Subseafloor microbial communities in hydrogen‐rich vent fluids from hydrothermal systems along the Mid‐Cayman Rise

Summary Warm fluids emanating from hydrothermal vents can be used as windows into the rocky subseafloor habitat and its resident microbial community. Two new vent systems on the Mid‐Cayman Rise each exhibits novel geologic settings and distinctively hydrogen‐rich vent fluid compositions. We have determined and compared the chemistry, potential energy yielding reactions, abundance, community composition, diversity, and function of microbes in venting fluids from both sites: Piccard, the world's deepest vent site, hosted in mafic rocks; and Von Damm, an adjacent, ultramafic‐influenced system. Von Damm hosted a wider diversity of lineages and metabolisms in comparison to Piccard, consistent with thermodynamic models that predict more numerous energy sources at ultramafic systems. There was little overlap in the phylotypes found at each site, although similar and dominant hydrogen‐utilizing genera were present at both. Despite the differences in community structure, depth, geology, and fluid chemistry, energetic modelling and metagenomic analysis indicate near functional equivalence between Von Damm and Piccard, likely driven by the high hydrogen concentrations and elevated temperatures at both sites. Results are compared with hydrothermal sites worldwide to provide a global perspective on the distinctiveness of these newly discovered sites and the interplay among rocks, fluid composition and life in the subseafloor.

[1]  Geoffrey S. Cook,et al.  A hydrothermal seep on the Costa Rica margin: middle ground in a continuum of reducing ecosystems , 2012, Proceedings of the Royal Society B: Biological Sciences.

[2]  Deborah S. Kelley,et al.  Volcanoes, Fluids, and Life at Mid-Ocean Ridge Spreading Centers , 2002 .

[3]  Anna-Louise Reysenbach,et al.  Microbial community structure of hydrothermal deposits from geochemically different vent fields along the Mid-Atlantic Ridge. , 2011, Environmental microbiology.

[4]  Ken Takai,et al.  Hydrogen-driven subsurface lithoautotrophic microbial ecosystems (SLiMEs): do they exist and why should we care? , 2005, Trends in microbiology.

[5]  Paul A. Tyler,et al.  Hydrothermal vent fields and chemosynthetic biota on the world's deepest seafloor spreading centre , 2012, Nature Communications.

[6]  T. Nunoura,et al.  Comparison of microbial communities associated with phase-separation-induced hydrothermal fluids at the Yonaguni Knoll IV hydrothermal field, the Southern Okinawa Trough. , 2009, FEMS microbiology ecology.

[7]  Torsten Seemann,et al.  Genomic Insights to Control the Emergence of Vancomycin-Resistant Enterococci , 2013, mBio.

[8]  T. McCollom Geochemical constraints on sources of metabolic energy for chemolithoautotrophy in ultramafic-hosted deep-sea hydrothermal systems. , 2007, Astrobiology.

[9]  J. Baross,et al.  Low archaeal diversity linked to subseafloor geochemical processes at the Lost City Hydrothermal Field, Mid-Atlantic Ridge. , 2004, Environmental microbiology.

[10]  Kenneth W. Doherty,et al.  A new gas-tight isobaric sampler for hydrothermal fluids , 2002 .

[11]  M. Zolotov,et al.  Experimental investigation of single carbon compounds under hydrothermal conditions , 2006 .

[12]  Steven L Salzberg,et al.  Fast gapped-read alignment with Bowtie 2 , 2012, Nature Methods.

[13]  K. Horikoshi,et al.  Deep-sea vent ε-proteobacterial genomes provide insights into emergence of pathogens , 2007, Proceedings of the National Academy of Sciences.

[14]  W. Brazelton,et al.  Metagenomic Evidence for H2 Oxidation and H2 Production by Serpentinite-Hosted Subsurface Microbial Communities , 2012, Front. Microbio..

[15]  J. Huber,et al.  Modeling the Impact of Diffuse Vent Microorganisms Along Mid‐Ocean Ridges and Flanks , 2013 .

[16]  Susan M. Huse,et al.  Isolated communities of Epsilonproteobacteria in hydrothermal vent fluids of the Mariana Arc seamounts. , 2010, FEMS microbiology ecology.

[17]  T. Thomas,et al.  Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts , 2012, Proceedings of the National Academy of Sciences.

[18]  J. Mcdermott,et al.  The origin of methanethiol in midocean ridge hydrothermal fluids , 2014, Proceedings of the National Academy of Sciences.

[19]  William J. Brazelton,et al.  Bacterial Communities Associated with Subsurface Geochemical Processes in Continental Serpentinite Springs , 2013, Applied and Environmental Microbiology.

[20]  Thomas M. McCollom,et al.  Catabolic and anabolic energy for chemolithoautotrophs in deep-sea hydrothermal systems hosted in different rock types , 2011 .

