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Wijayawardene, N.N.; Boonyuen, N.; Ranaweera, C.B.; De Zoysa, H.K.S.; Padmathilake, R.E.; Nifla, F.; Dai, D.; Liu, Y.; Suwannarach, N.; Kumla, J.; et al. OMICS in Food-Related Fungi and the Food Industry. Encyclopedia. Available online: https://encyclopedia.pub/entry/46169 (accessed on 15 April 2024).
Wijayawardene NN, Boonyuen N, Ranaweera CB, De Zoysa HKS, Padmathilake RE, Nifla F, et al. OMICS in Food-Related Fungi and the Food Industry. Encyclopedia. Available at: https://encyclopedia.pub/entry/46169. Accessed April 15, 2024.
Wijayawardene, Nalin N., Nattawut Boonyuen, Chathuranga B. Ranaweera, Heethaka K. S. De Zoysa, Rasanie E. Padmathilake, Faarah Nifla, Dong-Qin Dai, Yanxia Liu, Nakarin Suwannarach, Jaturong Kumla, et al. "OMICS in Food-Related Fungi and the Food Industry" Encyclopedia, https://encyclopedia.pub/entry/46169 (accessed April 15, 2024).
Wijayawardene, N.N., Boonyuen, N., Ranaweera, C.B., De Zoysa, H.K.S., Padmathilake, R.E., Nifla, F., Dai, D., Liu, Y., Suwannarach, N., Kumla, J., Bamunuarachchige, T.C., & Chen, H. (2023, June 28). OMICS in Food-Related Fungi and the Food Industry. In Encyclopedia. https://encyclopedia.pub/entry/46169
Wijayawardene, Nalin N., et al. "OMICS in Food-Related Fungi and the Food Industry." Encyclopedia. Web. 28 June, 2023.
OMICS in Food-Related Fungi and the Food Industry
Edit

Fungi comprise diverse taxa that are abundant in various environments. They have crucial ecological roles as decomposers, mutualists, and disease-causing agents. The use of high-throughput sequencing (HTS) and metagenomics in analyzing DNA from environmental samples has become crucial in the identification of new fungal lineages. In addition, the development of other omics technologies interrogating different cellular components and the use of these technologies in various polyphasic methods have significantly advanced research in areas such as biodiversity, physiological ecology, environmental sciences, and natural product biosynthesis. Among these omics approaches, proteomics, transcriptomics, metatranscriptomics, and metabolomics have revolutionized the current understanding of the biological processes of fungi. In addition, more specialized omics methods such as ionomics, glycomics, glycoproteomics, glycogenomics, lipidomics, and interactomics coupled with bioinformatics can contribute to a greater understanding of fungal metabolism. The combination of omics approaches (multiomics) can be used to characterize fungal genomes and their metabolites, making multiomics approaches essential for detecting and characterizing novel metabolites with important biological properties, such as anticancer, antimicrobial, and antidiabetic for human health applications.

food fungal toxins

1. Food Safety and Security Based on Omics Techniques

Food safety and security are pressing concerns as the human population continues to grow. The concept of food safety and security encompasses four essential elements, namely availability, access, utilization, and stability. The limited availability of food has necessitated the adoption of various measures, including establishing organizations such as the World Food Program by the United Nations’ Food and Agriculture Organization, increasing agricultural productivity, providing agricultural insurance, forming global partnerships, and the large-scale storage of food. Nonetheless, numerous challenges still exist with respect to global food security, including climate change, water scarcity, agricultural diseases, fuel, land degradation, food sovereignty, and politics [1]. In addition, food safety is an essential aspect of food science, which focuses primarily on preventing foodborne pathogens (mostly bacteria and fungi [2][3][4][5] from contaminating food during all stages of food production, including harvesting, handling, and storage [6]. This poses a significant challenge to the food production process, requiring constant vigilance to prevent such occurrences.

