Biodegradation mechanisms of fludioxonil revealed by multi-omics analysis

The role of microorganisms in the natural attenuation and bioremediation of fludioxonil is poorly understood, despite the persistent nature, ecotoxicity and environmental presence of this pesticide. Only recently the potential of microorganisms to degrade fludioxonil was clearly shown, but the molecular mechanisms underlying these biodegradation processes remain mostly unknown. To circumvent this knowledge gap, in this work we elucidate the catabolic mechanisms of the biodegradation of this fungicide, by an enriched bacterial consortium, through the combination of metaproteogenomics and ESI-LC-MS/MS-based metabolomics analyses. The degrading consortium removed over 90 % of fludioxonil from solution and was able to defluorinate about 50 % of the molecule in 28 days, though no sub-products were detected by comparative metabolomics. Nonetheless, a constitutive methyltransferase, originally belonging to the methionine biosynthetic pathway, was overexpressed during the biodegradation process and suggested to be involved in the promiscuous defluorination of fludioxonil. Furthermore, the upregulation of aerobic respiration pathways, coupled to the absence of any identified metabolites, suggests that fludioxonil was partially mineralized by the bacterial consortium. The employed in silico analyses further showed that Comamonas bacteria were likely responsible for most of this catabolic effort. This work provides an unprecedented outlook onto the biodegradation mechanics of the recalcitrant fungicide fludioxonil by an enriched bacterial consortium.