Distribution and function of prokaryotes involved in mercury methylation, demethylation, and reduction in the western North Pacific Subtropical Gyre

Methylmercury (MeHg), a bioaccumulative neurotoxic heavy metal, substantially threatens environmental and human health. In natural environments, MeHg formation and degradation are primarily mediated by microorganisms containing <i>hgcAB</i>, <i>merA</i>, or <i>merB</i> genes. However, these genes have not been simultaneously analyzed in open-ocean samples. This study aimed to investigate the distribution and phylogeny of functional genes associated with mercury (Hg) methylation (<i>hgcA</i> and <i>hgcB</i>), demethylation (<i>merB</i>), and reduction (<i>merA</i>), as well as dissolved total Hg (THg) and MeHg concentrations in the western North Pacific Subtropical Gyre (WNPSG) using metagenomic analysis. Although THg levels varied across sampling sites, MeHg concentrations consistently increased with depth. A strong correlation between dissolved MeHg and apparent oxygen utilization indicated a link between Hg methylation and microbial respiration. <i>hgcA</i>, <i>merB</i>, and <i>merA</i> were predominantly detected at depths of 500-1,500 m, where MeHg concentrations peaked, indicating active microbial Hg speciation within mesopelagic layers. A higher abundance of <i>hgcA</i> than <i>merB</i> suggests that microbial Hg methylation may surpass demethylation in this region. Phylogenetic analyses of <i>hgcAB</i> identified the <i>Nitrospina</i> lineage as dominant Hg methylators. Metabolic pathway analyses of metagenome-assembled genomes (MAGs) showed that <i>Nitrospina</i> harboring <i>hgcAB</i> possesses the nitrite reductase pathway, suggesting a linkage between Hg methylation and nitrogen cycling. MAGs with <i>hgcA</i> affiliated with <i>Myxococcota</i> (Deltaproteobacteria) exhibited a strong association with sulfur cycling. Diverse lineages harboring <i>merB</i> and <i>merA</i> genes were identified, suggesting that MeHg demethylation and Hg(II) reduction likely co-occur. Methanogenesis pathways in some Alphaproteobacteria with <i>merB</i> or <i>merA</i> suggest a potential connection between methane production and MeHg degradation and Hg(II) reduction. These findings provide novel insights into the intricate interactions between microbial communities, functional gene distributions, and Hg biogeochemical cycling in the WNPSG.