2. The Role of Fungi in the Food Industry

The role of fungi in the food industry is vast, and they have numerous potential applications in both food and feed processing industries. Fungi produce various bioactive metabolites, pigments, colorants, antioxidants, oligosaccharides, and enzymes that are widely used in the food industry. Multiomics approaches have been employed to identify different kinds of fungal products and analyze their potential applications in food security [5]. Fungi are also consumed as processed foods, fodder, and fermented foods. Fungal biomass has been utilized to produce mycoproteins, which can be used as meat substitutes such as Laetiporus sulphurous, Fusarium venenatum, F. oxysporum, Lentinula edodes, Aspergillus oryzae, and Fistulina hepatica. Fungal-based white (industrial) biotechnology techniques are emerging as a significant contributor to food security [1]. However, fungi can also have adverse effects on food security, such as causing food spoilage, foodborne illnesses, toxins, and diseases, which can ultimately damage food production. Additionally, fungi can have a detrimental impact on global crop production and harvesting, including domestic animals [3][6].
To ensure food safety and security, it is imperative to enhance the detection of fungi and their metabolites. Achieving this is a significant challenge that requires novel strategies and biotechnological solutions. In response, many fields of research have transitioned from classical methodologies to advanced technologies in recent decades. These technologies have been used to improve food crops, reduce environmental impacts, and produce alternative sources of protein.

3. Macrofungi and Edible Mushrooms

Macrofungi, which include Basidiomycota and a few Ascomycetous members, are used as human food in the form of mushrooms, dietary supplements, and beverages of fungal origin [7]. Although there are around 14,000 species of macro fungi, only about 350 species are consumed as food, such as the widely cultivated Agaricus bisporus, Lentinula edodes, and Flammulina velutipes [8][9][10][11]. Mushrooms are valued as human food because of their unique flavors, nutritional content, and health-promoting characteristics. Global mushroom production increased 13.8-fold to 42.8 million tons from 1990 to 2020 [12]. The market for edible mushrooms is expected to be worth USD 72.5 billion by 2027 [13].
To address the growing demand for edible macrofungi, researchers can employ omics technology to investigate their cultivation, breeding, and production. WGS and RNA sequencing (RNA-Seq) are particularly valuable tools for producing transgenic edible mushrooms with desirable characteristics, such as high nutrient and pharmaceutical value, and resistance to abiotic stress conditions [14]. Proteomic studies are also necessary to understand amino acid and enzyme biosynthesis pathways, while metabolome sequencing technology can be used to analyze the metabolic pathways of substances in edible fungi, including active ingredients, undiscovered small molecules, and secondary metabolites with pharmaceutical effects, and to discover metabolomic markers to recognize edible macrofungi [14][15].

4. Foodomics

Omics approaches are crucial for food and nutritional security by providing not only targeted analyses of biomolecules but also a better understanding of biological processes at the system level [4][6][16][17]. The application of omics technologies in the food and nutritional domains is referred to as “foodomics” [16][17][18]. Foodomics enables a better understanding of how food safety and security can be maintained while meeting human health requirements, particularly by studying food contaminants and toxicity to ensure a secure food supply chain [6][16].
Notable technologies used in foodomics include WGS, pulsed-field gel electrophoresis (PFGE), multiple-locus variable-number tandem repeat analysis (MLVA), and RNA-Seq. WGS can identify fungal species present as food contaminants. PFGE and MLVA can monitor the spread of pathogens within a food processing plant. RNA-Seq can monitor transcript abundance patterns in food samples, which change during microbial colonization, providing valuable insights into the mechanisms involved in fungal contamination. Furthermore, foodomics approaches can be used to prepare food safety legislation for specific types of food associated with fungi and other microbes [6][16].
Fungal biotechnology also offers solutions to ensure food safety and security that can be a part of the circular economy, mainly due to improvements in fungal cell factories [19]. Overall, foodomics offers a promising strategy for detecting and managing fungal contamination in food, and the continued advancement of high-tech approaches will improve researchers' ability toability to ensure food safety [6][16]. These examples demonstrate how multiomics approaches and tools can be used to address fungal threats to food safety and security. However, the use of these cutting-edge technologies can also present challenges. The large datasets generated by these omics approaches require careful data mining, reliable comparative analysis, and accurate statistical interpretation. Additionally, it is necessary to maintain comprehensive data banks and databases to store and manage the vast number of omics data.
The use of software tools has enabled access to omics datasets and an improved understanding of biological processes. However, the reliability of datasets needs to be constantly improved and upgraded. One challenge is obtaining adequate sample sizes and avoiding experimental design pitfalls to prevent overfitting and excessive false discoveries. It is important to address these issues to obtain real outputs and enable effective data sharing and mining [19][20]. Additionally, omics datasets are not static for both database providers and users, which presents another challenge that needs to be addressed [19].

