Petersen Jillian M 0000-0002-9852-3445 Zielinski Frank U Pape Thomas tpape@marum.de 0000-0002-6872-2144 Seifert Richard seifert@geowiss.uni-hamburg.de http://www.geowiss.uni-hamburg.de/i-bioge/start.html Moraru Cristina Amann Rudolf 0000-0002-0846-7372 Hourdez Stéphane Girguis Peter R 0000-0002-3599-8160 Wankel Scott D Barbe Valerie 0000-0002-8162-3343 Pelletier Eric 0000-0003-4228-1712 Fink Dennis Borowski Christian cborowsk@mpi-bremen.de 0000-0001-7921-3022 Bach Wolfgang wbach@uni-bremen.de https://www.marum.de/en/Wolfgang-Bach.html 0000-0002-3099-7142 Dubilier Nicole ndubilie@mpi-bremen.de http://www.marum.de/Nicole_Dubilier.html 0000-0002-9394-825X 2011 Results of H2-consumption experiments during METEOR cruise M64/2 dataset https://doi.org/10.1594/PANGAEA.807171 https://doi.org/10.1594/PANGAEA.810465 The discovery of deep-sea hydrothermal vents in 1977 revolutionized our understanding of the energy sources that fuel primary productivity on Earth. Hydrothermal vent ecosystems are dominated by animals that live in symbiosis with chemosynthetic bacteria. So far, only two energy sources have been shown to power chemosynthetic symbioses: reduced sulphur compounds and methane. Using metagenome sequencing, single-gene fluorescence in situ hybridization, immunohistochemistry, shipboard incubations and in situ mass spectrometry, we show here that the symbionts of the hydrothermal vent mussel Bathymodiolus from the Mid-Atlantic Ridge use hydrogen to power primary production. In addition, we show that the symbionts of Bathymodiolus mussels from Pacific vents have hupL, the key gene for hydrogen oxidation. Furthermore, the symbionts of other vent animals such as the tubeworm Riftia pachyptila and the shrimp Rimicaris exoculata also have hupL. We propose that the ability to use hydrogen as an energy source is widespread in hydrothermal vent symbioses, particularly at sites where hydrogen is abundant. Lackschewitz Klas Sven klackschewitz@geomar.de Armini M Augustin Nico Nico.Agustin@kaust.edu.sa 0000-0003-1905-4773 Dubilier Nicole ndubilie@mpi-bremen.de http://www.marum.de/Nicole_Dubilier.html 0000-0002-9394-825X Edge David Engemann Greg Fabian M Felden Janine janine.felden@awi.de https://www.awi.de/en/about-us/organisation/staff/single-view/janine-felden.html 0000-0002-4177-6644 Franke Philipp Gärtner Andrea Garbe-Schönberg Dieter dieter.garbe-schoenberg@ifg.uni-kiel.de 0000-0001-9006-9463 Gennerich Hans-Hermann hherm@uni-bremen.de Hüttig D Marbler Herwig h.marbler@jacobs-university.de Meyerdierks Anke ameyerdi@mpi-bremen.de 0000-0002-8834-5446 Pape Thomas tpape@marum.de 0000-0002-6872-2144 Perner Kerstin kerstin.perner@io-warnemuende.de http://www.io-warnemuende.de/kerstin-perner.html 0000-0002-7464-2191 Reuter Markus 0000-0003-2988-8368 Ruhland Götz gruhland@uni-bremen.de Schmidt K 0000-0002-6488-623X Schott Thorsten Schröder Michael michael.schroeder@awi.de https://www.awi.de/en/about-us/organisation/staff/single-view/michael-schroeder.html Schroll G Seiter Christian Stecher Jens jstecher@senckenberg.de Strauss Harald hstrauss@uni-muenster.de Viehweger Marc Weber Stefan stefan.weber@uni-hamburg.de Wenzhöfer Frank frank.wenzhoefer@awi.de https://www.awi.de/en/about-us/organisation/staff/single-view/frank-wenzhoefer.html Zielinski Frank frank.zielinski@ufz.de 2005 Mid-Atlantic Expedition 2005, Cruise No. 64, Leg 2, Longterm study of hydrothermalism and biology at the Logatchev field, Mid-Atlantic Ridge at 14°45' N (revisit 2005, HYDROMAR II), 6 May - 6 June 2005, Fortaleza (Brazil) - Dakar (Senegal) METEOR-Berichte, Leitstelle Meteor, Institut für Meereskunde der Universität Hamburg 05 hdl:10013/epic.32337.d001 