Abstract

BackgroundContamination of agricultural commodities with multiple trichothecene mycotoxins, produced by toxigenic Fusarium species, is a food safety issue, which greatly affects grain production and marketing worldwide. Importantly, exposure to multiple trichothecenes may increase toxicity in animals due to their synergistic and/or additive effects. To address the problem this study aimed to achieve a novel biological trait capable of detoxifying various food and feed contaminating trichothecenes under aerobic and anaerobic conditions and wide range of temperatures.ResultsA highly enriched microbial consortium (called DX100) capable of transforming eleven trichothecenes to significantly less toxic de-epoxy forms was achieved after prolonged incubation of soil microbial culture with 200 μg/mL deoxynivalenol (DON). DX100 demonstrated de-epoxidation activity under aerobic and anaerobic conditions, a greater range of temperatures and around neutral pH. The consortium contains 70% known and 30% unknown bacterial species, dominated by Stenotrophomonas species. Probably novel bacteria including strains of Stenotrophomonas and Alkaliphilus-Blautia species complex could be involved in aerobic and anaerobic de-epoxidation of trichothecenes, respectively. DX100 showed rapid and stable activity by de-epoxidizing 100% of 50 μg/mL deoxynivalenol at 48 h of incubation and retaining de-epoxidation ability after 100 subcultures in mineral salts broth (MSB). It was able to de-epoxidize high concentration of DON (500 μg/mL), and transformed ten more food contaminating trichothecenes into de-epoxy forms and/or other known/unknown compounds. Microbial de-epoxidation rate increased with increasing trichothecene concentrations in the broth media, suggesting that DX100 maintains a robust trichothecene detoxifying mechanism. Furthermore, the nature of microbial de-epoxidation reaction and inhibition of the reaction by sodium azide and the finding that bacterial cell culture lysate retained activity suggests that certain cytoplasmic reductases may be responsible for the de-epoxidation activity.ConclusionsThis study reports the enrichment procedure for obtaining an effective and stable microbial consortium DX100 capable of de-epoxidizing several food contaminating trichothecene mycotoxins. DX100, which has de-epoxidation ability under wide range of conditions, represents a unique enzymatic source which has great industrial potential for reducing contamination of foods/feeds with multiple trichothecenes, and minimizing their synergistic/additive cytotoxic effects on consumer health.

Highlights

  • Contamination of agricultural commodities with multiple trichothecene mycotoxins, produced by toxigenic Fusarium species, is a food safety issue, which greatly affects grain production and marketing worldwide

  • Functional stability and identification of bacteria in trichothecene transforming bacterial consortium Three months of co-incubating the soil microbes with 200 μg/mL DON in mineral salts broth (MSB) led to an enriched bacterial consortium DX100 that efficiently de-epoxidized trichothecenes, after 100 subcultures in broth

  • The generation metagenomic sequencing technology determined an altered composition of the bacterial consortium in DX100 compared to the original culture that was used for enrichment

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Summary

Introduction

Contamination of agricultural commodities with multiple trichothecene mycotoxins, produced by toxigenic Fusarium species, is a food safety issue, which greatly affects grain production and marketing worldwide. Exposure to multiple trichothecenes may increase toxicity in animals due to their synergistic and/or additive effects. The toxigenic Fusarium (mold) and other fungal pathogens contaminate cereal-based foods and feeds by producing a variety of health injurious trichothecene mycotoxins [1]. Trichothecenes are chemically tricyclic sesquiterpenes, characterized by a double bond at the C9, 10 position and a C12, 13 epoxy functional group The latter is the principal moiety responsible for the toxicity of these fungal secondary metabolites in eukaryotic organisms [9]. The toxicities of the members of two trichothecene types vary, exposure to multiple mycotoxins may increase their cytotoxicity because of their synergistic and/or additive cytotoxic effects on eukaryotic organisms [12, 13]. Common toxicity effects of the trichothecenes in humans and animals include diarrhea, vomiting, feed refusal, growth retardation, immunosuppression, reduced ovarian functions/reproductive disorders and even death [14, 15]

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