[21]  D. Lovley,et al.  A hydrogen-based subsurface microbial community dominated by methanogens , 2002, Nature.

[22]  K. Horikoshi,et al.  Deep-sea vent epsilon-proteobacterial genomes provide insights into emergence of pathogens. , 2007, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Satoshi Nakagawa,et al.  Cell proliferation at 122°C and isotopically heavy CH4 production by a hyperthermophilic methanogen under high-pressure cultivation , 2008, Proceedings of the National Academy of Sciences.

[24]  R. Amann,et al.  Novel microbial communities of the Haakon Mosby mud volcano and their role as a methane sink , 2006, Nature.

[25]  E. Shock,et al.  Geochemical constraints on chemolithoautotrophic metabolism by microorganisms in seafloor hydrothermal systems. , 1997, Geochimica et cosmochimica acta.

[26]  Kentaro Nakamura,et al.  Compositional, Physiological and Metabolic Variability in Microbial Communities Associated with Geochemically Diverse, Deep-Sea Hydrothermal Vent Fluids , 2010 .

[27]  Kentaro Nakamura,et al.  Ultramafics-Hydrothermalism-Hydrogenesis-HyperSLiME (UltraH3) linkage: a key insight into early microbial ecosystem in the Archean deep-sea hydrothermal systems , 2006 .

[28]  K. Lloyd,et al.  An Anaerobic Methane-Oxidizing Community of ANME-1b Archaea in Hypersaline Gulf of Mexico Sediments , 2006, Applied and Environmental Microbiology.

[29]  S. Hallam,et al.  Microbial community structure across fluid gradients in the Juan de Fuca Ridge hydrothermal system. , 2013, FEMS microbiology ecology.

[30]  W. Brazelton,et al.  Serpentinization, Carbon, and Deep Life , 2013 .

[31]  J. Huber,et al.  Microbiological characterization of post-eruption “snowblower” vents at Axial Seamount, Juan de Fuca Ridge , 2013, Front. Microbiol..

[32]  Susan M. Huse,et al.  Microbial Population Structures in the Deep Marine Biosphere , 2007, Science.

[33]  M. Sogin,et al.  A Filtering Method to Generate High Quality Short Reads Using Illumina Paired-End Technology , 2013, PloS one.

[34]  M. Coleman,et al.  Effect of depth and vent fluid composition on the carbon sources at two neighboring deep-sea hydrothermal vent fields (Mid-Cayman Rise) , 2015 .

[35]  Ken Takai,et al.  Geochemical and microbiological evidence for a hydrogen-based, hyperthermophilic subsurface lithoautotrophic microbial ecosystem (HyperSLiME) beneath an active deep-sea hydrothermal field , 2004, Extremophiles.

[36]  R. Amann,et al.  Multiple self-splicing introns in the 16S rRNA genes of giant sulfur bacteria , 2012, Proceedings of the National Academy of Sciences.

[37]  J. Mcdermott Geochemistry of deep-sea hydrothermal vent fluids from the Mid-Cayman Rise, Caribbean Sea , 2015 .

[38]  J. Charlou,et al.  Geochemistry of high H2 and CH4 vent fluids issuing from ultramafic rocks at the Rainbow hydrothermal field (36°14'N, MAR) , 2002 .

[39]  J. Baross,et al.  Physiological Differentiation within a Single-Species Biofilm Fueled by Serpentinization , 2011, mBio.

[40]  S. Plouviez,et al.  Characterization of vent fauna at the Mid-Cayman Spreading Center , 2015 .

[41]  K. Horikoshi,et al.  Rapid Detection and Quantification of Members of the Archaeal Community by Quantitative PCR Using Fluorogenic Probes , 2000, Applied and Environmental Microbiology.

[42]  Todd O. Stevens,et al.  Lithoautotrophic Microbial Ecosystems in Deep Basalt Aquifers , 1995, Science.

[43]  Dana R. Yoerger,et al.  A Serpentinite-Hosted Ecosystem: The Lost City Hydrothermal Field , 2005, Science.

[44]  Harald Strauss,et al.  The influence of ultramafic rocks on microbial communities at the Logatchev hydrothermal field, located 15 degrees N on the Mid-Atlantic Ridge. , 2007, FEMS microbiology ecology.

[45]  Masatsugu Horiuchi,et al.  London Radiation Symposium , 1963, Cell and tissue kinetics.

[46]  K. Nealson,et al.  Sulfurimonas autotrophica gen. nov., sp. nov., a novel sulfur-oxidizing epsilon-proteobacterium isolated from hydrothermal sediments in the Mid-Okinawa Trough. , 2003, International journal of systematic and evolutionary microbiology.

