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Abstract 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. 

Single‐celled microbial eukaryotes inhabit deep‐sea hydrothermal vent environments and play critical ecological roles in the vent‐associated microbial food web. 18S rRNA amplicon sequencing of diffuse venting fluids from four geographically‐ and geochemically‐distinct hydrothermal vent fields was applied to investigate community diversity patterns among protistan assemblages. The four vent fields include Axial Seamount at the Juan de Fuca Ridge, Sea Cliff and Apollo at the Gorda Ridge, all in the NE Pacific Ocean, and Piccard and Von Damm at the Mid‐Cayman Rise in the Caribbean Sea. We describe species diversity patterns with respect to hydrothermal vent field and sample type, identify putative vent endemic microbial eukaryotes, and test how vent fluid geochemistry may influence microbial community diversity. At a semi‐global scale, microbial eukaryotic communities at deep‐sea vents were composed of similar proportions of dinoflagellates, ciliates, Rhizaria, and stramenopiles. Individual vent fields supported distinct and highly diverse assemblages of protists that included potentially endemic or novel vent‐associated strains. These findings represent a census of deep‐sea hydrothermal vent protistan communities. Protistan diversity, which is shaped by the hydrothermal vent environment at a local scale, ultimately influences the vent‐associated microbial food web and the broader deep‐sea carbon cycle.

 

Vast and diverse microbial communities exist within the ocean. To better understand the global influence of these microorganisms on Earth’s climate, we developed a robot capable of sampling dissolved and particulate seawater biochemistry across ocean basins while still capturing the fine-scale biogeochemical processes therein. Carbon and other nutrients are acquired and released by marine microorganisms as they build and break down organic matter. The scale of the ocean makes these processes globally relevant and, at the same time, challenging to fully characterize. Microbial community composition and ocean biochemistry vary across multiple physical scales up to that of the ocean basins. Other autonomous underwater vehicles are optimized for moving continuously and, primarily, horizontally through the ocean. In contrast,Clio, the robot that we describe, is designed to efficiently and precisely move vertically through the ocean, drift laterally in a Lagrangian manner to better observe water masses, and integrate with research vessel operations to map large horizontal scales to a depth of 6000 meters. We present results that show howClioconducts high-resolution sensor surveys and sample return missions, including a mapping of 1144 kilometers of the Sargasso Sea to a depth of 1000 meters. We further show how the samples obtain filtered biomass from seawater that enable genomic and proteomic measurements not possible through in situ sensing. These results demonstrate a robotic oceanography approach for global-scale surveys of ocean biochemistry.