Microbial detoxification of mycotoxins in food

Abstract

Mycotoxins are toxic secondary metabolites produced by certain genera of fungi including but not limited to Fusarium, Aspergillus, and Penicillium. Their persistence in agricultural commodities poses a significant food safety issue owing to their carcinogenic, teratogenic, and immunosuppressive effects. Due to their inherent stability, mycotoxin levels in contaminated food often exceed the prescribed regulatory thresholds posing a risk to both humans and livestock. Although physical and chemical methods have been applied to remove mycotoxins, these approaches may reduce the nutrient quality and organoleptic properties of food. Microbial transformation of mycotoxins is a promising alternative for mycotoxin detoxification as it is more specific and environmentally friendly compared to physical/chemical methods. Here we review the biological detoxification of the major mycotoxins with a focus on microbial enzymes.

Keywords: Mycotoxins; T2; aflatoxins; citrinin; deoxynivalenol; ochratoxin; patulin; zearaleneone.

Figure 1

Summary of common functional groups of mycotoxins (circle) and their possible transformation by microbial enzymes.

Figure 2

In vivo effects of aflatoxin B1 and microbial detoxification approaches. (A) Aflatoxin B1, produced by members of Aspergillus is carcinogenic, genotoxic, and possesses immunosuppressive properties. (B) Bacillus licheniformis ANSB821 utilizes the laccase, CotA to biotransform aflatoxin B1. (C) The manganese peroxidase MnP from the white-rot fungus Phanerochaete sordida YK-624 oxidizes AFB1 to form AFB1-8,9-dihydrodiol via an 8,9-epoxide intermediate. (D) Proposed reduction of AFB1 ring by a deazaflavin cofactor (F₄₂₀) containing M. smegmatis enzyme.

Figure 3

In vivo effects of ZEN and microbial detoxification approaches. (A) ZEN possesses estrogenic properties which in turn affect the endocrine and reproductive systems of animals. (B) Transformation of ZEN to α-ZEL or β-ZEL by microorganisms. The C7-carbonyl oxygen is reduced to an alcohol stereospecifically (red). The enzyme(s) responsible for catalyzing this reaction have not been isolated and identified. (C) ZEN can be hydrolyzed by lactone hydrolases followed by spontaneous decarboxylation to produce DHZEN. (D) Transformation of ZEN to ZOM-1 was postulated to occur in two steps. The first step could potentially be catalyzed by a Baeyer-Villiger type monooxygenase. The lactone product can then be hydrolyzed to ZOM-1.

Figure 4

In vivo effects of citrinin, patulin, ochratoxin and microbial detoxification approaches. (A) These mycotoxins are produced by members of Aspergillus and Penicillium and typically, citrinin and ochratoxin possess nephrotoxic effects while patulin exerts serious gastrointestinal effects. (B) Decarboxylation of citrinin to decarboxycitrinin. (C) The hemiacetal ring of patulin likely exist in equilibrium with the ring-open form. The aldehyde in the ring-opened form of patulin can be reduced by enzymes from the short-chain dehydrogenase (SDR) or aldo-keto reductase (AKR) family to (E)-ascladiol. The E-ascladiol can be converted to the (Z)-isomer catalyzed by cellular sulfhydryl compounds, such as cysteine. Ascladiol can potentially be reduced to hydroascladiol by some microorganisms, such as Lactobacillus plantanum. Other basidiomycete yeasts can also transform patulin to DPA, although the formation of E-ascladiol appears to be more ubiquitous among various yeast and bacterial species. (D) The amide bond of ochratoxin A can be hydrolyzed to from L-phenylalanine and ochratoxin α.

Figure 5

In vivo effects of fumonisin B1 and microbial detoxification approaches. (A) Fumonisin B1, typically produced by Fusarium species exert toxic effects on the liver as well as kidneys. (B) Hydrolysis of fumonisin B1 catalyzed by carboxyesterases target the ester linkages highlighted in red. Deamination reaction catalyzed by (C) aminotransferase or (D) an amine oxidase with the targeted C2 amino group highlighted in fuschia. The aminotransferase and amine oxidase from Sphingopyxis sp. MTA144 and Exophiala spinifera utilize hydrolyzed fumonisin B1 as substrate.

Figure 6

Sub-classification of trichothecenes. Trichothecenes can be sub-classified into four groups based on substitution patterns around the EPT nucleus. Key functional groups which distinguish each group from one another are highlighted in red.

Figure 7

In vivo effects of Type B trichothecenes like DON and microbial detoxification approaches. (A) DON affects the gastrointestinal system and at a molecular level, the mycotoxin can bind to ribosomes triggering ribotoxic stress. (B–F) DON can be transformed by de-epoxidation, oxidation, epimerization, acetylation, hydroxylation and glycosylation.

Figure 8

In vivo effects of Type A trichothecenes like T-2 toxin and microbial detoxification approaches. (A) T-2, like DON, causes negative gastrointestinal effects and ribotoxic stress. (B–E) The mycotoxin can be detoxified by de-epoxidation, hydrolysis of the ester linkages or acetylation.