Metagenomics reveals diverse community of putative mercury methylators across different biogeochemical niches in Sansha Yongle blue hole

Methylmercury (MeHg) is a potent neurotoxin and bioaccumulates in food webs. Microbial transformation of inorganic mercury (Hg) produces most of the MeHg in the marine environment. The gene pair hgcAB encodes for Hg methylation, a process predominantly attributed to anaerobic bacteria. However, recent studies indicate the formation of methylmercury in low-oxygen zones within marine water columns, although the mechanisms remain poorly understood. "Blue holes" are marine sinkholes containing redox gradients stratified with depth and high microbial diversity across a range of biogeochemical cycles. Here, we present the first metagenomic analysis focused on the potential for Hg methylation in a blue hole ecosystem. Yongle Blue Hole (YBH), currently the world's deepest known blue hole, was selected as a representative site to investigate the genetic potential for Hg methylation and to explore the functional capabilities of putative Hg-methylators within this unique environment. Metagenomic analysis showed that the anoxic sulfidic deep water was likely to be a hotspot for Hg methylation, driven by abundant and diverse Deltaproteobacteria. In the suboxic intermediate layer, Nitrospina and Myxococcota dominated the Hg-methylating community. Furthermore, Hg methylators were found to have different lifestyles (free-living or particle-associated) and to occupy distinct ecological niches within the YBH. In addition, the contribution of sinking particles to Hg methylation, especially in the deep anoxic water column, was highlighted. Our study unveils the biodiversity and survival strategies of Hg methylators across distinct environments. The findings suggest that blue holes could serve as model stratified ecosystems for studying Hg methylation processes across different habitats.