Biotransformations of arsenic in marine sediments across marginal slope to hadal zone

Arsenic compounds are accumulating in deep ocean, but their ecological impacts on deep-sea ecosystem remain elusive. We studied 32 sediment cores (101 layers for metagenomes, along with 41 global reference sediment metagenomes) collected from the South China Sea and the Mariana Trench (MT), characterized with high arsenic accumulation in MT. In these metagenomes we revealed a significantly positive correlation between relative abundance of arsenite methyltransferase gene (arsM) and sampling depth, which suggests that arsenic methylation is the most prevalent arsenic biotransformation process in the deep sea. Lower relative abundance of arsenic efflux gene, compared with arsM, indicates that microbes in deep-sea sediments were prone to methylate arsenite and retain it rather than efflux it. Phylogenetic analysis identified seven clades of ArsM proteins, including two new clades derived primarily from deep-sea microorganisms. Five metagenome-assembled genomes containing aioA for arsenite oxidation also harbor carbon fixation genes in the deep-sea sediment layers, suggesting previously unnoticed contribution of arsenite-oxidizing autotrophic bacteria to the carbon cycle. Therefore, deep-sea microorganisms adopt different detoxification and transformation strategies in response to arsenic compounds, which renews our understanding of arsenic in their ecological impacts and potential contribution in deep ocean.