[47]  D. Moreira,et al.  Diversity of functional genes of methanogens, methanotrophs and sulfate reducers in deep-sea hydrothermal environments. , 2005, Environmental microbiology.

[48]  James R. Cole,et al.  rrndb: the Ribosomal RNA Operon Copy Number Database , 2001, Nucleic Acids Res..

[49]  D. Prieur,et al.  Comparison of microbial communities associated with three Atlantic ultramafic hydrothermal systems. , 2011, FEMS microbiology ecology.

[50]  B. Baker,et al.  The microbiology of deep-sea hydrothermal vent plumes: ecological and biogeographic linkages to seafloor and water column habitats , 2013, Front. Microbiol..

[51]  J. Baross,et al.  Temporal Changes in Archaeal Diversity and Chemistry in a Mid-Ocean Ridge Subseafloor Habitat , 2002, Applied and Environmental Microbiology.

[52]  Christopher R. German,et al.  Pathways for abiotic organic synthesis at submarine hydrothermal fields , 2015, Proceedings of the National Academy of Sciences.

[53]  M. Lilley,et al.  Elevated concentrations of formate, acetate and dissolved organic carbon found at the Lost City hydrothermal field , 2010 .

[54]  Folker Meyer,et al.  Genome of the Epsilonproteobacterial Chemolithoautotroph Sulfurimonas denitrificans , 2007, Applied and Environmental Microbiology.

[55]  J. Baross,et al.  Methane- and Sulfur-Metabolizing Microbial Communities Dominate the Lost City Hydrothermal Field Ecosystem , 2006, Applied and Environmental Microbiology.

[56]  R. Vrijenhoek,et al.  Molecular systematics of vestimentiferan tubeworms from hydrothermal vents and cold-water seeps , 1997 .

[57]  D. Gomez-Ibanez,et al.  A precision multi-sampler for deep-sea hydrothermal microbial mat studies , 2012 .

[58]  E. Baker,et al.  An authoritative global database for active submarine hydrothermal vent fields , 2013 .

[59]  Mirjam Perner,et al.  Geochemical constraints on the diversity and activity of H2 -oxidizing microorganisms in diffuse hydrothermal fluids from a basalt- and an ultramafic-hosted vent. , 2010, FEMS microbiology ecology.

[60]  Neil Hunter,et al.  Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. , 2002, Microbiology.

[61]  Karthik Anantharaman,et al.  Evidence for hydrogen oxidation and metabolic plasticity in widespread deep-sea sulfur-oxidizing bacteria , 2012, Proceedings of the National Academy of Sciences.

[62]  J. Huber,et al.  Phylogenetic diversity and functional gene patterns of sulfur-oxidizing subseafloor Epsilonproteobacteria in diffuse hydrothermal vent fluids , 2013, Front. Microbiol..

[63]  M. Lilley,et al.  Hydrogen-limited growth of hyperthermophilic methanogens at deep-sea hydrothermal vents , 2012, Proceedings of the National Academy of Sciences.

[64]  C. German,et al.  Sustained volcanically-hosted venting at ultraslow ridges: Piccard Hydrothermal Field, Mid-Cayman Rise , 2013 .

[65]  C. R. German,et al.  Diverse styles of submarine venting on the ultraslow spreading Mid-Cayman Rise , 2010, Proceedings of the National Academy of Sciences.

[66]  M. Coleman,et al.  Trophic regions of a hydrothermal plume dispersing away from an ultramafic‐hosted vent‐system: Von Damm vent‐site, Mid‐Cayman Rise , 2013 .

[67]  Kentaro Nakamura,et al.  Theoretical constraints of physical and chemical properties of hydrothermal fluids on variations in chemolithotrophic microbial communities in seafloor hydrothermal systems , 2014, Progress in Earth and Planetary Science.

[68]  J. Huber,et al.  Strain-level genomic variation in natural populations of Lebetimonas from an erupting deep-sea volcano , 2013, The ISME Journal.

[69]  Rudolf Amann,et al.  A single-cell sequencing approach to the classification of large, vacuolated sulfur bacteria. , 2011, Systematic and applied microbiology.

[70]  D. Nelson,et al.  Vacuolate-attached filaments: highly productive Ridgeia piscesae epibionts at the Juan de Fuca hydrothermal vents , 2009, Marine biology.

[71]  H. Teeling,et al.  Genome and physiology of a model Epsilonproteobacterium responsible for sulfide detoxification in marine oxygen depletion zones , 2011, Proceedings of the National Academy of Sciences.

[72]  F. Robb Faculty Opinions recommendation of Cell proliferation at 122 degrees C and isotopically heavy CH4 production by a hyperthermophilic methanogen under high-pressure cultivation. , 2008 .

[73]  A. Boetius,et al.  Mats of psychrophilic thiotrophic bacteria associated with cold seeps of the Barents Sea , 2012 .