Unveiling a Novel Zearalenone Biodegradation Pathway in Metarhizium anisopliae and Elucidating the Role of Cytochrome P450.

Metarhizium fungi, essential for ecosystem function and commonly utilised in pest control, often occupy ecological niches contaminated by toxic compounds of both anthropogenic and microbiological origin. The present study reveals the potential of Metarhizium anisopliae for biodegradation of the Fusarium mycotoxin zearalenone (ZEN), a common contaminant of crops that poses a significant threat to human and animal health due to its oestrogenic potential and toxicity. A key aspect of the pathway described is the degradation of ZEN by cleaving the lactone bond, which results in a significant reduction in mycotoxin toxicity, highlighting the fungus's bioremediation potential. Furthermore, this study provides the first evidence of subsequent degradation of ZEN metabolites through progressive shortening of the aliphatic chain, primarily via alternating oxidation and demethylation, ultimately yielding trihydroxybenzene. Significantly, lactone bond cleavage occurred not only in ZEN itself but also in its reduced forms, the zearalanols, formed through the initial reduction of ZEN to zearalenols. Elevated mRNA levels of cytochrome P450 (CYP450) monooxygenases in M. anisopliae exposed to ZEN indicate their significant involvement in degradation mechanisms. Intriguingly, the inhibition of CYP450 activity resulted in a substantial shift in the quantitative ratio of α- and β-epimers of zearalenols and zearalanols. The observed alteration towards β-form production likely stems from the inhibition of other CYP450-dependent reactions, indirectly influencing ZEN reduction pathways-a particularly noteworthy finding. These insights are crucial for developing strategies to utilise M. anisopliae in the bioremediation of ZEN-contaminated areas.