Biogeography and ecology of the rare and abundant microbial lineages in deep-sea hydrothermal vents

Author Posting. © The Author(s), 2014. This is the author's version of the work. It is posted here by permission of Oxford University Press for personal use, not for redistribution. The definitive version was published in FEMS Microbiology Ecology 91 (2015): 1-11, doi:10.1093/femsec/fiu016.Environmental gradients generate countless ecological niches in deep-sea hydrothermal vent systems, which foster diverse microbial communities. The majority of distinct microbial lineages in these communities occur in very low abundance. However, the ecological role and distribution of rare and abundant lineages, particularly in deep, hot subsurface environments, remains unclear. Here, we use 16S rRNA tag sequencing to describe biogeographic patterning and microbial community structure of both rare and abundant archaea and bacteria in hydrothermal vent systems. We show that while rare archaeal lineages and almost all bacterial lineages displayed geographically restricted community structuring patterns, the abundant lineages of archaeal communities displayed a much more cosmopolitan distribution. Finally, analysis of one high-volume, high-temperature fluid sample representative of the deep hot biosphere described a unique microbial community that differed from microbial populations in diffuse flow fluid or sulfide samples, yet the rare thermophilic archaeal groups showed similarities to those that occur in sulfides. These results suggest that while most archaeal and bacterial lineages in vents are rare and display a highly regional distribution, a small percentage of lineages, particularly within the archaeal domain, are successful at widespread dispersal and colonization.Funding for this work was provided by a grant from the NASA Astrobiology Institute to the Carnegie Institution of Washington.2015-12-0

Selection is a significant driver of gene gain and loss in the pangenome of the bacterial genus Sulfurovum in geographically distinct deep-sea hydrothermal vents

© The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Moulana, A., Anderson, R. E., Fortunato, C. S., & Huber, J. A. Selection is a significant driver of gene gain and loss in the pangenome of the bacterial genus Sulfurovum in geographically distinct deep-sea hydrothermal vents. Msystems, 5(2), (2020): e00673-19, doi:10.1128/mSystems.00673-19.Microbial genomes have highly variable gene content, and the evolutionary history of microbial populations is shaped by gene gain and loss mediated by horizontal gene transfer and selection. To evaluate the influence of selection on gene content variation in hydrothermal vent microbial populations, we examined 22 metagenome-assembled genomes (MAGs) (70 to 97% complete) from the ubiquitous vent Epsilonbacteraeota genus Sulfurovum that were recovered from two deep-sea hydrothermal vent regions, Axial Seamount in the northeastern Pacific Ocean (13 MAGs) and the Mid-Cayman Rise in the Caribbean Sea (9 MAGs). Genes involved in housekeeping functions were highly conserved across Sulfurovum lineages. However, genes involved in environment-specific functions, and in particular phosphate regulation, were found mostly in Sulfurovum genomes from the Mid-Cayman Rise in the low-phosphate Atlantic Ocean environment, suggesting that nutrient limitation is an important selective pressure for these bacteria. Furthermore, genes that were rare within the pangenome were more likely to undergo positive selection than genes that were highly conserved in the pangenome, and they also appeared to have experienced gene-specific sweeps. Our results suggest that selection is a significant driver of gene gain and loss for dominant microbial lineages in hydrothermal vents and highlight the importance of factors like nutrient limitation in driving microbial adaptation and evolution.We thank Julie Reveillaud and Emily Reddington for support in the collection and generation of metagenomic data, Chip Breier, David Butterfield, Bill Chadwick, Chris German, Jim Holden, Jill McDermott, and Jeff Seewald for sample collection support at sea, and Jaclyn Saunders for discussions regarding arsenate reductase. A.M. was supported by Carleton College. R.A. was supported by a NASA Postdoctoral Fellowship with the NASA Astrobiology Institute. This work was supported by a NASA Exobiology grant 80NSSC18K1076 to R.A. and J.A.H., a NASA Astrobiology Science and Technology for Exploring Planets (ASTEP) grant NNX-327 09AB75G and a grant from Deep Carbon Observatory’s Deep Life Initiative to J.A.H., the NSF Science and Technology Center for Dark Energy Biosphere Investigations (C-DEBI) to J.A.H., and the Gordon and Betty Moore Foundation grant GBMF3297 to J.A.H. Samples were collected from the Mid-Cayman Rise with the assistance of the captains and crew of the R/V Atlantis and R/V Falkor as well as ROVs Jason and Nereus. For Mid-Cayman Rise, ship and vehicle time in 2012 were supported by the NSF-OCE great OCE-1061863 to Chris German and Jeff Seewald and in 2013 by the Schmidt Ocean Institute during cruise FK008-2013 aboard the R/V Falkor. Samples collected from Axial Seamount were collected with the assistance of the captains and crew of the R/V Falkor, R/V Thompson, and R/V Brown as well as the ROV ROPOS and Jason groups, and in 2013 the Schmidt Ocean Institute during cruise FK010-2013 aboard the R/V Falkor

Is the genetic landscape of the deep subsurface biosphere affected by viruses?

