In globally distributed deep-sea hydrothermal vent plumes, microbiomes are shaped by the redox energy landscapes created by reduced hydrothermal vent fluids mixing with oxidized seawater. Plumes can disperse over thousands of kilometers and their characteristics are determined by geochemical sources from vents, e.g., hydrothermal inputs, nutrients, and trace metals. However, the impacts of plume biogeochemistry on the oceans are poorly constrained due to a lack of integrated understanding of microbiomes, population genetics, and geochemistry. Here, we use microbial genomes to understand links between biogeography, evolution, and metabolic connectivity, and elucidate their impacts on biogeochemical cycling in the deep sea. Using data from 36 diverse plume samples from seven ocean basins, we show that sulfur metabolism defines the core microbiome of plumes and drives metabolic connectivity in the microbial community. Sulfur-dominated geochemistry influences energy landscapes and promotes microbial growth, while other energy sources influence local energy landscapes. We further demonstrated the consistency of links among geochemistry, function, and taxonomy. Amongst all microbial metabolisms, sulfur transformations had the highest MW-score, a measure of metabolic connectivity in microbial communities. Additionally, plume microbial populations have low diversity, short migration history, and gene-specific sweep patterns after migrating from background seawater. Selected functions include nutrient uptake, aerobic oxidation, sulfur oxidation for higher energy yields, and stress responses for adaptation. Our findings provide the ecological and evolutionary bases of change in sulfur-driven microbial communities and their population genetics in adaptation to changing geochemical gradients in the oceans.
Bibliographical noteFunding Information:
This research was supported by the National Science Foundation under grant number OCE 2049478 to KA and OCE 1851208 to JAB, and the Gordon and Betty Moore Foundation under grant number GBMF3297 to JAH.
We thank all the members from the cruises of R/V New Horizon in Guaymas Basin, Gulf of California (July 2004), R/V Atlantis and R/V Falkor in Mid-Cayman Rise, Caribbean Sea (Jan 2012 and June 2013), R/V Thomas G Thompson in Eastern Lau Spreading Center (ELSC), Lau Basin, western Pacific Ocean (May-July 2009), and R/V Thomas G Thompson in Axial Seamount (Aug 2015) in assisting sampling and measurement and processing of physicochemical data.
© 2023, The Author(s).
PubMed: MeSH publication types
- Journal Article
- Research Support, U.S. Gov't, Non-P.H.S.
- Research Support, Non-U.S. Gov't