Abstract
Thiomicrospira species are ubiquitously found in various marine environments and appear particularly common in hydrothermal vent systems. Members of this lineage are commonly classified as sulfur-oxidizing chemolithoautotrophs. Although sequencing of Thiomicrospira crunogena’s genome has revealed genes that encode enzymes for hydrogen uptake activity and for hydrogenase maturation and assembly, hydrogen uptake ability has so far not been reported for any Thiomicrospira species. We isolated a Thiomicrospira species (SP-41) from a deep sea hydrothermal vent and demonstrated that it can oxidize hydrogen. We show in vivo hydrogen consumption, hydrogen uptake activity in partially purified protein extracts and transcript abundance of hydrogenases during different growth stages. The ability of this strain to oxidize hydrogen opens up new perspectives with respect to the physiology of Thiomicrospira species that have been detected in hydrothermal vents and that have so far been exclusively associated with sulfur oxidation.
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References
Adams MW, Hall DO . (1979). Purification of the membrane-bound hydrogenase of Escherichia coli. Biochem J 183: 11–22.
Balch WE, Fox GE, Magrum LJ, Woese CR, Wolfe RS . (1979). Methanogens: reevaluation of a unique biological group. Microbiol Rev 43: 260–296.
Bradford MM . (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248–254.
Brazelton WJ, Schrenk MO, Kelley DS, Baross JA . (2006). Methane- and sulfur-metabolizing microbial communities dominate the Lost City hydrothermal field ecosystem. Appl Environ Microbiol 72: 6257–6270.
Brazelton WJ, Baross JA . (2010). Metagenomic comparison of two Thiomicrospira lineages inhabiting contrasting deep-sea hydrothermal environments. PLoS One 5: e13530.
Brazelton WJ, Ludwig KA, Sogin ML, Andreishcheva EN, Kelley DS, Shen CC et al. (2010). Archaea and bacteria with surprising microdiversity show shifts in dominance over 1,000-year time scales in hydrothermal chimneys. Proc Natl Acad Sci USA 107: 1612–1617.
Brinkhoff T, Muyzer G . (1997). Increased species diversity and extended habitat range of sulfur-oxidizing Thiomicrospira spp. Appl Environ Microbiol 63: 3789–3796.
Brinkhoff T, Muyzer G, Wirsen CO, Kuever J . (1999a). Thiomicrospira kuenenii sp. nov. and Thiomicrospira frisia sp. nov., two mesophilic obligately chemolithoautotrophic sulfur-oxidizing bacteria isolated from an intertidal mud flat. Int J Syst Bacteriol 49 (Pt 2): 385–392.
Brinkhoff T, Muyzer G, Wirsen CO, Kuever J . (1999b). Thiomicrospira chilensis sp. nov., a mesophilic obligately chemolithoautotrophic sulfuroxidizing bacterium isolated from a Thioploca mat. Int J Syst Bacteriol 49: 875–879.
Campbell BJ, Engel AS, Porter ML, Takai K . (2006). The versatile ɛ-proteobacteria: key players in sulphidic habitats. Nat Rev Microbiol 4: 458–468.
Dobrinski KP, Longo DL, Scott KM . (2005). The carbon-concentrating mechanism of the hydrothermal vent chemolithoautotroph Thiomicrospira crunogena. J Bacteriol 187: 5761–5766.
Dobrinski KP, Boller AJ, Scott KM . (2010). Expression and function of four carbonic anhydrase homologs in the deep-sea chemolithoautotroph Thiomicrospira crunogena. Appl Environ Microbiol 76: 3561–3567.
Fuchs G, Eitinger T, Heider J, Kemper B, Kothe E, Schink B et al. (2007) Allgemeine Mikrobiologie. Georg Thieme Verlag: Stuttgart, Germany.
Garbe-Schönberg D, Koschinsky A, Ratmeyer V, Jähmlich H, Westernströer U . (2006). KIPS - A new multiport valve-based all-teflon fluid sampling system for ROVs. Geophys Res Abstr 8: 07032.
Glöckner FO, Fuchs BM, Amann R . (1999). Bacterioplankton compositions of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Appl Environ Microbiol 65: 3721–3726.
Guindon S, Gascuel O . (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696–704.
Häring V, Conrad R . (1991). Kinetics of H2 oxidation in respiring and denitrifying Paracoccus denitrificans. FEMS Microbiol Lett 78: 259–264.