5. Fungal Secondary Metabolites

Fungi produce a diverse range of secondary metabolites, including vitamins, amino acids, pigments, and antibiotics, which have numerous biotechnological applications, such as in agrochemicals, pharmaceuticals, agriculture, food, and cosmetic products. These metabolites have been found to possess anti-inflammatory, antioxidant, antimicrobial, and anticancer properties [21]. Fungal pigments are increasingly being used in the food industry due to their low production costs, easy processing, and consistent production yields [22]. These pigments are also safer for human health and the environment compared with synthetic pigments [23] (Table 1). Despite the potential use of fungal pigments as food additives, their usage is restricted because of the potential presence of naturally occurring toxic secondary metabolites (mycotoxins). One such example is Monascus, which is a promising source of natural colorant, but is prohibited in the European Union and the United States due to the presence of the mycotoxin citrinin [24].
Table 1. Safety evaluation of fungal pigments used in the food industry.
Fungal secondary metabolites are important sources of food flavors. Vanillin, for example, is primarily produced by engineered microorganisms rather than vanilla plants, with Aspergillus niger and Pycnoporus cinnabarinus being used to produce it from waste residues of rice bran oil, whereas Schizosaccharomyces pombe and Saccharomyces cerevisiae are used to produce it from inexpensive glucose. Benzaldehyde, which is an important flavoring compound for baked goods, can be produced using phenylalanine by P. cinnabarinus. In addition, S. cerevisiae has been used to reconstruct the primary aroma compound in raspberries, [4-(4-Hydroxyphenyl) butan-2-one] [25][26][27][28][29].
Plants and microorganisms are the main sources of natural metabolites. The cultivation of fungi is not affected by seasonal or geographical variations like plant crops, and fungi can be genetically engineered for increased metabolite production. The advantages of fungi over plants also include high growth rates, small space requirements, and the ability to be cultivated in inexpensive media with high biomass concentrations [30]. Despite the advantages of metabolite production from fungi, the potential of fungi to produce secondary metabolites for industrial application has not been fully realized yet, as most gene clusters responsible for secondary metabolite biosynthesis are only expressed under stress conditions and are silent under standard cultivation conditions [31]. To expand the potential pool of secondary metabolites, various approaches such as multiomics analyses, gene cluster activation, chemical genomics, metabolic identification, and genetic engineering can be utilized [21].
It is essential to explore alternative food sources, including alternative protein sources, as a means of reducing food security risks. Fungal enzymes have a crucial role in the food industry, as demonstrated by the use of amylases from A. niger and A. oryzae, proteases from A. oryzae, pectic enzymes from various Aspergillus species, galactosidase from Mortierella vinaceae, lactase from A. oryzae and A. niger, and invertase from Saccharomyces species [32][33][34]. Aspergillus oryzae is used for fermenting traditional Japanese foods like sake, shoyu, miso, and vinegar. Fungi also produce important vitamins used in the food industry, such as vitamin B2 (riboflavin), which is synthesized by Candida guilliermondii, Debaryomyces subglobosus, and Ashbya gossypii [35]. Mortierella alpiney has the capability to synthesize longer polyunsaturated fatty acids [36]. The nutraceutical properties of edible fungi like Lentinula edodes, Ganoderma lucidum, Tremella mesnterica, Hericium erinaceus, Sclerotinia sclerotiorum, Cordyceps sinensis, and Trametes versicolor are responsible for their popularity [37]. Since 1985, mycoprotein extracted from Fusarium venenatum has been used as a food-grade protein source with a texture similar to meat that can be frozen, canned, and dried. Mycoproteins are versatile and can be combined with different food items such as biscuits, soups, and fortified drinks. Analyzing the genetic makeup and nutritional value of these alternative food sources can be achieved through a combination of genomics, proteomics, and metabolomics [38].

