Extremophiles

, Volume 8, Issue 4, pp 317–323

The first evidence of anaerobic CO oxidation coupled with H2 production by a hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent

  • Tatyana G. Sokolova
  • Christian Jeanthon
  • Nadezhda A. Kostrikina
  • Nikolai A. Chernyh
  • Alexander V. Lebedinsky
  • Erko Stackebrandt
  • Elizaveta A. Bonch-Osmolovskaya
Original Paper

Abstract

From 24 samples of hydrothermal venting structures collected at the East Pacific Rise (13°N), 13 enrichments of coccoid cells were obtained which grew on CO, producing H2 and CO2 at 80°C. A hyperthermophilic archaeon capable of lithotrophic growth on CO coupled with equimolar production of H2 was isolated. Based on its 16S rRNA sequence analysis, this organism was affiliated with the genus Thermococcus. Other strains of Thermococcales species (Pyrococcus furiosus, Thermococcus peptonophilus, T. profundus, T. chitonophagus, T. stetteri, T. gorgonarius, T. litoralis, and T. pacificus) were shown to be unable to grow on CO. Searches in sequence databases failed to reveal deposited sequences of genes related to CO metabolism in Thermococcales. Our work provides the first evidence of anaerobic CO oxidation coupled with H2 production performed by an archaeon as well as the first documented case of lithotrophic growth of a Thermococcales representative.

