductase, decarboxylases, keratinase, phospholipase B, and triosephosphate isomerase [32][33][34][35][36][37][38][39][40][41][42][32,33,34,35,36,37,38,39,40,41,42]. Further, F. oxysporum is widely employed for the synthesis of different types of metal nanoparticles that could have various biotechnological, pharmaceutical, industrial, and medicinal applications [43][44][45][46][47][48][49][50][51][52][53][54][55][43,44,45,46,47,48,49,50,51,52,53,54,55]. The intensive literature search revealed the lack of review articles that deal with F. oxysporum particularly the bright side of this economically valuable fungus.

2. Nanotechnological Applications

Nanotechnology holds promise in the medicine, agriculture, and pharmaceutical industries [56][112]. Natural nanostructures have gained more attention due to the wide spectrum of bioactivities and fewer animals, humans, and environmental toxicity. The microbial synthesis of nanoparticles is an approach of green chemistry that combines both nanotechnology and microbial biotechnology [57][113]. Metals nanoparticles are increasingly used in various biotechnological, pharmaceutical, and medicinal applications, including drug delivery, gene transfer, insect-pests management in agriculture, and bioelectronics devices fabrication, as well as antibacterial agents towards many pathogenic bacteria, including the MDR (multidrug-resistant) strains [58][59][60][114,115,116].

2.1. Metal Nanoparticles

Several studies reported the synthesis and characterization of metal nanoparticles (NPs) using F. oxysporum, as well as their bioactivities. Additionally, some studies dealt with optimizing the conditions for the synthesis of NPs by F. oxysporum, including temperature, media, pH, salt concentration, light intensity, the volume of filtrate, and biomass quantity [44][47][50][51][54][55][44,47,50,51,54,55]. Marcato et al., synthesized AgNPs (silver nanoparticles) using F. oxysporum. The incorporation of these NPs in cotton cloth was found to exhibit a bactericidal effect towards S. aureus, leading to its sterilization [50]. Ishida et al., synthesized AgNPs using F. oxysporum aqueous extract that showed significant antifungal potential towards Cryptococcus and Candida (MIC values ≤ 1.68 µg/mL) [51]. Moreover, it was found that the biosynthesized AgNPs by two F. oxysporum isolates exhibited higher antibacterial potential towards human-pathogenic bacteria; E. coli, Proteus vulgaris, S. aureus, and K. pneumonia than the used antibiotics. These AgNPs could be favorable antibacterial agents, especially towards MDR bacteria [44]. Ahmed et al., synthesized AgNPs using F. oxysporum, which inhibited some MDR species of Staphylococcus and Enterobacteriaceae (conc. 50% v/v), as well as Candida krusei and C. albicans, suggesting that they might be potential alternatives to antibiotics [46]. The in-silico and in-vitro studies demonstrated the immense antibacterial potential of F. oxysporum’s AgNPs against P. aeruginosa and E. coli [45]. The AgNPs synthesized using nitrate reductase purified from F. oxysporum IRAN-31C showed potent antimicrobial potential towards a wide array of human pathogenic bacteria and fungi in the disk diffusion method [61][117]. A study by Ballottin et al., revealed that the cotton fibers impregnated with biogenic AgNPs synthesized from F. oxysporum filtrate solution possessed potent antimicrobial potential even after repeated mechanical washing cycles. This might highlight the potential use of biogenic AgNPs as an antiseptic in textiles for medical applications [62][118].
Moreover, a study by Hamedi et al., revealed that the existence of ammonium lowered the productivity of AgNPs using F. oxysporum cell-free filtrate and prohibited the nitrate reductase enzyme secretion [63][119]. Longhi et al., reported that the combination of AgNPs synthesized using F. oxysporum with FLC (fluconazole) reduced the MIC of FLC around 16 to 64 times towards planktonic cells of C. albicans and induced a significant dose-dependent inhibition of both initial and mature biofilms of FLC-resistant C. albicans. Therefore, these AgNPs could represent a new strategy for treating FLC-resistant C. albicans infections [49]. Additionally, the combination of simvastatin with these AgNPs demonstrated antibacterial activity towards E. coli-producing ESBL (extended-spectrum β-lactamase) and MRSA (methicillin-resistant S. aureus). This could be a great future alternative in bacterial infection control, where smaller doses of these AgNPs are required with the same antibacterial activity [64][120]. Besides, its combination with polymyxin B showed a 16-fold reduction of the MIC of polymyxin B and decreased carbapenem-resistant Acinetobacter baumannii viability with additive and synergic effects, as well as significantly reduced cytotoxicity towards mammalian Vero cells, indicating its pharmacological safety [65][121]. The AgNPs synthesized with F. oxysporum f.sp. pisi were found to have moderate adulticidal potential on Culex quinquefasciatus (vector of filariasis) (LC50 0.4, LC99 4.8, and LC90 4 μL/cm2) after 24 h exposure [66][122]. The synthesized AgNPs using F. oxysporum aqueous extract had anticancer potential towards MCF7 (IC50 14 µg/mL) that was characterized using CLSM (confocal laser scanning microscopic) technique [67][123]. Bawskar et al. stated that the biosynthesized AgNPs using F. oxysporum possessed more potent antibacterial potential towards E. coli and S. aureus than chemo-synthesized AgNPs that may be due to the protein capping and their mode of entry into the bacterial cell, which encouraged biosynthetic method over the chemosynthetic one in AgNPs synthesis [68][124]. Two types of AgNPs, phyto-synthesized and myco-synthesized NPs were biosynthesized by AgNO3 reduction with Azadirachta indica extract and F. oxysporum cell filtrate, respectively that possessed lower cytotoxic potential on C26 and HaCaT cell lines as compared with citrate coated AgNPs [69][125]. Santos et al. proved that F. oxysporum-biosynthesized AgNPs without pluronic F68 (stabilizing agent) had high antibacterial potential towards E. coli, P. aeruginosa, and S. aureus. On the contrary, chemo-synthesized AgNPs exhibited synergism in antibacterial activity in the presence of pluronic F68 [70][126]. Streptococcus agalactiae is an important cause of invasive diseases, mainly in newborns, pregnant women, and elderly individuals [71][127]. The combination of F. oxysporum-produced AgNPs (AgNPbio) and eugenol led to a remarkable synergistic effect and significant reduction of the MIC values of both eugenol and AgNPbio towards planktonic cells of S. agalactiae [71][127]. Thakker et al., reported the synthesis of GNPs (gold nanoparticles) using F. oxysporum f. sp. cubense JT1 that showed antibacterial potential versus Pseudomonas sp. [72][128]. Moreover, the conjugated GNPs with tetracycline demonstrated powerful antibacterial activity against Gram-negative and -positive bacteria in comparison to tetracycline and free GNPs. Therefore, tetracycline conjugation with these GNPs enhanced the antibacterial potential, which may have significant therapeutic applications [73][129]. Yahyaei and Pourali studied the conjugation of GNPs with chemotherapeutic agents such as paclitaxel, tamoxifen, and capecitabine. Moreover, the cytotoxic effect of conjugated GNPs was assessed towards MCF7 and AGS cell lines, using MTT assay. Unlike the paclitaxel conjugated GNPs, the tamoxifen and capecitabine conjugated GNPs revealed no toxic effects due to their low half-lives and deactivation [74][130]. Further, Syed and Ahmad reported the synthesis of stable extracellular platinum nanoparticles, using F. oxysporum [75][131]. CdSe (cadmium/selenium) quantum dots are often used in industry as fluorescent materials. Kumar et al., and Yamaguchi et al., reported the synthesis of highly luminescent CdSe quantum dots by F. oxysporum [76][77][132,133]. In 2013, Syed and Ahmad synthesized highly fluorescent CdTe quantum dots using F. oxysporum at ambient conditions by the reaction with a mixture of TeCl4 and CdCl2. These nanoparticles exhibited antibacterial potential towards Gram-negative and -positive bacteria [53]. Riddin et al., analyzed the biosynthesized platinum (Pt) nanoparticles by F. oxysporum f. sp. lycopersici at both intercellular and extracellular levels. It was found that only the extracellular nanoparticle production was proved to be statistically significant with a yield of 4.85 mg/L [78][134].