Viruses are powerful manipulators of microbial diversity, biogeochemistry, and evolution in the marine environment. Viruses can directly influence the genetic capabilities and the fitness of their hosts through the use of fitness factors and through horizontal gene transfer. However, the impact of viruses on microbial ecology and evolution is often overlooked in studies of the deep subsurface biosphere. Subsurface habitats connected to hydrothermal vent systems are characterized by constant fluid flux, dynamic environmental variability, and high microbial diversity. In such conditions, high adaptability would be an evolutionary asset, and the potential for frequent host-virus interactions would be high, increasing the likelihood that cellular hosts could acquire novel functions. Here, we review evidence supporting this hypothesis, including data indicating that microbial communities in subsurface hydrothermal fluids are exposed to a high rate of viral infection, as well as viral metagenomic data suggesting that the vent viral assemblage is particularly enriched in genes that facilitate horizontal gene transfer and host adaptability. Therefore, viruses are likely to play a crucial role in facilitating adaptability to the extreme conditions of these regions of the deep subsurface biosphere. We also discuss how these results might apply to other regions of the deep subsurface, where the nature of virus-host interactions would be altered, but possibly no less important, compared to more energetic hydrothermal systems

Microbial populations are shaped by dispersal and recombination in a low biomass subseafloor habitat

© The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Anderson, R., Graham, E., Huber, J., & Tully, B. Microbial populations are shaped by dispersal and recombination in a low biomass subseafloor habitat. MBio, 13(4), (2022): e0035422, https://doi.org/10.1128/mbio.00354-22.The subseafloor is a vast habitat that supports microorganisms that have a global scale impact on geochemical cycles. Many of the endemic microbial communities inhabiting the subseafloor consist of small populations under growth-limited conditions. For small populations, stochastic evolutionary events can have large impacts on intraspecific population dynamics and allele frequencies. These conditions are fundamentally different from those experienced by most microorganisms in surface environments, and it is unknown how small population sizes and growth-limiting conditions influence evolution and population structure in the subsurface. Using a 2-year, high-resolution environmental time series, we examine the dynamics of microbial populations from cold, oxic crustal fluids collected from the subseafloor site North Pond, located near the mid-Atlantic ridge. Our results reveal rapid shifts in overall abundance, allele frequency, and strain abundance across the time points observed, with evidence for homologous recombination between coexisting lineages. We show that the subseafloor aquifer is a dynamic habitat that hosts microbial metapopulations that disperse frequently through the crustal fluids, enabling gene flow and recombination between microbial populations. The dynamism and stochasticity of microbial population dynamics in North Pond suggest that these forces are important drivers in the evolution of microbial populations in the vast subseafloor habitat.This work was supported by NSF OCE-1062006, OCE-1745589, and OCE-1635208 to J.A.H. The Gordon and Betty Moore Foundation sponsored observatory components at North Pond through grant GBMF1609. The Center for Dark Energy Biosphere Investigations (C-DEBI) (OCE-0939564) supported J.A.H. and B.J.T. This is C-DEBI contribution 598

Diverse viruses in deep-sea hydrothermal vent fluids have restricted dispersal across ocean basins

