Geomicrobiology of Hydrothermal Plumes: Elucidating the Role of Microorganisms in Deep Ocean Carbon and Sulfur Biogeochemical Cycles.

Deep-sea hydrothermal vents are distributed globally across mid-ocean ridges and back-arc basins and represent an important interface at which elements and energy are transferred between the lithosphere and the oceans. Deep-sea hydrothermal plumes occur where hot fluids rise from hydrothermal vents on the ocean floor, enriched with reduced chemicals such as hydrogen sulfide, hydrogen, methane, iron, manganese and ammonia that serve as energy sources for microbial metabolism. Microbial chemosynthesis in plumes contributes significantly to organic carbon in the deep oceans. Recent work suggests that microbial chemosynthesis is also pervasive throughout the dark oceans, serving as a significant CO2 sink even at sites far-removed from vents. Although ammonia and sulfur have been identified as potential electron donors for such chemosynthesis, they do not fully account for measured rates of carbon fixation in the dark oceans. Thus, there is a need to identify potential electron donors for chemosynthesis in the dark oceans and advance our understanding of the relationship between biogeochemistry, microbial metabolism and diversity. We used DNA and cDNA sequencing of samples from Guaymas Basin (GB) (Gulf of California) and the Eastern Lau Spreading Center (ELSC) (Western Pacific Ocean) to reveal the genetic potential and activity of microorganisms in hydrothermal plumes and the surrounding deep oceans. First, we characterized the gene content and expression of SUP05, a globally distributed group of uncultured sulfur-oxidizing bacteria, at GB. GB SUP05 contains and highly expresses genes for H2 oxidation; this is the first H2-oxidizing chemolithotroph to be identified in the pelagic deep ocean. Second, we show that at ELSC, prominent differences in the geochemistry of hydrothermal vents did not manifest in the composition of microbial communities of hydrothermal plumes, which were dominated by sulfur-based chemolithotrophic energy metabolism. Finally, we identified five distinct viruses that infect SUP05 bacteria at GB and ELSC and showed that they contain SUP05-derived genes for sulfur oxidation, thereby providing the first evidence of viral genes involved in lithotrophy. We suggest that SUP05 viruses use a novel ecological strategy to access abundant elemental sulfur in the environment by supplementing sulfur oxidation in their hosts to support viral infection and replication.