Advertisement

Archives of Microbiology

, Volume 160, Issue 5, pp 338–349 | Cite as

Pyrococcus abyssi sp. nov., a new hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent

  • Gaël Erauso
  • Anna-Louise Reysenbach
  • Anne Godfroy
  • Jean-Roch Meunier
  • Byron Crump
  • Frédéric Partensky
  • John A. Baross
  • Viggo Marteinsson
  • Georges Barbier
  • Norman R. Pace
  • Daniel Prieur
Original Papers

Abstract

A novel, hyperthermophilic, anaerobic, sulfurmetabolizing archaeon was isolated from a fluid sample from recently discovered hydrothermal vents in the North Fiji basin (SW Pacific), at 2000 m depth. The new organism, strain GE5, is a gram-negative, highly motile coccus. It grows between 67° and 102°C under atmospheric pressure, with an optimum at 96°C (doubling time 33 min). The upper growth temperature is extended by at least 3°C when cells are cultivated under in situ hydrostatic pressures (20 MPa). Strain GE5 is an obligate heterotroph, fermenting peptides, or mixtures of amino acids to acetate, isovalerate, isobutyrate, propionate, H2 and CO2. Hydrogen inhibits growth unless sulfur is present. In the presence of sulfur, H2S is then produced. Phylogenetic analyses of the 16 S rRNA sequence of strain GE5 places the new isolate within the Thermococcales. By its high growth temperature and physiological features the new isolate ressembles Pyrococcus sp. However it deffers by a 7% mol upper G+C-content and shows low level of DNA similarity with the two previously described species. Based on these differences the description of strain GE5 as a new species Pyrococcus abyssi (CNCM I-1302) is proposed.