171 pp Petersen Jillian M 0000-0002-9852-3445 Zielinski Frank U Pape Thomas tpape@marum.de 0000-0002-6872-2144 Seifert Richard seifert@geowiss.uni-hamburg.de http://www.geowiss.uni-hamburg.de/i-bioge/start.html Moraru Cristina Amann Rudolf 0000-0002-0846-7372 Hourdez Stéphane Girguis Peter R 0000-0002-3599-8160 Wankel Scott D Barbe Valerie 0000-0002-8162-3343 Pelletier Eric 0000-0003-4228-1712 Fink Dennis Borowski Christian cborowsk@mpi-bremen.de 0000-0001-7921-3022 Bach Wolfgang wbach@uni-bremen.de https://www.marum.de/en/Wolfgang-Bach.html 0000-0002-3099-7142 Dubilier Nicole ndubilie@mpi-bremen.de http://www.marum.de/Nicole_Dubilier.html 0000-0002-9394-825X 2011 Hydrogen is an energy source for hydrothermal vent symbioses journal article Nature 476 https://doi.org/10.1038/nature10325 176-180 Zielinski Frank frank.zielinski@ufz.de 2009 Geobiological coupling of hydrothermal vent fluids with endosymbiotic primary producers of bathymodiolus mussels from hydrothermal vents on the Mid-Atlantic Ridge dissertation University of Bremen, Germany urn:nbn:de:gbv:46-diss000115375 159 pp -44.9802 -44.9778 14.7517 14.7535 -44.97902 14.7529 2005-05-17T00:00:00 2005-05-26T00:00:00 -3053.0 -3003.0 irregular surface DERIDGE From Mantle to Ocean: Energy-, Material- and Life-cycles at Spreading Axes https://www.geomar.de/forschen/fb4/fb4-muhs/projekte/spp1144/ Research Center for Marine Geosciences at Christian Albrechts University, Kiel Geomar http://www.geomar.de/en/ German Research Foundation DFG http://www.dfg.de/en/ https://doi.org/10.13039/501100001659 5471797 From Mantle to Ocean: Energy-, Material- and Life-cycles at Spreading Axes https://gepris.dfg.de/project/5471797 M64/2-244-ROV 14.753 -44.9788 Mid-Atlantic Ridge at 10-15°N -3032.0 2005-05-17T00:00:00 M64/2 M64/2 HYDROMAR2 HYDROMAR2 Fortaleza, Brazil 2005-05-06T00:00:00 2005-05-06 Dakar, Senegal https://www.geonames.org/2253350/dakar.html 2005-06-06T00:00:00 2005-06-06 Meteor (1986) https://en.wikipedia.org/wiki/RV_Meteor_(1986) DBBH 8411279 Lackschewitz, Klas Sven Lackschewitz, Klas Sven doi:10.2312/cr_m64 20060213 hdl:10013/epic.44784.d016 hdl:10013/epic.44803.d075 Meteor (1986) https://en.wikipedia.org/wiki/RV_Meteor_(1986) DBBH 8411279 Remote operated vehicle ROV IRINA II; OBT and OBP positioned, biological sampling M64/2-263-ROV 14.7533 -44.9793 Mid-Atlantic Ridge at 10-15°N -3045.0 2005-05-22T00:00:00 M64/2 M64/2 HYDROMAR2 HYDROMAR2 Fortaleza, Brazil 2005-05-06T00:00:00 2005-05-06 Dakar, Senegal https://www.geonames.org/2253350/dakar.html 2005-06-06T00:00:00 2005-06-06 Meteor (1986) https://en.wikipedia.org/wiki/RV_Meteor_(1986) DBBH 8411279 Lackschewitz, Klas Sven Lackschewitz, Klas Sven doi:10.2312/cr_m64 20060213 hdl:10013/epic.44784.d016 hdl:10013/epic.44803.d075 Meteor (1986) https://en.wikipedia.org/wiki/RV_Meteor_(1986) DBBH 8411279 Remote operated vehicle ROV IRINA II, QUEST; Biological sampling, OBT re-positioning M64/2-266-ROV 14.753 -44.979 Mid-Atlantic Ridge at 10-15°N -3034.0 2005-05-23T00:00:00 14.7517 -44.9778 -3003.0 M64/2 M64/2 HYDROMAR2 HYDROMAR2 Fortaleza, Brazil 2005-05-06T00:00:00 2005-05-06 Dakar, Senegal https://www.geonames.org/2253350/dakar.html 2005-06-06T00:00:00 2005-06-06 Meteor (1986) https://en.wikipedia.org/wiki/RV_Meteor_(1986) DBBH 8411279 Lackschewitz, Klas Sven Lackschewitz, Klas Sven doi:10.2312/cr_m64 20060213 hdl:10013/epic.44784.d016 hdl:10013/epic.44803.d075 Meteor (1986) https://en.wikipedia.org/wiki/RV_Meteor_(1986) DBBH 8411279 Remote operated vehicle ROV IRINA II and Site B; Profiler and biological sampling, Fluid sampling M64/2-281-ROV 14.7535 -44.9802 Mid-Atlantic Ridge at 10-15°N -3053.0 