Deep-sea hydrothermal sediments are enriched in transition metals that exert selective pressure on resident microbial communities. Despite the recognized influence of metal toxicity on microbial diversity, the genomic basis of metal resistance and its phylogenetic distribution in hydrothermal deposits and the surrounding sediments of the Southern Mid-Atlantic Ridge (SMAR) remain poorly understood. Here, we performed metagenomic sequencing of surface sediments collected from five SMAR stations and reconstructed 157 high- and medium-quality non-redundant metagenome-assembled genomes (MAGs) to investigate the taxonomic diversity and genome-resolved distribution of metal resistance genes (MRGs). The recovered MAGs represented 15 bacterial and archaeal phyla, with Pseudomonadota dominating the community, followed by Nitrospirota and Bacteroidota. Annotation of the recovered MAGs revealed widespread resistance potential to multiple metals, indicating that diverse metal resistance mechanisms are broadly conserved across SMAR sediments. Genome-resolved taxonomic analysis further demonstrated pronounced lineage-specific patterns of MRG distribution. Gammaproteobacteria encoded the most diverse repertoire of resistance determinants, whereas Alphaproteobacteria preferentially harbored arsenic- and mercury-resistance genes. Other taxonomic groups exhibited specialized adaptive strategies, including zinc homeostasis in Bacteroidota. Our genome-resolved analyses demonstrate that metal resistance potential in SMAR sediments is taxonomically structured distribution, reflecting differences in genomic potential among microbial lineages to hydrothermal metal enrichment. These findings expand our understanding of microbial survival strategies in deep-sea hydrothermal ecosystems and provide a genomic framework for future studies of metal cycling in the deep ocean.
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