Key words

Archaea Hyperthermophile Hydrostatic pressure Pyrococcus Deep-sea vent 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Achenbach-Richter L, Gupta R, Zillig W, Woese CR (1988) Rooting the archaebacterial tree: the pivotal role of Thermococcus celer in archaebacterial evolution. Syst Appl Microbiol 10: 231–240Google Scholar
  2. Balch W, Wolfe RS (1976) new approach to the cultivation of methanogenic bacteria: 2-mercaptoethaanesulfonic acid (HS-CoM)-dependent growth of Methanobacterium ruminantium in a pressurized atmosphere. Appl Environ Microbiol 32: 781–791Google Scholar
  3. Balch WE, Fox GE, Magrum LS, Woese CR, Wolfe RS (1979) Methanogens: reevaluation of a unique biological group. Microbial Rev 43: 260–296Google Scholar
  4. Bligh EG, Dyer WJ (1959) A rapid method for lipid extraction and purification. Can J Microbiol 35: 911–917Google Scholar
  5. Blumentals II, Itoh M, Olson GJ, Kelly RM (1990) Role of polysulfides in reduction of elemental sulfur by the hyperthermophilic archaebacterium Pyrococcus furiosus. Appl Environ Microbiol, 56: 1255–1262Google Scholar
  6. Burggraf S, Jannasch HW, Nicolaus B, Stetter CO (1990a) Archaeoglobus profundus sp. nov., represents a new species within the sulfate-reducing archaebacteria. Syst Appl Microbiol 13: 24–28Google Scholar
  7. Burggraf S, Fricke H., Neuner AM, Kristjansson J, Rouvier P, Mandelco L, Woese CR. Stetter KO (1990b) Methanococcus igneus sp. nov., a novel hyperthermophilic methanogen from a shallow submarine hydrothermal system. Syst Appl Microbiol 13: 263–269Google Scholar
  8. Charbonnier F, Erauso G, Barbeyron T, Prieur D, Forterre P (1992) Evidence that a plasmid from a hyperthermophilic archaebacterium is relaxed at physiological temperatures. J Bacteriol 174: 6103–6108Google Scholar
  9. Cline JD (1969) Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 14: 454–458Google Scholar
  10. De Rosa M, Gambacorta A, Trincone A, Basso A, Zillig W, Holz I (1987) Lipids of the Thermococcus celer, a sulfur-reducing archaebacterium: structure and biosynthesis. Syst Appl Microbiol 9: 1–5Google Scholar
  11. Delaney JR, Mcduff RE, Lupton JE (1984) Hydrothermal fluid temperatures of 400°C on the endeavour segment, northern Juan de Fuca. Trans Am Geophys Union 65: 973Google Scholar
  12. Deming JW, Baross JA (1986) Solid medium for culturing black smoker bacteria at temperatures to 120°C. Appl Environ Microbiol 51: 238–243Google Scholar
  13. Deming JW, Hada H, Colwell RR, Luehrsen, Fox GE (1984) The ribonucleotide sequence of 5S rRNA from two strains of deep-sea barophilic bacteria. J Gen Microbiol 130: 1911–1920Google Scholar
  14. Deming JW, Somers LK, Straube WL, Swartz DG, Macdonell MT (1988) Isolation of an obligately barophilic bacterium and description of a new genus, Colwellia gen. nov. Syst Appl Microbiol 10: 152–160Google Scholar
  15. Desbruyères D, Alayse AM, Otha S (1993) Deep-sea hydrothermal communities in the Southwestern Pacific back-arc basins (the North-Fiji and Lau Basins): composition, microdistribution and food web. Marine Geol (in press)Google Scholar
  16. Feinberg AP, Vogelstein B (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132: 6–13Google Scholar
  17. Felsenstein J (1985) Confidence limits on phylogenies: an approach using bootstrap. Evolution 39: 783–791Google Scholar
  18. Fiala G, Stetter KO (1986) Pyrococcus furiosus sp. nov. represents a new genus of marine heterotrophic archaebacteria growing optimally at 100°C. Arch Microbiol 145: 56–61Google Scholar
  19. 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
  20. Fox GE, Wisotzkey JD, Jurtshuk P (1992) How close is close: 16S rRNA sequence identity may not be sufficient to guarantee species identity. Int J Syst Bacteriol 42: 166–170Google Scholar
  21. Grimaud D, Ishibashi JI, Lagabriele Y, Auzende JM, Urabe T (1991) Chemistry of hydrothermal fluids from the 17°S active site on the North Fiji basin ridge (SW Pacific). Chem Geol 93: 209–218Google Scholar
  22. Grimont PAD, Popoff MY, Grimont F, Coynault C, Lemelin M (1980) Reproducibility and correlation study of three deoxyribonucleic acid hybridization procedures. Curr Microbiol 4: 325–330Google Scholar
