Virus diversity and interactions with hosts in deep-sea hydrothermal vents

Background: The deep sea harbors many viruses, yet their diversity and interactions with hosts in hydrothermal ecosystems are largely unknown. Here, we analyzed the viral composition, distribution, host preference, and metabolic potential in different habitats of global hydrothermal vents, including vent plumes, background seawater, diffuse fluids, and sediments. Results: From 34 samples collected at eight vent sites, a total of 4662 viral populations (vOTUs) were recovered from the metagenome assemblies, encompassing diverse phylogenetic groups and defining many novel lineages. Apart from the abundant unclassified viruses, tailed phages are most predominant across the global hydrothermal vents, while single-stranded DNA viruses, including Microviridae and small eukaryotic viruses, also constitute a significant part of the viromes. As revealed by protein-sharing network analysis, hydrothermal vent viruses formed many novel genus-level viral clusters and are highly endemic to specific vent sites and habitat types. Only 11% of the vOTUs can be linked to hosts, which are the key microbial taxa of hydrothermal habitats, such as Gammaproteobacteria and Campylobacterota. Intriguingly, vent viromes share some common metabolic features in that they encode auxiliary genes that are extensively involved in the metabolism of carbohydrates, amino acids, cofactors, and vitamins. Specifically, in plume viruses, various auxiliary genes related to methane, nitrogen, and sulfur metabolism were observed, indicating their contribution to host energy conservation. Moreover, the prevalence of sulfur-relay pathway genes indicated the significant role of vent viruses in stabilizing the tRNA structure, which promotes host adaptation to steep environmental gradients. Conclusions: The deep-sea hydrothermal systems hold untapped viral diversity with novelty. They may affect both vent prokaryotic and eukaryotic communities and modulate host metabolism related to vent adaptability. More explorations are needed to depict global vent virus diversity and its roles in this unique ecosystem.