Heijnen JJ, Van Dijken JP . (1992). In search of a thermodynamic description of biomass yields for the chemotrophic growth of microorganisms. Biotechnol Bioeng 39: 833–858.
Jannasch HW, Mottl MJ . (1985). Geomicrobiology of deep-sea hydrothermal vents. Science 229: 717–725.
Jannasch HW, Wirsen CO, Nelson DC, Robertson LA . (1985). Thiomicrospira crunogena sp. nov., a colorless, sulfur-oxidizing bacterium from a deep-sea hydrothermal vent. Int J Syst Bacteriol 35: 422–424.
Klüber HD, Conrad R . (1993). Ferric iron-reducing Shewanella putrefaciens and N2-fixing Bradyrhizobium japonicum with uptake hydrogenase are unable to oxidize atmospheric H2 . FEMS Microbiol Lett 111: 337–341.
Knittel K, Kuever J, Meyerdierks A, Meinke R, Amann R, Brinkhoff T . (2005). Thiomicrospira arctica sp. nov. and Thiomicrospira psychrophila sp. nov., psychrophilic, obligately chemolithoautotrophic, sulfur-oxidizing bacteria isolated from marine Arctic sediments. Int J Syst Evol Microbiol 55: 781–786.
Koschinsky A, Garbe-Schönberg D, Sander S, Schmidt K, Gennerich H-H, Strauss H . (2008). Hydrothermal venting at pressure-temperature conditions above the critical point of seawater, 5°S on the Mid-Atlantic Ridge. Geology 36: 615–618.
Kuenen JG, Veldkamp H . (1972). Thiomicrospira pelophila, gen. n., sp. n., a new obligately chemolithotrophic colourless sulfur bacterium. Antonie Van Leeuwenhoek 38: 241–256.
Lane DJ . (1991). 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M, (eds) Nucleic Acid Techniques in Bacterial Systematics. John Wiley: Chichester, UK, pp 115–175.
Miroshnichenko ML, Bonch-Osmolovskaya EA . (2006). Recent developments in the thermophilic microbiology of deep-sea hydrothermal vents. Extremophiles 10: 85–96.
Muth E, Morschel E, Klein A . (1987). Purification and characterization of an 8-hydroxy-5-deazaflavin-reducing hydrogenase from the archaebacterium Methanococcus voltae. Eur J Biochem 169: 571–577.
Nishihara H, Igarashi Y, Kodama T . (1991). Hydrogenovibrio marinus gen. nov., sp. nov., a Marine Obligately Chemolithoautotrophic Hydrogen-Oxidizing Bacterium. Int J Syst Bacteriol 41: 130–133.
Nishihara H, Yaguchi T, Chung SY, Suzuki K, Yanagi M, Yamasato K et al. (1998). Phylogenetic position of an obligately chemoautotrophic, marine hydrogen-oxidizing bacterium, Hydrogenovibrio marinus, on the basis of 16 S rRNA gene sequences and two form I RuBisCO gene sequences. Arch Microbiol 169: 364–368.
Nishihara H, Miyata Y, Miyashita Y, Bernhard M, Pohlmann A, Friedrich B et al. (2001). Analysis of the molecular species of hydrogenase in the cells of an obligately chemolithoautotrophic, marine hydrogen-oxidizing bacterium Hydrogenovibrio marinus. Biosci Biotechnol Biochem 65: 2780–2784.
Olson JW, Maier RJ . (2002). Molecular hydrogen as an energy source for Helicobacter pylori. Science 298: 1788–1790.
Payne MJ, Chapman A, Cammack R . (1993). Evidence for an [Fe]-type hydrogenase in the parasitic protozoan Trichomonas vaginalis. FEBS Lett 317: 101–104.
Perner M, Bach W, Hentscher M, Koschinsky A, Garbe-Schönberg D, Streit WR et al. (2009). Short-term microbial and physico-chemical variability in low-temperature hydrothermal fluids near 5°S on the Mid-Atlantic Ridge. Environ Microbiol 11: 2526–2541.
Perner M, Petersen JM, Zielinski F, Gennerich HH, Seifert R . (2010). Geochemical constraints on the diversity and activity of H2-oxidizing microorganisms in diffuse hydrothermal fluids from a basalt- and an ultramafic-hosted vent. FEMS Microbiol Ecol 74: 55–71.
Perner M, Hentscher M, Rychlik N, Seifert R, Strauss H, Bach W . (2011). Driving forces behind the biotope structures in two low-temperature hydrothermal venting sites on the southern Mid-Atlantic Ridge. Environ Microbiol Rep 3: 727–737.
