Genomic potential for mercury biotransformation in marine sediments across marginal slope to hadal zone

Abstract Mercury accumulates in the deep sea, but its ecological impact on deep-sea ecosystems remains poorly understood. We conduct an analysis of 32 sediment cores, comprising 101 layers for the study of metagenomes, and additional 41 global reference sediment metagenomes. These sediment cores are collected from two deep-sea regions: the South China Sea and Mariana Trench, followed by revealing high mercury accumulation in the South China Sea. In these metagenomes, we find that the mercury methylation genes hgcAB are abundant in marginal seas but negligible in open oceans. Genomics result indicates that some Hg-methylating microorganisms affiliated with Desulfobacterota, Spirochaetota, and Zixibacteria in the deep-sea sediments encode MttB, the sole corrinoid-dependent methyltransferase identified in these taxa, which may interact with HgcA to transfer methyl groups from possibly osmolyte-derived trimethylamine for methylation. The demethylation gene merB is widely distributed and exhibits higher abundance in the open ocean. Moreover, we identify a large number of novel Hg demethylating taxa that are associated with horizontal transfer of the merB gene potentially involving methane generation. Our results expand the diversity of Hg-transforming taxa and reveal their unique ecophysiological adaptations in deep-sea sediments.