Deep sea hydrothermal vents as oases of virus-driven biogeochemical cycling

Abstract:

The deep ocean is one of the planet’s largest biomes. In spite of cold temperatures and the lack of light, the deep sea hosts abundant microbial life that play critical roles in the biogeochemical cycling of carbon, nitrogen, sulfur and other nutrients. Globally distributed hydrothermal vents are hotspots of microbial biogeochemistry and elemental cycling in the deep oceans. At hydrothermal vents, high temperature water-rock reactions manifest in chemically reduced fluids rich in hydrogen, hydrogen sulfide, methane and metals that facilitate chemolithotrophic primary production and the growth of diverse microbial communities. Viruses are central components of ecosystem dynamics that manipulate host metabolic networks during infection and release labile nutrients by killing their hosts. Recent studies have expanded our understanding of the metabolic potential and ecological interactions of bacteria and archaea that inhabit different vent environments such as vent chimneys, hydrothermal plumes, sediments, and the surrounding water column. However, very little is known about viruses that infect these microbes and their impacts on biogeochemical cycling at hydrothermal vents and beyond into the deep oceans. Here, we investigate viral ecology and potential for biogeochemical cycling of nutrients across vent-associated natural geochemical gradients in the deep oceans. Using a combination of submersible and robotic vehicle-based sampling, we collected viruses from hydrothermal vent fields at Guaymas Basin, Eastern Lau Spreading Center, and Brother Volcano in the Pacific Ocean. We identified a rich diversity of viruses across geochemically distinct vent fields. Viruses infecting chemolithotrophs were common in vent environments suggesting they represent an important control on primary producers. We also identified a large repertoire of auxiliary metabolic genes associated with energy metabolism indicating that viruses modulate keystone processes including those directly impacting biogeochemical cycling within vent-associated microbial communities. Overall, our study provides evidence for the importance of viral infection on the ecology, evolution and diversity of vent-associated communities, and biogeochemical cycling in the deep sea.