Keywords

Anaerobic CO oxidation Deep-sea hot vents Hyperthermophilic archaea Thermococcus 

References

  1. Baross JA, Deming JW (1983) Growth of “black smoker” bacteria at temperatures of at least 250°C. Nature 303:423–426Google Scholar
  2. Blöhl E, Rachel R, Burggraf S, Hafenbradl D, Jannasch HW, Stetter KO (1997) Pyrolobus fumarii gen. and sp. nov., represents a novel group of Archaea, extending the upper temperature limit for life to 113°C. Extremophiles 1:14–21CrossRefPubMedGoogle Scholar
  3. Bonch-Osmolovskaya EA, Miroshnichenko ML, Slobodkin AI, Sokolova TG, Karpov GA, Kostrikina NA, Zavarzina DG, Prokof’eva MI, Rusanov II, Pimenov NV (1999) Biodiversity of anaerobic lithotrophic prokaryotes in terrestrial hot springs of Kamchatka. Microbiology 68:343–351Google Scholar
  4. Burggraf S, Jannasch HW, Nicolaus B, Stetter KO (1990) Archaeoglobus profundus sp. nov., represents a new species within the sulphate-reducing archeabacteria. Syst Appl Microbiol 13:24–28Google Scholar
  5. Cary SC, Shank T, Stein J (1998) Worms bask in extreme temperatures. Nature 391:545–546CrossRefGoogle Scholar
  6. Charlou JL, Donval JP, Fouquet Y, Jean-Baptiste P, Holm N (2002) Geochemistry of high H2 and CH4 vent fluids issuing from ultramafic rocks at the Rainbow vent field (36 degrees 14′N, MAR). Chem Geol 191:345–359CrossRefGoogle Scholar
  7. Daniels L, Fuchs G, Thauer RK, Zeikus JG (1977) Carbon monoxide oxidation by methanogenic bacteria. J Bacteriol 132:118–126PubMedGoogle Scholar
  8. Drake HL (1994) Acetogenesis, acetogenic bacetria, and the acetyl-CoA “Wood/Ljungdahl” pathway: past and current perspectives. In: Drake HL (ed) Acetogenesis. Chapman and Hall, New York, pp 1–15Google Scholar
  9. Ensign SA (1995) Reactivity of carbon monoxide dehydrogenase from Rhodospirillum rubrum with carbon dioxide, carbonyl sulphide, and carbon disulphide. Biochemistry 34:5372–5381PubMedGoogle Scholar
  10. Fardeau ML, Bonilla Salinas M, L’Haridon S, Jeanthon C, Verhé F, Cayol JL, Patel BKC, Garcia JL, Ollivier B (2004) Isolation from oil reservoirs of novel thermophilic anaerobes phylogenetically related to Thermoanaerobacter subterraneus: reassignment of T. subterraneus, Thermoanaerobacter yonseiensis, Thermoanaerobacter tengcongensis and Carboxydibrachium pacificum to Caldanaerobacter subterraneus gen. nov., sp. nov., comb. nov. as four novel subspecies. Int J Syst Evol Microbiol 54:467–474CrossRefPubMedGoogle Scholar
  11. Felsenstein J (1993) PHYLIP (PHYlogenetic Inference Package), version 3.5c. Department of Genetics, University of Washington, SeattleGoogle Scholar
  12. Ferry, JG (1999) Enzymology of one-carbon metabolism in methanogenic pathways. FEMS Microbiol Rev 23:13–38CrossRefPubMedGoogle Scholar
  13. Fiala G, Stetter KO, Jannasch HW, Langworthy TA, Madon J (1986) Staphylothermus marinus sp. nov. represents a novel genus of extremely thermophilic submarine heterotrophic archaebacteria growing up to 98°C. Syst Appl Microbiol 8:106–113Google Scholar
  14. Fukui M, Teske A, Assmus B, Muyzer G, Widdel F (1999) Physiology, phylogenetic relationships, and ecology of filamentous sulfate-reducing bacteria (genus Desulfonema). Arch Microbiol 172:193–203 CrossRefPubMedGoogle Scholar
  15. Hekinian R, Fouquet Y (1985) Volcanism and metallogenesis of axial and off-axial structures on the East Pacific Rise near 13°N. Econ Geol 80:221–249Google Scholar
  16. Holden JF, Takai K, Summit M, Bolton S, Zykowski J, Baross JA (2001) Diversity of three novel groups of hyperthermophilic deep-sea Thermococcus species from three sites in the northeastern Pacific Ocean. FEMS Microbiol Ecol 36:51–60CrossRefPubMedGoogle Scholar
  17. Huber H, Burggraf S, Mayer T, Wyschkony I, Rachel R, Stetter KO (2000) Ignicoccus gen. nov., a novel genus of hyperthermophilic, chemolithoautotrophic Archaea, represented by two new species, Ignicoccus islandicus sp. nov. and Ignicoccus pacificus sp. nov. Int J Syst Evol Microbiol 50:2093–2100PubMedGoogle Scholar
  18. Kevbrin VV, Zavarzin GA (1992) The influence of sulfur compounds on the growth of halophilic homoacetic bacterium Acetohalobium arabaticum. Microbiology (English translation of Mikrobiologiya) 61:812–817Google Scholar
  19. Kostyukova AS, Gongadze GM, Polosina YY, Bonch-Osmolovskaya EA, Miroshnichenko ML, Chernyh NA, Obraztsova MV, Svetlichny VA, Messner P, Sleytr UB, L’Haridon S, Jeanthone C, Prieur D (1999) Investigation of structure and antigenic capacities of Thermococcales cell envelopes and reclassification of Caldococcus litoralis Z-1301 as Thermococcus litoralis Z-1301. Extremophiles 3:239–245CrossRefPubMedGoogle Scholar
  20. Kurr M, Huber R, König H, Jannasch HW, Fricke H, Trincone A, Kristjansson JK, Stetter KO (1991) Methanopyrus kandleri, gen. and sp. nov. represents a novel group of hyperthermophilic methanogens, growing at 110°C. Arch Microbiol 156:239–247Google Scholar
  21. Lindahl PA (2002) The Ni-containing carbon monoxide dehydrogenase family: light at the end of the tunnel? Curr Topics Biochem 41:2097–2105CrossRefGoogle Scholar
