Aerobic methane oxidation by microorganisms exacerbates neurotoxic methylmercury accumulation in rice paddy fields.

Abstract

Aerobic methane (CH4) oxidation is the dominant biological sink for CH4 in wetland soils and is increasingly linked to diverse biogeochemical processes; however, whether and how aerobic CH4 oxidation influences the production of the neurotoxin methylmercury (MeHg) through microbial mercury (Hg) methylation remains poorly understood. Here, we combined a ~3300 km field survey across the main rice-producing areas of China with 13CH4-DNA-stable isotope probing (SIP) to investigate the microbial linkage between aerobic CH4 oxidation and Hg methylation in paddy fields. Field observations showed positive relationships between CH4 oxidation activity and the ratio of MeHg at a continental scale, as well as between gene abundances of CH4 oxidation (pmoA) and Hg methylation (hgcA). Microcosm experiments further demonstrated that CH4 addition significantly increased MeHg production by 40.7-177.7% and enhanced hgcA gene expression by 49.5-416.0% across three typical paddy soils. Moreover, 13CH4-DNA-SIP analyses identified 112 hgcA-containing operational taxonomic units (OTUs) that incorporated 13CH4-derived 13C, of which 75.0-85.5% were affiliated with the families Geobacteraceae, Anaerolineaceae, and unclassified Desulfobacterales. Integrated analyses of 13C-metagenome-assembled genomes and metabolomics indicated that this carbon transfer was likely mediated by metabolic handoffs from methanotrophs to Hg-methylating microorganisms through intermediates (e.g., malate and fumarate) released during aerobic CH4 oxidation. Soil incubation and pure-culture experiments further confirmed the functional significance of methanotroph-derived metabolites, as their addition significantly enhanced MeHg production. These findings highlight microbial metabolic handoffs as an important mechanism linking aerobic CH4 oxidation and Hg methylation, with implications for developing synergistic strategies for MeHg pollution mitigation and carbon reduction.

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