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.

Soil microorganisms can mediate the occurrence of plant diseases. Potato common scab (CS) is a refractory disease caused by pathogenic Streptomyces that occurs worldwide, but little is known about the interactions between CS and the soil microbiome. In this study, four soil-root system compartments (geocaulosphere soil (GS), rhizosphere soil (RS), root-zone soil (ZS), and furrow soil (FS)) were analyzed for potato plants with naturally high (H) and low (L) scab severity levels. We aimed to determine the composition and putative function of the soil microbiome associated with potato CS. The copy numbers of the scab phytotoxin biosynthetic gene txtAB and the bacterial 16S rRNA gene as well as the diversity and composition of each of the four soil-root system compartments were examined; GS was the only compartment that exhibited significant differences between the H and L groups. Compared to the H group, the L group exhibited a lower txtAB gene copy number, lower bacterial 16S copy number, higher diversity, higher co-occurrence network complexity, and higher community function similarity within the GS microbiome. The community composition and function of the GS samples were further revealed by shotgun metagenomic sequencing. Variovorax, Stenotrophomonas, and Agrobacterium were the most abundant genera that were significantly and positively correlated with the scab severity level, estimated absolute abundance (EAA) of pathogenic Streptomyces, and txtAB gene copy number. In contrast, Geobacillus, Curtobacterium, and unclassified Geodermatophilaceae were significantly negatively correlated with these three parameters. Compared to the function profiles in the L group, several genes involved in “ABC transporters,” the “bacterial secretion system,” “quorum sensing (QS),” “nitrogen metabolism,” and some metabolism by cytochrome P450 were enriched in the H group. In contrast, some antibiotic biosynthesis pathways were enriched in the L group. Based on the differences in community composition and function, a simple model was proposed to explain the putative relationships between the soil microbiome and CS occurrence. The GS microbiome was closely associated with CS severity in the soil-root system, and the occurrence of CS was accompanied by changes in community composition and function. The differential functions provide new clues to elucidate the mechanism underlying the interaction between CS occurrence and the soil microbiome, and varying community compositions provide novel insights into CS occurrence.

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.