2.2. Metal Sulfide Nanoparticles

In addition, Q-state CdS NPs were biosynthesized by the reaction of aqueous CdSO4 solution with F. oxysporum [79][135]. The chemically-synthesized CdSQDs inhibited E. coli cell proliferation in a dose-dependent manner, unlike the biogenic CdSQDs synthesized by F. oxysporum f. sp. lycopersici, which showed an antibacterial potential only at high concentration. Additionally, only the biogenic CdSQDs showed no inhibition on seed germination after incubation of biogenic and chemical CdSQDs with Lactuca sativa seeds [43]. Bi2S3 (bismuth sulfide) NPs have significantly varied applications, including photodiode arrays, photovoltaic materials, and bio-imaging. Uddin et al., synthesized a highly fluorescent, natural protein capped Bi2S3NPs by subjecting F. oxysporum to bismuth nitrate penta-hydrate, along with sodium sulfite under ambient conditions of pressure, temperature, and pH. It was found that they were fundamentally much more fluorescent than fluorophores (toxic fluorescent chemical compounds), which are largely utilized in immunohistochemistry, imaging, and biochemistry [48].

2.3. Metal Oxide Nanoparticles

It was reported that F. oxysporum might have vast commercial implications in low-cost, room-temperature, ecofriendly syntheses of technologically significant oxide nanomaterials from available potentially cheap naturally raw materials [80][136]. F. oxysporum rapidly bio-transformed the naturally occurring amorphous biosilica in rice husk into crystalline silica NPs. This could lead to an economically viable and energy-conserving green approach toward the large-scale synthesis of oxide nanomaterials [80][136]. Moreover, the mesophilic F. oxysporum bioleached Fly-ash at ambient conditions produced highly stable, crystalline, fluorescent, water-soluble, and protein-capped silica nanoparticles [52]. It was found that F. oxysporum enriched zirconia in zircon sand by a process of selective extracellular bioleaching of silica nanoparticles. It was proposed that the fungal enzymes specifically hydrolyzed the silicates in the sand to form silicic acid, which on condensation by certain other fungal enzymes resulted in silica nanoparticles synthesis at room temperature [80][136]. A water dispersible and thermo-stable Ag/Ag2O NPs were produced from silver oxide micro-powder using F. oxysporum. These Ag/Ag2O NPs may become a potential candidate for enzyme-free glucose determination and exhibited catalytic potency for MB (methylene blue) degradation in presence of NaBH4 (reducing agent). Additionally, they showed an excellent antimicrobial potential against A. niger and B. subtilis [81][137].
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