  22. Marmur J (1961) A procedure for the isolation of desoxyribonucleic acid from microorganisms. J Mol Biol 3:208–218Google Scholar
  23. Marmur J, Doty P (1962) Determination of the base composition of deoxyribonucleic acid from its thermal denaturation temperature. J Mol Biol 5:109–118Google Scholar
  24. Meyer O, Frunzke K, Morsdorf G (1993) Biochemistry of aerobic utilization of carbon monoxide. In: Murrell JC, Kelly DP (eds) Microbial growth on C1 compounds. Intercept, Ltd, Andover, Hampshire, UK, pp 433–459Google Scholar
  25. Miroshnichenko ML, Gongadze GM, Rainey FA, Kostyukova AS, Lysenko AM, Chernyh NA, Bonch-Osmolovskaya EA (1998) Thermococcus gorgonarius sp. nov. and Thermococcus pacificus sp. nov.: heterotrophic extremely thermophilic Archaea from New Zealand submarine hot vents. Int J Syst Bacteriol 48:23–29Google Scholar
  26. Möller-Zinkhan D, Thauer RK (1990) Anaerobic lactate oxidation to 3CO2 by Archaeoglobus fulgidus via the carbon monoxide dehydrogenase pathway: demonstration of the acetyl-CoA carbon-carbon cleavage reaction in cell extracts. Arch Microbiol 153:213–218Google Scholar
  27. Pley U, Schipka J, Gambacorta A, Jannasch HW, Fricke H, Rachel R, Stetter KO (1991) Pyrodictium abysii sp. nov. represents a novel heterotrophic marine archaeal hyperthermophile growing at 110°C. Syst Appl Microbiol 14:245–253Google Scholar
  28. Rainey FA, Ward-Rainey N, Kroppenstedt RM, Stackebrandt E (1996) The genus Nocardiopsis represents a phylogenetically coherent taxon and a distinct actinomycete lineage: proposal of Nocardiopsaceae fam. nov. Int J Syst Bacteriol 46:1088–1092PubMedGoogle Scholar
  29. Sokolova TG, González JM, Kostrikina NA, Chernyh NA, Tourova TP, Kato C, Bonch-Osmolovskaya EA, Robb FT (2001) Carboxydobrachium pacificum gen. nov., sp. nov., a new anaerobic, thermophilic, CO-utilizing marine bacterium from Okinawa Trough. Int J Syst Evol Microbiol 51:141–149PubMedGoogle Scholar
  30. Sokolova TG, Kostrikina NA, Chernyh NA, Tourova TP, Bonch-Osmolovskaya EA (2002) Carboxydocella thermautotrophica gen. nov., sp. nov., a novel anaerobic CO-utilizing thermophile from a Kamchatkan hot spring. Int J Syst Evol Microbiol 52:1961–1967CrossRefPubMedGoogle Scholar
  31. Stetter KO, König H, Stackebrandt E (1983) Pyrodictium, a new genus of submarine disc-shaped sulfur reducing archaebacteria growing optimally at 105°C. Syst Appl Microbiol 4:535–551Google Scholar
  32. Svetlichny VA, Sokolova TG, Gerhardt M, Ringpfeil M, Kostrikina NA, Zavarzin GA (1991) Carboxydothermus hydrogenoformans gen. nov., sp. nov., a CO-utilizing thermophilic anaerobic bacterium from hydrothermal environments of Kunashir Island. Syst Appl Microbiol 14:254–260Google Scholar
  33. Svetlichny VA, Sokolova TG, Kostrikina NA, Lysenko AM (1994) A new thermophilic anaerobic carboxydotrophic bacterium Carboxydothermus restrictus sp. nov. Microbiology (English translation of Mikrobiologiya) 63:294–297Google Scholar
  34. Svetlitchny V, Peschel C, Acker G, Meyer O (2001) Two membrane-associated NiFeS-carbon monoxide dehydrogenases from the anaerobic carbon monoxide-utilizing eubacterium Carboxydothermus hydrogenoformans. J Bacteriol 183:5134–5144CrossRefPubMedGoogle Scholar
  35. Symonds RB, Rose WI, Bluth GJS, Gerlach TM (1994) Volcanic gas studies: methods, results and applications. In: Carroland MR, Holloway JR (eds) Volatiles in magma. Mineral Society of America, Washington, pp 1–66Google Scholar
  36. Takai K, Inoue A, Horikoshi K (2002) Methanothermococcus okinawensis sp. nov., a thermophilic, methane-producing archaeon isolated from a Western Pacific deep-sea hydrothermal vent system. Int J Syst Evol Microbiol 52:1089–1095CrossRefPubMedGoogle Scholar
  37. Uffen RL (1983) Metabolism of carbon monoxide by Rhodopseudomonas gelatinosa: cell growth and properties of the oxidation system. J Bacteriol 155:956–965PubMedGoogle Scholar
  38. Vorholt JA, Hafenbradl D, Stetter KO, Thauer RK (1997) Pathways of autotrophic CO2 fixation and of dissimilatory nitrate reduction to N2O in Ferroglobus placidus. Arch Microbiol 167:19–23CrossRefGoogle Scholar
  39. Whitman WB, Boone DR, KogaY (2001) Order I. Methanococcales. In: Garrity GM (ed) Bergey’s manual of systematic bacteriology, vol 1, 2nd edn. Springer, Berlin Heidelberg New York, p 236Google Scholar
  40. Wolin EA, Wolin MJ, Wolfe RS (1963) Formation of methane by bacterial extracts. J Biol Chem 238:2882–2886Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Tatyana G. Sokolova
    • 1
  • Christian Jeanthon
    • 2
  • Nadezhda A. Kostrikina
    • 1
  • Nikolai A. Chernyh
    • 1
  • Alexander V. Lebedinsky
    • 1
  • Erko Stackebrandt
    • 3
  • Elizaveta A. Bonch-Osmolovskaya
    • 1
  1. 1.Institute of MicrobiologyRussian Academy of SciencesMoscowRussia
  2. 2.UMR 6539 Centre National de la Recherche Scientifique et Université de Bretagne OccidentaleInstitut Universitaire Européen de la MerPlouzanéFrance
  3. 3.DSMZGerman Collection of Microorganisms and Cell CulturesBraunschweigGermany

Personalised recommendations