Perner M, Hansen M, Seifert R, Strauss H, Koschinsky A, Petersen S . (2013). Linking geology, fluid chemistry, and microbial activity of basalt- and ultramafic-hosted deep-sea hydrothermal vent environments. Geobiology 11: 340–355.
Perner M, Gonnella G, Kurtz S, LaRoche J . (2014). Handling temperature bursts reaching 464 degrees C: different microbial strategies in the Sisters Peak hydrothermal chimney. Appl Environ Microbiol 80: 4585–4598.
Petersen JM, Zielinski FU, Pape T, Seifert R, Moraru C, Amann R et al. (2011). Hydrogen is an energy source for hydrothermal vent symbioses. Nature 476: 176–180.
Rákhely G, Laurinavichene TV, Tsygankov AA, Kovács KL . (2007). The role of Hox hydrogenase in the H2 metabolism of Thiocapsa roseopersicina. Biochim Biophys Acta 1767: 671–676.
Ruby EG, Jannasch HW . (1982). Physiological characteristics of Thiomicrospira sp. Strain L-12 isolated from deep-sea hydrothermal vents. J Bacteriol 149: 161–165.
Sako Y, Takai K, Ishida Y, Uchida A, Katayama Y . (1996). Rhodothermus obamensis sp. nov., a modern lineage of extremely thermophilic marine bacteria. Int J Syst Bacteriol 46: 1099–1104.
Sarrazin J, Rodier P, Tivey MK, Singh H, Schultz A, Sarradin PM . (2009). A dual sensor device to estimate fluid flow velocity at diffuse hydrothermal vents. Deep Sea Res I: Oceanogr Res Papers 56: 2065–2074.
Scott KM, Sievert SM, Abril FN, Ball LA, Barrett CJ, Blake RA et al. (2006). The genome of deep-sea vent chemolithoautotroph Thiomicrospira crunogena XCL-2. PLoS Biol 4: e383.
Takai K, Hirayama H, Nakagawa T, Suzuki Y, Nealson KH, Horikoshi K . (2004). Thiomicrospira thermophila sp. nov., a novel microaerobic, thermotolerant, sulfur-oxidizing chemolithomixotroph isolated from a deep-sea hydrothermal fumarole in the TOTO caldera, Mariana Arc, Western Pacific. Int J Syst Evol Microbiol 54: 2325–2333.
Takai K, Campbell BJ, Cary SC, Suzuki M, Oida H, Nunoura T et al. (2005). Enzymatic and genetic characterization of carbon and energy metabolisms by deep-sea hydrothermal chemolithoautotrophic isolates of Epsilonproteobacteria. Appl Environ Microbiol 71: 7310–7320.
Vrede K, Heldal M, Norland S, Bratbak G . (2002). Elemental composition (C, N, P) and cell volume of exponentially growing and nutrient-limited bacterioplankton. Appl Environ Microbiol 68: 2965–2971.
Wallner G, Amann R, Beisker W . (1993). Optimizing fluorescent in situ hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms. Cytometry 14: 136–143.
Wankel SD, Germanovich LN, Lilley MD, Genc G, DiPerna CJ, Bradley AS et al. (2011). Influence of subsurface biosphere on geochemical fluxes from diffuse hydrothermal fluids. Nature Geosci 4: 461–468.
Wirsen CO, Brinkhoff T, Kuever J, Muyzer G, Molyneaux S, Jannasch HW . (1998). Comparison of a new Thiomicrospira strain from the mid-atlantic ridge with known hydrothermal vent isolates. Appl Environ Microbiol 64: 4057–4059.
Acknowledgements
We thank the captain and crew members of the RV Meteor as well as the ROV Kiel6000 (GEOMAR, Kiel) for helping us to obtain deep-sea vent samples. We thank Wenke Bahnsen and Dagmar Svensson for technical assistance in the laboratory. The work was supported by grants from the Deutsche Forschungsgemeinschaft (DFG) priority program 1144 ‘From Mantle to Ocean: Energy-, Material- and Life-cycles at Spreading Axes’.
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Hansen, M., Perner, M. A novel hydrogen oxidizer amidst the sulfur-oxidizing Thiomicrospira lineage. ISME J 9, 696–707 (2015). https://doi.org/10.1038/ismej.2014.173
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DOI: https://doi.org/10.1038/ismej.2014.173
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