Microbial potential to mitigate neurotoxic methylmercury accumulation in farmlands and rice

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.