Comparative metagenomics highlights the habitat-related diversity in taxonomic composition and metabolic potential of deep-sea sediment microbiota

Sediment plays a pivotal role in deep-sea ecosystems by providing habitats for a diverse range of microorganisms and facilitates the cycling processes of carbon, sulfur and nitrogen. Beyond the normal seafloor (NS), distinctive geographical features such as cold seeps (CS) and hydrothermal vent (HV) are recognized as life oases harboring highly diverse microbial communities. A global atlas of microorganisms can reveal the notable association between geological processes and microbial colonization. However, a comprehensive understanding of the systematic comparison of microbial communities in sediments across various deep-sea regions worldwide and their contributions to Earth's elemental cycles remains limited. Analyzing metagenomic data from 163 deep-sea sediment samples across 73 locations worldwide revealed that microbial communities in CS sediments exhibited the highest richness and diversity, followed by HV sediments, with NS sediments showing the lowest diversity. The NS sediments were predominantly inhabited by <i>Nitrosopumilaceae</i>, a type of ammonia-oxidizing archaea (AOA). In contrast, CSs and HVs were dominated by <i>ANME-1</i>, a family of anaerobic methane-oxidizing archaea (ANME), and <i>Desulfofervidaceae</i>, a family of sulfate-reducing bacteria (SRB), respectively. Microbial networks were established for each ecosystem to analyze the relationships and interactions among different microorganisms. Additionally, we analyzed the metabolic patterns of microbial communities in different deep-sea sediments. Despite variations in carbon fixation pathways in ecosystems with different oxygen concentrations, carbon metabolism remains the predominant biogeochemical cycle in deep-sea sediments. Benthic ecosystems exhibit distinct microbial potentials for sulfate reduction, both assimilatory and dissimilatory sulfate reduction (ASR and DSR), in response to different environmental conditions. The presence of nitrogen-fixing microorganisms in CS sediments may influence the global nitrogen balance. In this study, the significant differences in the taxonomic composition and functional potential of microbial communities inhabiting various deep-sea environments were investigated. Our findings emphasize the importance of conducting comparative studies on ecosystems to reveal the complex interrelationships between marine sediments and global biogeochemical cycles.