6. Mycotoxins and Fungi

Fungi are a major cause of damage to cereal production worldwide, affecting major crops such as wheat, maize, and rice. Therefore, the detection of fungi and their metabolites is important in the food industry to ensure food security [3][39]. Fungal diseases also pose a threat to other species, such as Pseudogymnoascus destructans, which can cause catastrophic epidemics in bats and a concomitant increase in crop-destroying insects in fields [3]. Mycotoxins can contaminate a range of food products including meat, milk, eggs, and field crops [40]. Aspergillus and Penicillium are common mycotoxin-producing fungi that can contaminate food products [4]. Mycotoxins can be detected using metabolomic approaches [4][6][40].
The metabolomic approach has been successful in detecting various types of mycotoxins produced by different fungal species, including Alternaria, Fusarium, and Claviceps, which have the highest toxigenic potential [40]. These mycotoxins include Citrinin, Aflatoxins, Fumonisins, Zearalenone, Ochratoxins, Ergot Alkaloids, Patulin, Tremorgenic toxins, and Trichothecenes, which can be found in various foods [4][6][41]. The main fungal genera that are represented among food pathogens and mycotoxins in food industries that are the focus of foodomics applications include: (a) Aspergillus responsible for Aculeacin A, B, C, D, E, F, and G; Aflatoxin B; Aflatrem; and Ochratoxin; (b) Penicillium responsible for Citrinin, Amauromine, Agroclavine, and Patulin; (c) Claviceps responsible for Aflatrem, Chanoclavine I, Ergochromes, Ergobutine, Ergobutyrine, and Ergobine; and (d) Fusarium responsible for Deoxynivalenol, Fumonisins, Trichothecenes, and Zearalenone [4]. Metabolomics has provided insights into the interactions between phytopathogenic fungi and their hosts. Metabolomic studies of phytopathogenic fungi including Rhizoctonia solani, Botrytis cinerea, Ustilago maydis, Sclerotinia sclerotiorum, Magnaporthe oryzae, and Fusarium graminearum have revealed mechanisms of fungal infection and plant defense [42]. The interactions between fungal pathogens and plants are vital for global agricultural production and food security and have been widely researched [42][43]. Besides the study of mycotoxin-producing phytopathogenic fungi, metabolomics is useful for identifying fungal endophytes that produce bioactive compounds in a host-dependent manner [44]. In addition to the metabolomic study of interactions between phytopathogenic fungi and hosts, the impact of interacting fungi on the mineral and elemental composition of plants can be revealed by ionomics [17][45], notably, the effect of arbuscular mycorrhizal fungi inoculation on the growth of maize under various environmental stressors [46].
Fungal omics approaches such as transcriptomics and proteomics are important for the development of biomarkers and biosensors of mycotoxin-producing fungi [20]. Aspergillus flavus produces aflatoxin, a major contaminant of several crops including groundnut and maize. Transcriptomic and proteomics approaches have been used to identify genes and proteins associated with resistance to aflatoxin contamination in groundnut and maize, leading to understanding the host defense mechanism that includes pathogenesis and antioxidant-related genes involved in the suppression of aflatoxin biosynthesis or its detoxification [47]. The study of phosphorylated proteins (phosphoproteomics) has also revealed the ability of crops such as wheat and grapevine (Vitis vinifera) to resist a fungal pathogen (Septoria tritici) [48].
The knowledge of candidate biomarkers of resistance to fungal pathogens obtained from omics approaches has spurred efforts to create pathogen-resistant transgenic crop varieties with modifications of resistance-associated genes. For example, transgenic finger millet crops have been developed with enhanced gene expression to combat fungal blast disease and improve yield [49]. The generation of transgenic plants has benefitted from the emergence of genome editing technology. Clustered regularly interspaced short palindromic repeats (CRISPR) and CRISPR-associated (Cas) protein genome editing tools offer a cost-effective and versatile approach to generate transgenic plants with modifications of genes associated with traits of interest. Genome-editing of plants has been used to generate high-yielding and stress- and disease-resistant crop varieties [50][51][52]. Of particular interest, genome editing technology has been used to knock out genes associated with susceptibility to fungal pathogens, including the rice blast pathogen Magnaporthe oryzae and the powdery mildew pathogen Podosphaera xanthii [51].

