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  1. Abstract

    Deep-sea hydrothermal vent geochemistry shapes the foundation of the microbial food web by fueling chemolithoautotrophic microbial activity. Microbial eukaryotes (or protists) play a critical role in hydrothermal vent food webs as consumers and hosts of symbiotic bacteria, and as a nutritional source to higher trophic levels. We measured microbial eukaryotic cell abundance and predation pressure in low-temperature diffuse hydrothermal fluids at the Von Damm and Piccard vent fields along the Mid-Cayman Rise in the Western Caribbean Sea. We present findings from experiments performed under in situ pressure that show cell abundances and grazing rates higher than those done at 1 atmosphere (shipboard ambient pressure); this trend was attributed to the impact of depressurization on cell integrity. A relationship between the protistan grazing rate, prey cell abundance, and temperature of end-member hydrothermal vent fluid was observed at both vent fields, regardless of experimental approach. Our results show substantial protistan biomass at hydrothermally fueled microbial food webs, and when coupled with improved grazing estimates, suggest an important contribution of grazers to the local carbon export and supply of nutrient resources to the deep ocean.

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  2. Abstract Background

    Marine symbioses are predominantly established through horizontal acquisition of microbial symbionts from the environment. However, genetic and functional comparisons of free-living populations of symbionts to their host-associated counterparts are sparse. Here, we assembled the first genomes of the chemoautotrophic gammaproteobacterial symbionts affiliated with the deep-sea snailAlviniconcha hesslerifrom two separate hydrothermal vent fields of the Mariana Back-Arc Basin. We used phylogenomic and population genomic methods to assess sequence and gene content variation between free-living and host-associated symbionts.


    Our phylogenomic analyses show that the free-living and host-associated symbionts ofA. hesslerifrom both vent fields are populations of monophyletic strains from a single species. Furthermore, genetic structure and gene content analyses indicate that these symbiont populations are differentiated by vent field rather than by lifestyle.


    Together, this work suggests that, despite the potential influence of host-mediated acquisition and release processes on horizontally transmitted symbionts, geographic isolation and/or adaptation to local habitat conditions are important determinants of symbiont population structure and intra-host composition.

