In marine ecosystems, viruses exert control on the composition and metabolism of microbial communities, influencing overall biogeochemical cycling. Deep sea sediments associated with cold seeps are known to host taxonomically diverse microbial communities, but little is known about viruses infecting these microorganisms. Here, we probed metagenomes from seven geographically diverse cold seeps across global oceans to assess viral diversity, virus–host interaction, and virus-encoded auxiliary metabolic genes (AMGs). Gene-sharing network comparisons with viruses inhabiting other ecosystems reveal that cold seep sediments harbour considerable unexplored viral diversity. Most cold seep viruses display high degrees of endemism with seep fluid flux being one of the main drivers of viral community composition. In silico predictions linked 14.2% of the viruses to microbial host populations with many belonging to poorly understood candidate bacterial and archaeal phyla. Lysis was predicted to be a predominant viral lifestyle based on lineage-specific virus/host abundance ratios. Metabolic predictions of prokaryotic host genomes and viral AMGs suggest that viruses influence microbial hydrocarbon biodegradation at cold seeps, as well as other carbon, sulfur and nitrogen cycling via virus-induced mortality and/or metabolic augmentation. Overall, these findings reveal the global diversity and biogeography of cold seep viruses and indicate how viruses may manipulate seep microbial ecology and biogeochemistry.

Microbially mediated nitrogen cycling in carbon-dominated cold seep environments remains poorly understood. So far anaerobic methanotrophic archaea (ANME-2) and their sulfate-reducing bacterial partners (SEEP-SRB1 clade) have been identified as diazotrophs in deep sea cold seep sediments. However, it is unclear whether other microbial groups can perform nitrogen fixation in such ecosystems. To fill this gap, we analyzed 61 metagenomes, 1428 metagenome-assembled genomes, and six metatranscriptomes derived from 11 globally distributed cold seeps. These sediments contain phylogenetically diverse nitrogenase genes corresponding to an expanded diversity of diazotrophic lineages. Diverse catabolic pathways were predicted to provide ATP for nitrogen fixation, suggesting diazotrophy in cold seeps is not necessarily associated with sulfate-dependent anaerobic oxidation of methane. Nitrogen fixation genes among various diazotrophic groups in cold seeps were inferred to be genetically mobile and subject to purifying selection. Our findings extend the capacity for diazotrophy to five candidate phyla (Altarchaeia, Omnitrophota, FCPU426, Caldatribacteriota and UBA6262), and suggest that cold seep diazotrophs might contribute substantially to the global nitrogen balance.

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The seafloor sulfide structures of inactive vents are known to host abundant and diverse microorganisms potentially supported by mineralogy of sulfides. However, little is known about the diversity and distribution of microbial functions. Here, we used genome-resolved metagenomics to predict microbial metabolic functions and the contribution of horizontal gene transfer to the functionality of microorganisms inhabiting several hydrothermally inactive seafloor deposits among globally distributed deep-sea vent fields. Despite of geographically distant vent fields, similar microbial community patterns were observed with the dominance of Gammaproteobacteria, Bacteroidota and previously overlooked Candidatus Patescibacteria. Metabolically flexible Gammaproteobacteria are major potential primary producers utilizing mainly sulfur, iron and hydrogen as electron donors coupled with oxygen and nitrate respiration for chemolithoautotrophic growth. In addition to heterotrophic microorganisms like free-living Bacteroidota, Ca. Patescibacteria potentially perform fermentative recycling of organic carbon. Finally, we provided evidence that many functional genes that are central to energy metabolism have been laterally transferred among members within the community and largely within the same class. Taken together, these findings shed light on microbial ecology and evolution in inactive seafloor sulfide deposits after the cessation of hydrothermal activities.

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Mercury (Hg) is an important element in seafloor cold seeps that might govern methane emission. However, so far, the knowledge of biogeochemical Hg cycle in it remains poorly understood. In this study, Hg geochemical characteristics and microorganisms involved in Hg biogeochemical cycling were examined in three (active, inactive seep vs reference) different types of sediments sampled from the Haima cold seep in the South China Sea. Sediments in the active seep area were significantly enriched in mercury and methylmercury (MeHg) compared to the reference. Accordingly, abundant genes related to Hg methylation (hgcAB), demethylation (merB) and reduction (merA) were detected in the active seep sediments, phylogenetically associated with various bacterial and archaeal linages (e.g. Desulfobacterota, Gammaproteobacteria and Halobacteriota). Hg odd-mass number isotopes (Δ199Hg and Δ201Hg) pointed to their source from the upper ocean and the occurrence of abiotic dark oxidation. The δ202Hg values indicate Hg mass fractionation, migration and transformation in the active seep sediments. These geochemical and microbial data highlight active Hg biogeochemical cycles in seafloor cold seeps, functioning as important Hg-sinks and MeHg sources in the deep ocean.

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