 7. Food Industry

Among food industries, the dairy industry is the most impacted by fungi. Spoilage of dairy products by molds poses a major food safety challenge. To control molds, antifungal lactobacilli species like Lacticaseibacillus rhamnosus and L. paracasei can delay spoilage and increase the shelf life of dairy products. Metabolomics can identify the key compounds that are essential for antifungal activity. This approach has been successfully applied against Penicillium commune and Mucor racemosus, resulting in the development of new protective strains [53]. Additionally, meta-transcriptomics (RNA-Seq of complex community microbial samples) has led to insights into the role of fungal microflora such as Geotrichum candidum and Penicillium camemberti in the cheese ripening process [54]. The use of omics approaches and their applications has proven to be efficient in producing safe foods and ensuring food security (Figure 1). Furthermore, these applications are effective and productive tools for conducting systems biology investigations and studying fungi [16][45].
Figure 1. Outline of omics tools and applications in fungal omics to ensure food safety and security.

8. Postharvest Losses

Postharvest losses of food affect quality, nutrition, seed viability, and market value [55]. The global postharvest food loss has been calculated to be approximately 1.3 billion tons annually, which disproportionally affects developing countries. For instance, post-harvest losses account for 30–40% of fruits and vegetables produced in India [56]. A major cause of postharvest loss of fresh fruits and vegetables is pathogenic fungi. Penicillium spp., Botrytis cinerea, Alternaria alternata, Monilinia spp., Trichothecium roseum, Fusarium spp., and Colletotrichum spp. are responsible for the majority of postharvest losses [57].
Understanding the infection process mechanism of fungal pathogens is crucial for mitigation of post-harvest diseases. Phytotoxic metabolites, secreted proteins, and small RNAs of fungal pathogens contribute to the infection process. At the early stage of infection, necrotrophic pathogenic fungi kill host cells and develop necrotic areas for successful colonization [57]. Proteins secreted by the pathogenic fungus Fusarium proliferatum in the infection process of banana peel were identified by comparative proteomics [58], and cell-wall-degrading enzymes and secondary metabolites secreted by the pathogenic fungus Monilinia fructicola were identified by sequence analyses and gene expression studies [59]. Furthermore, analysis of B. cinerea mutants identified genes encoding the cell-wall-degrading enzymes cellobiohydrolase and xylanase to be essential for virulence [60].
When a pathogenic fungus attacks a plant, reactive oxygen species (ROS) accumulate around the infection site as part of the plant defense mechanism [61]. ROS derived from pathogenic fungi also play a significant role in the infection process [62]. In fungi, the NADPH oxidase complex (Nox) is the most important enzyme complex for ROS production. The reduction in vegetative growth, conidia formation, and loss of virulence in B. cinerea were observed by NoxR gene knockout [63]. In addition to ROS, small non-coding RNAs (sRNAs) play roles in regulating plant immunity against pathogen infections [64]. The pathogenic fungus B. cinerea produces sRNAs that hijack the host RNA interference machinery and selectively silence host plant immune genes [65]. In addition to sRNAs, pathogen-protein-coding genes important for virulence have been identified using the gene knockout approach. Using this approach, the MAP kinase genes Pdos2, PdSlt2, and PdMpkB in the signal transduction pathway were shown to regulate the pathogenicity of Penicillium digitatum [66], and transcription factors regulating development and pathogenicity were identified in Fusarium graminearum [67].

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