Linking geology, fluid chemistry, and microbial activity of basalt‐ and ultramafic‐hosted deep‐sea hydrothermal vent environments

Hydrothermal fluids passing through basaltic rocks along mid-ocean ridges are known to be enriched in sulfide, while those circulating through ultramafic mantle rocks are typically elevated in hydrogen. Therefore, it has been estimated that the maximum energy in basalt-hosted systems is available through sulfide oxidation and in ultramafic-hosted systems through hydrogen oxidation. Furthermore, thermodynamic models suggest that the greatest biomass potential arises from sulfide oxidation in basalt-hosted and from hydrogen oxidation in ultramafic-hosted systems. We tested these predictions by measuring biological sulfide and hydrogen removal and subsequent autotrophic CO2 fixation in chemically distinct hydrothermal fluids from basalt-hosted and ultramafic-hosted vents. We found a large potential of microbial hydrogen oxidation in naturally hydrogen-rich (ultramafic-hosted) but also in naturally hydrogen-poor (basalt-hosted) hydrothermal fluids. Moreover, hydrogen oxidation-based primary production proved to be highly attractive under our incubation conditions regardless whether hydrothermal fluids from ultramafic-hosted or basalt-hosted sites were used. Site-specific hydrogen and sulfide availability alone did not appear to determine whether hydrogen or sulfide oxidation provides the energy for primary production by the free-living microbes in the tested hydrothermal fluids. This suggests that more complex features (e.g., a combination of oxygen, temperature, biological interactions) may play a role for determining which energy source is preferably used in chemically distinct hydrothermal vent biotopes.

[1]  H. Jannasch,et al.  Chemosynthetic microbial activity at Mid-Atlantic Ridge hydrothermal vent sites , 1993 .

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

[3]  R. Amann,et al.  Hydrogen is an energy source for hydrothermal vent symbioses , 2011, Nature.

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

[5]  Robert Robson,et al.  Hydrogen as a Fuel : Learning from Nature , 2001 .

[6]  D. Nelson,et al.  Characterization of Large, Autotrophic Beggiatoa spp. Abundant at Hydrothermal Vents of the Guaymas Basin , 1989, Applied and environmental microbiology.

[7]  Harald Strauss,et al.  Driving forces behind the biotope structures in two low-temperature hydrothermal venting sites on the southern Mid-Atlantic Ridge. , 2011, Environmental microbiology reports.

[8]  L. Bongers Energy Generation and Utilization in Hydrogen Bacteria , 1970, Journal of bacteriology.

[9]  E. Ruby,et al.  Physiological characteristics of Thiomicrospira sp. Strain L-12 isolated from deep-sea hydrothermal vents , 1982, Journal of bacteriology.

[10]  R. Maier,et al.  Molecular Hydrogen as an Energy Source for Helicobacter pylori , 2002, Science.

[11]  W. Seyfried,et al.  Compositional controls on vent fluids from ultramafic-hosted hydrothermal systems at mid-ocean ridges: An experimental study at 400°C, 500 bars , 2003 .

[12]  N. Pimenov,et al.  Carbon Dioxide Assimilation and Methane Oxidation in Various Zones of the Rainbow Hydrothermal Field , 2000, Microbiology.

[13]  G. Massoth,et al.  Mixing, Reaction and Microbial Activity in the Sub‐Seafloor Revealed by Temporal and Spatial Variation in Diffuse Flow Vents at Axial Volcano , 2013 .

[14]  Y. Sako,et al.  Distribution, phylogenetic diversity and physiological characteristics of epsilon-Proteobacteria in a deep-sea hydrothermal field. , 2005, Environmental microbiology.

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

[16]  Yohey Suzuki,et al.  Sulfurimonas paralvinellae sp. nov., a novel mesophilic, hydrogen- and sulfur-oxidizing chemolithoautotroph within the Epsilonproteobacteria isolated from a deep-sea hydrothermal vent polychaete nest, reclassification of Thiomicrospira denitrificans as Sulfurimonas denitrificans comb. nov. and emend , 2006, International journal of systematic and evolutionary microbiology.

[17]  C. A. Ward,et al.  Hydrogen as a fuel , 1983 .

[18]  Stefan Weber,et al.  Microbial CO(2) fixation and sulfur cycling associated with low-temperature emissions at the Lilliput hydrothermal field, southern Mid-Atlantic Ridge (9 degrees S). , 2007, Environmental microbiology.

[19]  J. Escartín,et al.  Oceanic detachment faults focus very large volumes of black smoker fluids , 2007 .

[20]  B. Tebo,et al.  In situ sulfide removal and CO2 fixation rates at deep-sea hydrothermal vents and the oxic/anoxic interface in Framvaren Fjord, Norway , 1999 .

[21]  G. Garrity,et al.  Class V. Epsilonproteobacteria class. nov. , 2005 .

[22]  S. Petersen,et al.  Fe–Si-oxyhydroxide deposits at a slow-spreading centre with thickened oceanic crust: The Lilliput hydrothermal field (9°33′S, Mid-Atlantic Ridge) , 2010 .