© The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Thomas, E., Anderson, R. E., Li, V., Rogan, L. J., & Huber, J. A. Diverse viruses in deep-sea hydrothermal vent fluids have restricted dispersal across ocean basins. Msystems, 6(3), (2021): e00068-21, https://doi.org/10.1128/mSystems.00068-21.In the ocean, viruses impact microbial mortality, regulate biogeochemical cycling, and alter the metabolic potential of microbial lineages. At deep-sea hydrothermal vents, abundant viruses infect a wide range of hosts among the archaea and bacteria that inhabit these dynamic habitats. However, little is known about viral diversity, host range, and biogeography across different vent ecosystems, which has important implications for how viruses manipulate microbial function and evolution. Here, we examined viral diversity, viral and host distribution, and virus-host interactions in microbial metagenomes generated from venting fluids from several vent sites within three different geochemically and geographically distinct hydrothermal systems: Piccard and Von Damm vent fields at the Mid-Cayman Rise in the Caribbean Sea, and at several vent sites within Axial Seamount in the Pacific Ocean. Analysis of viral sequences and clustered regularly interspaced short palindromic repeat (CRISPR) spacers revealed highly diverse viral assemblages and evidence of active infection. Network analysis revealed that viral host range was relatively narrow, with very few viruses infecting multiple microbial lineages. Viruses were largely endemic to individual vent sites, indicating restricted dispersal, and in some cases, viral assemblages persisted over time. Thus, we show that hydrothermal vent fluids are home to novel, diverse viral assemblages that are highly localized to specific regions and taxa.Funding for E.T. was provided by Carleton College. R.E.A. was supported by a NASA Postdoctoral Fellowship with the NASA Astrobiology Institute. This work was supported by a NASA Exobiology grant 80NSSC18K1076 to R.E.A. and J.A.H., a NASA Astrobiology Science and Technology for Exploring Planets (ASTEP) grant NNX-327 09AB75G, and a grant from Deep Carbon Observatory's Deep Life Initiative to J.A.H., the NSF Science and Technology Center for Dark Energy Biosphere Investigations (C-DEBI) to J.A.H., and the Gordon and Betty Moore Foundation grant GBMF3297 to J.A.H. Samples were collected from the Mid-Cayman Rise with the assistance of the captains and crew of the R/V Atlantis and R/V Falkor as well as ROVs Jason and Nereus. For Mid-Cayman Rise, ship and vehicle time in 2012 were supported by the NSF-OCE grant OCE-1061863 to Chris German and Jeff Seewald and in 2013 by the Schmidt Ocean Institute during cruise FX008-2013 aboard the R/V Falkor. Samples collected from Axial Seamount were collected with the assistance of the captains and crew of the R/V Falkor, R/V Thompson, and R/V Brown as well as the ROV ROPOS and Jason groups, and in 2013 the Schmidt Ocean Institute during cruise FK010-2013 aboard the R/V Falkor

New opportunities and untapped scientific potential in the abyssal ocean

© The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Marlow, J., Anderson, R., Reysenbach, A.-L., Seewald, J., Shank, T., Teske, A., Wanless, V., & Soule, S. New opportunities and untapped scientific potential in the abyssal ocean. Frontiers in Marine Science, 8, (2022): 798943, https://doi.org/10.3389./fmars.2021.798943The abyssal ocean covers more than half of the Earth’s surface, yet remains understudied and underappreciated. In this Perspectives article, we mark the occasion of the Deep Submergence Vehicle Alvin’s increased depth range (from 4500 to 6500 m) to highlight the scientific potential of the abyssal seafloor. From a geologic perspective, ultra-slow spreading mid-ocean ridges, Petit Spot volcanism, transform faults, and subduction zones put the full life cycle of oceanic crust on display in the abyss, revealing constructive and destructive forces over wide ranges in time and space. Geochemically, the abyssal pressure regime influences the solubility of constituents such as silica and carbonate, and extremely high-temperature fluid-rock reactions in the shallow subsurface lead to distinctive and potentially unique geochemical profiles. Microbial residents range from low-abundance, low-energy communities on the abyssal plains to fast growing thermophiles at hydrothermal vents. Given its spatial extent and position as an intermediate zone between coastal and deep hadal settings, the abyss represents a lynchpin in global-scale processes such as nutrient and energy flux, population structure, and biogeographic diversity. Taken together, the abyssal ocean contributes critical ecosystem services while facing acute and diffuse anthropogenic threats from deep-sea mining, pollution, and climate change.We would like to thank the National Science Foundation for their support through grants NSF 2009117 and 2129431 to SAS

LKR/SDH Plays Important Roles throughout the Tick Life Cycle Including a Long Starvation Period

BACKGROUND:Lysine-ketoglutarate reductase/saccharopine dehydrogenase (LKR/SDH) is a bifunctional enzyme catalyzing the first two steps of lysine catabolism in plants and mammals. However, to date, the properties of the lysine degradation pathway and biological functions of LKR/SDH have been very little described in arthropods such as ticks. METHODOLOGY/PRINCIPAL FINDINGS:We isolated and characterized the gene encoding lysine-ketoglutarate reductase (LKR, EC 1.5.1.8) and saccharopine dehydrogenase (SDH, EC 1.5.1.9) from a tick, Haemaphysalis longicornis, cDNA library that encodes a bifunctional polypeptide bearing domains similar to the plant and mammalian LKR/SDH enzymes. Expression of LKR/SDH was detected in all developmental stages, indicating an important role throughout the tick life cycle, including a long period of starvation after detachment from the host. The LKR/SDH mRNA transcripts were more abundant in unfed and starved ticks than in fed and engorged ticks, suggesting that tick LKR/SDH are important for the starved tick. Gene silencing of LKR/SDH by RNAi indicated that the tick LKR/SDH plays an integral role in the osmotic regulation of water balance and development of eggs in ovary of engorged females. CONCLUSIONS/SIGNIFICANCE:Transcription analysis and gene silencing of LKR/SDH indicated that tick LKR/SDH enzyme plays not only important roles in egg production, reproduction and development of the tick, but also in carbon, nitrogen and water balance, crucial physiological processes for the survival of ticks. This is the first report on the role of LKR/SDH in osmotic regulation in animals including vertebrate and arthropods