2005-05-26T00:00:00 M64/2 M64/2 HYDROMAR2 HYDROMAR2 Fortaleza, Brazil 2005-05-06T00:00:00 2005-05-06 Dakar, Senegal https://www.geonames.org/2253350/dakar.html 2005-06-06T00:00:00 2005-06-06 Meteor (1986) https://en.wikipedia.org/wiki/RV_Meteor_(1986) DBBH 8411279 Lackschewitz, Klas Sven Lackschewitz, Klas Sven doi:10.2312/cr_m64 20060213 hdl:10013/epic.44784.d016 hdl:10013/epic.44803.d075 Meteor (1986) https://en.wikipedia.org/wiki/RV_Meteor_(1986) DBBH 8411279 Remote operated vehicle ROV QUEST; Benthic chamber deployed at IRINA II, fluid, biological and geological sampling at QUEST site 986 CC-BY-3.0 Creative Commons Attribution 3.0 Unported https://creativecommons.org/licenses/by/3.0/ Hydrogen consumption incubations Sampling site: For on-board physiological experiments specimens of Bathymodiolus puteoserpentis were sampled at the Logatchev hydrothermal vent field on the northern MAR. Mussels were sampled using nets (40 cm length, 20 cm diameter opening, mesh size 335 µm [Hydrobios, Kiel, Germany]) handled by the manipulator arm of the remotely operated vehicles (ROVs) Quest 4000 m (MARUM, Bremen, Germany). Mussel dissection for shipboard incubations: For hydrogen consumption experiments, tissues from three individuals were used in each experiment. Mussels were opened with a scalpel by cutting through the posterior and anterior adductor muscles. Viability was tested by prodding the foot with a dissection needle and only mussels whose foot contracted were used. The foot and both gills were separated from the remaining tissue using dissection scissors. Tissue pieces of 6 mm in diameter were cut out of the gill and the foot tissues using a steel hole-puncher. One tissue piece from each individual was frozen in liquid nitrogen for weight determination in the home laboratory. The mean wet weight was 34.2 mg +/- 10.5 mg (n=18). For negative controls, foot tissues that do not contain endosymbiotic bacteria and boiled gill tissues were used. Experimental setup: Glass serum vials (58 ml) were fully filled with chilled (4°C) sterile-filtered (0.22 µm) bottom seawater retrieved from 3000 m water depth. One piece of gill tissue was placed in the vial, the vial closed with a gas-tight rubber stopper avoiding any inclusion of air bubbles, and crimped with aluminum seals. Control vials contained foot tissue, boiled gill tissue or no tissue at all. 20 ml of hydrogen gas (100 ppm in helium, Linde) were injected through the rubber stopper using a gas-tight syringe with a second syringe allowing pressure compensation through the outflow of seawater. All vials were placed up-side down to avoid possible gas exchange via the rubber stopper and incubated at 4°C on a slowly rotating table. At given time points a subsample was taken with a gas-tight syringe from the headspace with the pressure decrease compensated through the inflow of chilled sterile-filtered seawater from a second syringe. Analysis of the headspace hydrogen content: The hydrogen concentration in the headspace was determined using a gas chromatograph (Thermo Trace GC ultra) equipped with a packed stainless steel column (Molecular Sieve 5A, carrier gas: He) and a pulse discharge detector (PDD). Recording and calculation of results was performed using a PC operated integration system (Thermo Chrom Card A/D). Analytical procedures were calibrated daily with commercial gas standards (Linde). Incubation conditions and rate calculations: The concentrations of dissolved hydrogen and oxygen were calculated from Crozier and Yamamoto (1974) [Solubility of hydrogen in water, seawater, and NaCl solutions. Journal of Chemical and Engineering Data, 19(3), 