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  3. 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. 
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  4. Fluids circulating through oceanic crust play important roles in global biogeochemical cycling mediated by their microbial inhabitants, but studying these sites is challenged by sampling logistics and low biomass. Borehole observatories installed at the North Pond study site on the western flank of the Mid-Atlantic Ridge have enabled investigation of the microbial biosphere in cold, oxygenated basaltic oceanic crust. Here we test a methodology that applies redox-sensitive fluorescent molecules for flow cytometric sorting of cells for single cell genomic sequencing from small volumes of low biomass (approximately 10 3 cells ml –1 ) crustal fluid. We compare the resulting genomic data to a recently published paired metagenomic and metatranscriptomic analysis from the same site. Even with low coverage genome sequencing, sorting cells from less than one milliliter of crustal fluid results in similar interpretation of dominant taxa and functional profiles as compared to ‘omics analysis that typically filter orders of magnitude more fluid volume. The diverse community dominated by Gammaproteobacteria, Bacteroidetes, Desulfobacterota, Alphaproteobacteria, and Zetaproteobacteria, had evidence of autotrophy and heterotrophy, a variety of nitrogen and sulfur cycling metabolisms, and motility. Together, results indicate fluorescence activated cell sorting methodology is a powerful addition to the toolbox for the study of low biomass systems or at sites where only small sample volumes are available for analysis. 
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  5. Abstract The deep seafloor covers two-thirds of Earth's surface area, but our understanding of the ecosystems and resources found in the deep ocean, as well as the ability of deep-sea ecosystems to withstand human perturbation, is limited. These deep-sea habitats demand urgent study as there are emergent human uses in the form of deep-sea mining and carbon sequestration that will fundamentally alter physical, chemical, and biological conditions that took millions of years to establish. We propose the international network COBRA, a research accelerator for the crustal ocean biosphere. COBRA will bring together diverse stakeholders and experts, including interdisciplinary academic and government scientists, private institutions, policy makers, data systems engineers, industry experts, and others to coordinate efforts that generate new knowledge and inform decision making about activities that could affect the deep ocean and, by extension, all of society. We will also train the next generation of leaders in ocean exploration, science, and policy through an innovative virtual program to carry this effort into future generations of ocean and earth science research. COBRA will inform policies relating to emergent industrial uses of the deep ocean, decrease the likelihood of serious harm to the environment, and maintain ecosystem services for the benefit of society. 
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  6. Hydrogenotrophic methanogens are ubiquitous chemoautotrophic archaea inhabiting globally distributed deep-sea hydrothermal vent ecosystems and associated subseafloor niches within the rocky subseafloor, yet little is known about how they adapt and diversify in these habitats. To determine genomic variation and selection pressure within methanogenic populations at vents, we examined five Methanothermococcus single cell amplified genomes (SAGs) in conjunction with 15 metagenomes and 10 metatranscriptomes from venting fluids at two geochemically distinct hydrothermal vent fields on the Mid-Cayman Rise in the Caribbean Sea. We observed that some Methanothermococcus lineages and their transcripts were more abundant than others in individual vent sites, indicating differential fitness among lineages. The relative abundances of lineages represented by SAGs in each of the samples matched phylogenetic relationships based on single-copy universal genes, and genes related to nitrogen fixation and the CRISPR/Cas immune system were among those differentiating the clades. Lineages possessing these genes were less abundant than those missing that genomic region. Overall, patterns in nucleotide variation indicated that the population dynamics of Methanothermococcus were not governed by clonal expansions or selective sweeps, at least in the habitats and sampling times included in this study. Together, our results show that although specific lineages of Methanothermococcus co-exist in these habitats, some outcompete others, and possession of accessory metabolic functions does not necessarily provide a fitness advantage in these habitats in all conditions. This work highlights the power of combining single-cell, metagenomic, and metatranscriptomic datasets to determine how evolution shapes microbial abundance and diversity in hydrothermal vent ecosystems. 
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  7. null (Ed.)
    Biogeochemical processes occurring in fluids that permeate oceanic crust make measurable contributions to the marine carbon cycle, but quantitative assessments of microbial impacts on this vast, subsurface carbon pool are lacking. We provide bulk and single-cell estimates of microbial biomass production from carbon and nitrogen substrates in cool, oxic basement fluids from the western flank of the Mid-Atlantic Ridge. The wide range in carbon and nitrogen incorporation rates indicates a microbial community well poised for dynamic conditions, potentially anabolizing carbon and nitrogen at rates ranging from those observed in subsurface sediments to those found in on-axis hydrothermal vent environments. Bicarbonate incorporation rates were highest where fluids are most isolated from recharging bottom seawater, suggesting that anabolism of inorganic carbon may be a potential strategy for supplementing the ancient and recalcitrant dissolved organic carbon that is prevalent in the globally distributed subseafloor crustal environment. 
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  8. The unique ecosystems and biodiversity associated with mid-ocean ridge (MOR) hydrothermal vent systems contrast sharply with surrounding deep-sea habitats, however both may be increasingly threatened by anthropogenic activity (e.g., mining activities at massive sulphide deposits). Climate change can alter the deep-sea through increased bottom temperatures, loss of oxygen, and modifications to deep water circulation. Despite the potential of these profound impacts, the mechanisms enabling these systems and their ecosystems to persist, function and respond to oceanic, crustal, and anthropogenic forces remain poorly understood. This is due primarily to technological challenges and difficulties in accessing, observing and monitoring the deep-sea. In this context, the development of deep-sea observatories in the 2000s focused on understanding the coupling between sub-surface flow and oceanic and crustal conditions, and how they influence biological processes. Deep-sea observatories provide long-term, multidisciplinary time-series data comprising repeated observations and sampling at temporal resolutions from seconds to decades, through a combination of cabled, wireless, remotely controlled, and autonomous measurement systems. The three existing vent observatories are located on the Juan de Fuca and Mid-Atlantic Ridges (Ocean Observing Initiative, Ocean Networks Canada and the European Multidisciplinary Seafloor and water column Observatory). These observatories promote stewardship by defining effective environmental monitoring including characterizing biological and environmental baseline states, discriminating changes from natural variations versus those from anthropogenic activities, and assessing degradation, resilience and recovery after disturbance. This highlights the potential of observatories as valuable tools for environmental impact assessment (EIA) in the context of climate change and other anthropogenic activities, primarily ocean mining. This paper provides a synthesis on scientific advancements enabled by the three observatories this last decade, and recommendations to support future studies through international collaboration and coordination. The proposed recommendations include: i) establishing common global scientific questions and identification of Essential Ocean Variables (EOVs) specific to MORs, ii) guidance towards the effective use of observatories to support and inform policies that can impact society, iii) strategies for observatory infrastructure development that will help standardize sensors, data formats and capabilities, and iv) future technology needs and common sampling approaches to answer today’s most urgent and timely questions. 
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  9. Abstract

    The oceanic crustal aquifer is one of the largest habitable volumes on Earth, and it harbors a reservoir of microbial life that influences global-scale biogeochemical cycles. Here, we use time series metagenomic and metatranscriptomic data from a low-temperature, ridge flank environment representative of the majority of global hydrothermal fluid circulation in the ocean to reconstruct microbial metabolic potential, transcript abundance, and community dynamics. We also present metagenome-assembled genomes from recently collected fluids that are furthest removed from drilling disturbances. Our results suggest that the microbial community in the North Pond aquifer plays an important role in the oxidation of organic carbon within the crust. This community is motile and metabolically flexible, with the ability to use both autotrophic and organotrophic pathways, as well as function under low oxygen conditions by using alternative electron acceptors such as nitrate and thiosulfate. Anaerobic processes are most abundant in subseafloor horizons deepest in the aquifer, furthest from connectivity with the deep ocean, and there was little overlap in the active microbial populations between sampling horizons. This work highlights the heterogeneity of microbial life in the subseafloor aquifer and provides new insights into biogeochemical cycling in ocean crust.

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