  23. Hedrick DB, Guckert JB, White DC (1991) Archaebacterial ether lipid diversity analyzed by supercritical fluid chromatography: integration with a bacterial lipid protocol. J Lipid Res 32: 659–666Google Scholar
  24. Hilpert R, Winter J, Hammes W, Kandler O (1981) The sensitivity of archaebacteria to antibiotics. Zentralbl Bakt Hyg I Abt Orig C 2: 11–20Google Scholar
  25. Hobbie JE, Dahney RJ, Jasper S (1977) Use of nucleopore filters for counting bacteria by fluorescence microscopy. Appl Environ Microbiol 33: 1225–1228Google Scholar
  26. Huber R, Kurr M, Jannasch HW, Stetter KO (1989) A novel group of abyssal methanogenic archaebacteria (Methanopyrus) growing at 110°C. Nature 342: 833–834Google Scholar
  27. Ingvorsen K, Jorgensen BB (1979) Combined measurement of oxygen and sulfide in water samples. Limnol Oceanogr 24: 390–393Google Scholar
  28. Ivanova TL, Turova TP, Antonov AS (1988) DNA-DNA hybridization studies on some purple non sulfur bacteria. Syst Appl Microbiol 10: 259–263Google Scholar
  29. Jannasch HW, Wirsen CO, Molyneaux SJ, Langworthy TA (1988) Extremely thermophilic fermentative archaebacteria of the genus Desulfurococcus from deep-sea hydrothermal vents. Appl Environ Microbiol 54: 1203–1209Google Scholar
  30. Jannasch HW, Wirsen CO, Molyneaux SJ, Langworthy TA (1992) Comparative physiological studies of hyperthermophilic archae isolated from deep-sea hot vents with emphasis on Pyrococcus strain GB-D. Appl Environ Microbiol 58: 3472–3481Google Scholar
  31. Johnson JL (1985a) DNA reassociation and RNA hybridisation of bacterial nuclei acids. Methods Microbiol 18: 33–74Google Scholar
  32. Johnson JL (1985b) Nucleic acid in bacterial classification. In: Krieg NR, Holt IG (eds) Bergey's manual of systematic bacteriology, vol I. Williams & Wilkins, BaltimoreGoogle Scholar
  33. Jollivet D, Hashimoto J, Auzende JM (1989) Premières observations de communautés animales associées à l'hydrothermalisme arrière arc du bassin Nord-Fidjien. CR Acad Sci Paris 309: 301–308Google Scholar
  34. Jones WJ, Leigh JA, Mayer F, Woese CR, Wolfe RS (1983) Methanococcus jannaschii sp. nov., an extremely thermophilic methanogen from a submarine hydrothermal vent. Arch Microbiol 136: 254–261Google Scholar
  35. Kurr M, Huber R, Konig 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
  36. Lanzotti V, Trincone A, Nicolaus B, Zillig W, De Rosa M, Gambacorta A (1989) Complex lipids of Pyrococcus and AN1, thermophilic members of the archaebacteria belonging to the Thermococcales. Biochim Biophys Acta 1004: 44–48Google Scholar
  37. 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
  38. Mesbah M, Premachandran U, Whitman WB (1989) Precise measurement of the G+C content of dideoxyribonucleic acid by high performance liquid chromatography. Int J Syst Bacteriol 39: 159–167Google Scholar
  39. Miller JF, Shah NN, Nelson CN, Ludlow JM, Clark DS (1988) Pressure and temperature effects on growth and methane production of the extreme thermophile Methanococcus jannaschii. Appl Environ Microbiol 54: 3029–3042Google Scholar
  40. Nelson CM, Shuppenhauer MR, Clark DS (1991) Effect of hyperbaric pressure on a deep-sea archaebacterium in stainless steel and glass-lined vessels. Appl Environ Microbiol 57: 3576–3580Google Scholar
  41. Nelson CM, Shuppenhauer MR, Clark DS (1992) High pressure, high temperature bioreactor for comparing effects of hyperbaric and hydrostatic pressure on bacterial growth. Appl Environ Microbiol 58: 1789–1793Google Scholar
  42. Olsen GJ (1987) The earliest phylogenetic branchings: comparing rRNA-based evolutionary trees inferred with various techniques. Cold Spring Harbor Symp Quant Biol 52: 825–838Google Scholar
  43. Olsen GJ, Overback R, Larsen N, Marsh TL, Mc Canghey MJ, Macinkenas MA, Kuan WM, Macke TJ, Xing Y, Woese CR (1992) The ribosomal database project. Nucleic Acids Res 20: 2199–2200Google Scholar
  44. Pledger RJ, Baross JA (1991) Preliminary description and nutritional characterization of a chemoorganotrophic archaebacterium growing of up to 110°C isolated from a submarine hydrothermal vent environment. J Gen Microbiol 137: 203–211Google Scholar
