Potential biotransformations of mercury in marine sediments across marginal slope to hadal zone

Mercury accumulates in the deep sea, but its ecological impact on deep-sea ecosystems remains poorly understood. We conducted an analysis of 32 sediment cores, comprising 101 layers for the study of metagenomes, and additional 41 global reference sediment metagenomes. These sediment cores were collected from two deep-sea regions: the South China Sea (SCS) and Mariana Trench (MT), followed by revealing high mercury accumulation in the SCS. In these metagenomes, we found that the mercury methylation genes hgcA/B as detoxification regulators were abundant in marginal seas but negligible in open oceans. Instead of taking the Wood-Ljungdahl pathway as methyl group donor, some Hg-methylating microorganisms affiliated with Desulfobacterota, Spirochaetota, and Zixibacteria in the deep-sea sediments have the potential to utilize osmolyte-derived trimethylamine for methylation. The demethylation gene merB was widely distributed and exhibits higher abundance in the open ocean. Moreover, we identified 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-metabolizing taxa and reveal their unique ecophysiological adaptations in deep-sea sediments.