[23]  Joel D. Cline,et al.  SPECTROPHOTOMETRIC DETERMINATION OF HYDROGEN SULFIDE IN NATURAL WATERS1 , 1969 .

[24]  R. Conrad,et al.  Ferric iron-reducing Shewanella putrefaciens and N2-fixing Bradyrhizobium japonicum with uptake hydrogenase are unable to oxidize atmospheric H2 , 1993 .

[25]  J. Charlou,et al.  Geodiversity of hydrothermal processes along the Mid-Atlantic Ridge and ultramafic-hosted mineralization: A new type of oceanic Cu-Zn-Co-Au volcanogenic massive sulfide deposit , 2013 .

[26]  A. Koschinsky,et al.  Rare earth elements in mussel shells of the Mytilidae family as tracers for hidden and fossil high-temperature hydrothermal systems , 2010 .

[27]  H. G. Trüper Sulphur metabolism in Thiorhodaceae. II. stoichiometric relationship of CO2 fixation to oxidation of hydrogen sulphide and intracellular sulphur inChromatium okenii , 2005, Antonie van Leeuwenhoek.

[28]  A. Koschinsky,et al.  Fluid elemental and stable isotope composition of the Nibelungen hydrothermal field (8°18'S, Mid-Atlantic Ridge): Constraints on fluid-rock interaction in heterogeneous lithosphere , 2011 .

[29]  Dana R. Yoerger,et al.  First evidence for high-temperature off-axis venting of deep crustal/mantle heat: The Nibelungen hydrothermal field, southern Mid-Atlantic Ridge , 2008 .

[30]  Danielle M. Winget,et al.  Lysogenic virus–host interactions predominate at deep-sea diffuse-flow hydrothermal vents , 2008, The ISME Journal.

[31]  F. Azam,et al.  Microbes, Molecules, and Marine Ecosystems , 2004, Science.

[32]  S. Petersen,et al.  The geological setting of the ultramafic-hosted Logatchev hydrothermal field (14°45′N, Mid-Atlantic Ridge) and its influence on massive sulfide formation , 2009 .

[33]  R. Conrad,et al.  Kinetics of H2 oxidation in respiring and denitrifying Paracoccus denitrificans , 1991 .

[34]  J. H. Carpenter THE CHESAPEAKE BAY INSTITUTE TECHNIQUE FOR THE WINKLER DISSOLVED OXYGEN METHOD , 1965 .

[35]  D. Lovley,et al.  Hydrogen concentrations as an indicator of the predominant terminal electron-accepting reactions in aquatic sediments , 1988 .

[36]  E. Oelkers,et al.  The rainbow vent fluids (36°14′N, MAR): the influence of ultramafic rocks and phase separation on trace metal content in Mid-Atlantic Ridge hydrothermal fluids , 2002 .

[37]  J. Boonstra,et al.  Competition for inorganic substrates among chemoorganotrophic and chemolithotrophic bacteria , 1977, Microbial Ecology.

[38]  D. Yoerger,et al.  Young volcanism and related hydrothermal activity at 5°S on the slow‐spreading southern Mid‐Atlantic Ridge , 2007 .

[39]  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.

[40]  P. Girguis,et al.  In situ chemistry and microbial community compositions in five deep-sea hydrothermal fluid samples from Irina II in the Logatchev field. , 2013, Environmental microbiology.

[41]  A. Koschinsky,et al.  Short-term microbial and physico-chemical variability in low-temperature hydrothermal fluids near 5 degrees S on the Mid-Atlantic Ridge. , 2009, Environmental microbiology.

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

[43]  A. Koschinsky,et al.  KIPS -A new Multiport Valve-based all-Teflon Fluid Sampling System for ROVs , 2006 .

[44]  W. Martens-Habbena,et al.  Impact of Different In Vitro Electron Donor/Acceptor Conditions on Potential Chemolithoautotrophic Communities from Marine Pelagic Redoxclines , 2005, Applied and Environmental Microbiology.

[45]  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.

[46]  E. Ruby,et al.  Chemolithotrophic Sulfur-Oxidizing Bacteria from the Galapagos Rift Hydrothermal Vents , 1981, Applied and environmental microbiology.

[47]  J. G. Kuenen,et al.  Growth physiology and competitive interaction of obligately chemolithoautotrophic, haloalkaliphilic, sulfur-oxidizing bacteria from soda lakes , 2003, Extremophiles.

[48]  B. Campbell,et al.  The versatile ε-proteobacteria: key players in sulphidic habitats , 2006, Nature Reviews Microbiology.

[49]  A. Koschinsky,et al.  Geochemistry of hydrothermal fluids from the ultramafic-hosted Logatchev hydrothermal field, 15°N on the Mid-Atlantic Ridge: Temporal and spatial investigation , 2007 .

[50]  Y. Sorokin The Bacterial Population and the Processes of Hydrogen Sulphide Oxidation in the Black Sea , 1972 .

[51]  K. Haase,et al.  Diking, young volcanism and diffuse hydrothermal activity on the southern Mid-Atlantic Ridge: The Lilliput field at 9°33'S , 2009 .

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