242-244, doi:10.1021/je60062a007] and Weiss (1970) [Weiss, Ray F (1970): Solubility of nitrogen, oxygen and argon in water and seawater. Deep Sea Research Part I: Oceanographic Research Papers, 17, 721-735, doi:10.1016/0011-7471(70)90037-9] under the assumption of Henry's law i.e. that the concentration of a dissolved gas in a solution is directly proportional to the partial pressure of that gas above the solution. The molar volume of an ideal gas (22.414 l mol-1) was used to convert between the partial pressure of a gas (ppm) and the amount of the gas (in moles) in the headspace. The rates of hydrogen removal from the headspace [in nmol h-1 (piece tissue)-1] were calculated for the first 60 minutes after addition of the electron source performing non-linear regression through the data points obtained during the complete incubation period of up to 60 hours. Exponential and hyperbolic regression described by the equations f=a*exp(b/(x+c)) and f=y0+(a*b)/(b+x) gave well-fitting regression curves (R2 = 0.920 and 0.921, respectively; standard error of estimate 6.434 and 6.400, respectively). The effect of methodological hydrogen removal from the headspace through subsampling was considered. The rates at which hydrogen disappeared from incubation vials containing only seawater but no tissues (chemical oxidation, hydrogen loss by diffusion) were subtracted from the tissue rates. Resulting rates were then normalized to gram wet weight (in nmol h-1 [g wet weight]-1). Event label Event Event Sample ID Sample ID Zielinski Frank frank.zielinski@ufz.de Sample ID Time in minutes Time min min Time T http://dbpedia.org/resource/Time Zielinski Frank frank.zielinski@ufz.de Time min [min] Hydrogen H2 ppmv hydrogen Zielinski Frank frank.zielinski@ufz.de headspace H2 [ppmv] Hydrogen concentration H2 nmol Amount of Substance N http://dbpedia.org/resource/Amount_of_substance Zielinski Frank frank.zielinski@ufz.de dissolved H2 [nmol] Wet mass Wet m mg wet mass Mass M http://dbpedia.org/resource/Mass Zielinski Frank frank.zielinski@ufz.de Wet m [mg] Hydrogen consumption rate H2 cons rate nmol/h Catalytic Activity http://dbpedia.org/resource/Catalysis Zielinski Frank frank.zielinski@ufz.de per gill tissue piece H2 cons rate [nmol/h] Hydrogen consumption rate per weight H2 cons rate nmol/h/g Weight http://dbpedia.org/resource/Weight Specific Activity http://search.ebscohost.com/login.aspx?direct=true&db=nlebk&AN=98508&site=ehost-live&ebv=EB&ppid=pp_610 Zielinski Frank frank.zielinski@ufz.de normalized to wet weight H2 cons rate [nmol/h/g] Comment Comment Zielinski Frank frank.zielinski@ufz.de related to H2 consumption rate Comment citable deNBIchemical author10407 author20257 author21730 author21933 author22511 author26521 author28084 author28857 author29589 author29735 author30034 author30038 author30476 author30670 author30795 author30805 author31095 author32400 author32402 author33322 author34326 author34426 author34648 author34884 author34903 author35200 author35201 author35209 author35219 author35221 author35222 author35223 author35224 author35225 author35226 author36453 author36655 author39220 author39221 author39222 author39223 author39224 author617 award112 basis2 campaign27829 campaign3375826 event2382113 event2382132 event2382135 event2382150 funder20472 geocode1599 geocode1600 geocode1601 geocode8128 inst20038 journal11658 journal16725 license101 method11520 param105457 param122890 param122891 param123142 param1570 param16065 param5058 param53104 pi28857 project4042 ref27348 ref34797 ref39232 term22566 term33871 term38563 term40811 term43762 term43783 term43892 term43975 term43989 term44032 term75846 term77700 topotype6