Microbial potential to mitigate neurotoxic methylmercury accumulation in farmlands and rice

Abstract

Toxic methylmercury (CH3Hg+) is produced by microbial conversion of inorganic mercury in hypoxic environments such as rice paddy soils, and can accumulate in rice grains. Although microbial demethylation has been recognized as a crucial pathway for CH3Hg+ degradation, the identities of microbes and pathways accountable for CH3Hg+ degradation in soil remain elusive. Here, we combine 13CH3Hg+-DNA stable-isotope probing experiments with shotgun metagenomics to explore microbial taxa and associated biochemical processes involved in CH3Hg+ degradation in paddy and upland soils. We identify Pseudarthrobacter, Methylophilaceae (MM2), and Dechloromonas as the most significant taxa potentially engaged in the degradation of 13CH3Hg+ in paddy soil with high mercury contamination. We confirm that strains affiliated with two of those taxa (species Dechloromonas denitrificans and Methylovorus menthalis) can degrade CH3Hg+ in pure culture assays. Metagenomic analysis further reveals that most of these candidate 13CH3Hg+ degraders carry genes associated with the Wood-Ljungdahl pathway, dicarboxylate-hydroxybutyrate cycle, methanogenesis, and denitrification, but apparently lack the merB and merA genes involved in CH3Hg+ reductive demethylation. Finally, we estimate that microbial degradation of soil CH3Hg+ contributes to 0.08–0.64 fold decreases in CH3Hg+ accumulation in rice grains across China (hazard quotient (HQ) decrements of 0.62–13.75%). Thus, our results provide insights into microorganisms and pathways responsible for CH3Hg+ degradation in soil, with potential implications for development of bioremediation strategies.