Search for: All records

Abstract Viruses are ubiquitous in deep-sea hydrothermal vents, where they influence microbial communities and biogeochemistry. Yet, viral ecology and evolution remain understudied in these environments. Here, we identify 49,962 viruses from 52 globally distributed hydrothermal vent samples (10 plume, 40 deposit, and 2 diffuse flow metagenomes), and reconstruct 5708 viral metagenome-assembled genomes, the majority of which were bacteriophages. Hydrothermal viruses were largely endemic, however, some viruses were shared between geographically separated vents, predominantly between the Lau Basin and Brothers Volcano in the Pacific Ocean. Geographically distant viruses shared proteins related to core functions such as structural proteins, and rarely, proteins of auxiliary functions involved in processes such as fermentation and cobalamin biosynthesis. Common microbial hosts of viruses included members of Campylobacterota, Alpha-, and Gammaproteobacteria in deposits, and Gammaproteobacteria in plumes. Campylobacterota- and Gammaproteobacteria-infecting viruses reflected variations in hydrothermal chemistry and functional redundancy in their predicted microbial hosts, suggesting that hydrothermal geology is a driver of viral ecology and coevolution of viruses and hosts. Our results indicate that viral ecology and evolution in globally distributed hydrothermal vents is shaped by endemism and thus may have increased susceptibility to the negative impacts of deep-sea mining and anthropogenic change in ocean ecosystems. 

Abstract Microorganisms play vital roles in sulfur cycling through the oxidation of elemental sulfur and reduction of sulfite. These metabolisms are catalyzed by dissimilatory sulfite reductases (Dsr) functioning in either the reductive or reverse, oxidative direction. Dsr-mediated sulfite reduction is an ancient metabolism proposed to have fueled energy metabolism in some of Earth’s earliest microorganisms, whereas sulfur oxidation is believed to have evolved later in association with the widespread availability of oxygen on Earth. Organisms are generally believed to carry out either the reductive or oxidative pathway, yet organisms from diverse phyla have been discovered with gene combinations that implicate them in both pathways. A comprehensive investigation into the metabolisms of these phyla regarding Dsr is currently lacking. Here, we selected one of these phyla, the metabolically versatile candidate phylum SAR324, to study the ecology and evolution of Dsr-mediated metabolism. We confirmed that diverse SAR324 encode genes associated with reductive Dsr, oxidative Dsr, or both. Comparative analyses with other Dsr-encoding bacterial and archaeal phyla revealed that organisms encoding both reductive and oxidative Dsr proteins are constrained to a few phyla. Further, DsrAB sequences from genomes belonging to these phyla are phylogenetically positioned at the interface between well-defined oxidative and reductive bacterial clades. The phylogenetic context and dsr gene content in these organisms points to an evolutionary transition event that ultimately gave way to oxidative Dsr-mediated metabolism. Together, this research suggests that SAR324 and other phyla with mixed dsr gene content are associated with the evolution and origins of Dsr-mediated sulfur oxidation.