Genome Sequence of a Mesophilic Hydrogenotrophic Methanogen Methanocella paludicola, the First Cultivated Representative of the Order Methanocellales

We report complete genome sequence of a mesophilic hydrogenotrophic methanogen Methanocella paludicola, the first cultured representative of the order Methanocellales once recognized as an uncultured key archaeal group for methane emission in rice fields. The genome sequence of M. paludicola consists of a single circular chromosome of 2,957,635 bp containing 3004 protein-coding sequences (CDS). Genes for most of the functions known in the methanogenic archaea were identified, e.g. a full complement of hydrogenases and methanogenesis enzymes. The mixotrophic growth of M. paludicola was clarified by the genomic characterization and re-examined by the subsequent growth experiments. Comparative genome analysis with the previously reported genome sequence of RC-IMRE50, which was metagenomically reconstructed, demonstrated that about 70% of M. paludicola CDSs were genetically related with RC-IMRE50 CDSs. These CDSs included the genes involved in hydrogenotrophic methane production, incomplete TCA cycle, assimilatory sulfate reduction and so on. However, the genetic components for the carbon and nitrogen fixation and antioxidant system were different between the two Methanocellales genomes. The difference is likely associated with the physiological variability between M. paludicola and RC-IMRE50, further suggesting the genomic and physiological diversity of the Methanocellales methanogens. Comparative genome analysis among the previously determined methanogen genomes points to the genome-wide relatedness of the Methanocellales methanogens to the orders Methanosarcinales and Methanomicrobiales methanogens in terms of the genetic repertoire. Meanwhile, the unique evolutionary history of the Methanocellales methanogens is also traced in an aspect by the comparative genome analysis among the methanogens

Data from: Using CRISPRs as a metagenomic tool to identify microbial hosts of a diffuse flow hydrothermal vent viral assemblage

Metagenomic analyses of viruses have revealed widespread diversity in the viriosphere, but it remains a challenge to identify specific hosts for a viral assemblage. To address this problem, we analyze the viral metagenome of a northeast Pacific hydrothermal vent with a comprehensive database of spacers derived from the CRISPR (Clustered Regularly Interspaced Short Palindromic Repeat) putative immune system. CRISPR spacer matches to the marine vent virome suggest that viruses infecting hosts from diverse taxonomic groups are present in this vent environment. Comparative virome analyses show that CRISPR spacers from vent isolates and from thermophiles in general have a higher percentage of matches to the vent virome than to other marine or terrestrial hot spring viromes. However, a high percentage of hits to spacers from mesophilic hosts, combined with a moderately high modeled alpha diversity, suggest that the marine vent virome is comprised of viruses that have the potential to infect diverse taxonomic groups of multiple thermal regimes in both the bacterial and archaeal domains

Genome-resolved metagenomics and metatranscriptomics reveal niche differentiation in functionally redundant microbial communities at deep-sea hydrothermal vents

International audienceThe structure and function of microbial communities inhabiting the subseafloor near hydrothermal systems are influenced by fluid geochemistry, geologic setting and fluid flux between vent sites, as well as biological interactions. Here, we used genome-resolved metagenomics and metatranscriptomics to examine patterns of gene abundance and expression and assess potential niche differentiation in microbial communities in venting fluids from hydrothermal vent sites at the Mid-Cayman Rise. We observed similar patterns in gene and transcript abundance between two geochemically distinct vent fields at the community level but found that each vent site harbours a distinct microbial community with differing transcript abundances for individual microbial populations. Through an analysis of metabolic pathways in 64 metagenome-assembled genomes (MAGs), we show that MAG transcript abundance can be tied to differences in metabolic pathways and to potential metabolic interactions between microbial populations, allowing for niche-partitioning and divergence in both population distribution and activity. Our results illustrate that most microbial populations have a restricted distribution within the seafloor, and that the activity of those microbial populations is tied to both genome content and abiotic factors