  45. Pley U, Schipka J, Gambacorta A, Jannasch HW, Fricke H, Rachel R, Stetter KO (1991) Pyrodictium abyssi sp. nov. represents a novel heterotrophic marine archaeal hyperthermophile growing at 110°C. Syst Appl Microbiol 14: 245–253Google Scholar
  46. Reysenbach AL, Deming JW (1991) Effects of hydrostatic pressure on growth of hyperthermophilic archaebacteria from the Juan de Fuca Ridge. Appl Environ Microbiol 57: 1271–1274Google Scholar
  47. Reysenbach AL, Giver LJ, Wickham GS, Pace NR (1992) Differential amplification f rRNA genes by polymerase chain reaction. Appl Environ Microbiol 58: 3417–3418Google Scholar
  48. Saiki RK, Gelfand DH, Stoffel SJ, Scharf S, Higuchi R, Horn GT, Mullis HB, Erlich HA (1988) Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 230: 1350–1354Google Scholar
  49. Sambrook J, Fritch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Habor, NYGoogle Scholar
  50. Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5483Google Scholar
  51. Schleifer KH, Stuckebrandt E (1983) Molecular systematics of prokaryotes. Ann Rev Microbiol 37: 143–187Google Scholar
  52. Spiess FN, Macdonald KV, Atwater T, Ballard R, Carranza A, Cordoba D, Cox C, Diaz Garcia VM, Francheteau J, Guerrero J, Hawkins J, Haymon R, Hessler R, Juteau T, Kastner M, Larson R, Luyendyk B, Macdougall JD, Miller S, Normark W, Orcutt J, Rangin C (1980) Wast Pacific Rise: hot springs and geophysical experiments. Science 207: 1421–1433Google Scholar
  53. Stetter KO (1988) Archaeoglobus fervidus gen. nov., sp. nov.: a new taxon of extremely thermophilic archaebacteria. Syst Appl Microbiol 10: 172–173Google Scholar
  54. Stetter KO, Konig H, Stackebrandt E (1983) Pyrodictium gen. nov., a new genus of submarine disc-shaped sulphur reducing archaebacteria growing optimaly at 105°C. Syst Appl Microbiol 4: 535–551Google Scholar
  55. Trincone A, Nicolaus B, Palmieri G, De Rosa M, Huber R, Stetter KO, Gambacorta A (1992) Distribution of complex and core lipids within new hyperthermophilic members of the Archaea Domain. Syst Appl Microbiol 15: 11–17Google Scholar
  56. Vaulot D, Courties C, Partensky F (1989) A simple method to preserve oceanic phytoplankton for flow cytometric analyses. Cytometry 10: 629–635Google Scholar
  57. Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O, Krichevsky MI, Moore LH, Moore WEC, Murray HE, Stakkebrandt E, Starr MP, Truper HG (1987) Report of the ad hoc committee on reconciliation of the approaches to bacterial systematics. Int Syst Bacteriol 37: 463–464Google Scholar
  58. Wermann SD, Springer MS, Britten RJ (1990) Nucleic acids I: DNA-DNA hybridization. In: Hillis DM, Moritz C (eds) Molecular systematic. Sinauer Associates, Massachusetts, USA, pp 204–245Google Scholar
  59. White DC, Bobbie RJ, King JD, Nickels JS, Amoe P (1979) Lipid analysis of sediments for microbial biomass and community structure. In: Litch CD, Seyfried PL (eds) Methodology for biomass determinations and microbial activities in sediments. ASTM, Washington, pp 87–103Google Scholar
  60. Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA 87: 4576–4579Google Scholar
  61. Yayanos AA (1986) Evolution and ecological implications of the properties of deep-sea barophilic bacteria. Proc Natl Acad Sci USA 83: 9542–9546Google Scholar
  62. Yayanos AA, Dietz AZ, Boxtel R van (1982) Dependence of reproduction rate on pressure as a hallmark of deep-sea bacteria. Appl Environ Microbiol 44: 1356–1361Google Scholar
  63. Zehnder AJB, Wuhrmann K (1976) Titanium(III)-citrate as a nontoxic oxidation-reduction buffering system for the culture of obligate anaerobes. Science 194: 1165–1166Google Scholar
  64. Zhao H, Wood AG, Widdel F, Bryant MP (1988) An extremely thermophilic Methanococcus from a deep sea hydrothermal vent and its plasmid. Arch Microbiol 150: 178–183Google Scholar
  65. Zillig W, Stetter KO, Prangishwilli D, Schafer W, Wunderl S, Janekovic D, Holz I, Palm P (1982) Desulfurococcae, the second family of extremely thermophilic, anaerobic sulfur-respiring Thermoproteales. Zentralbl Bakt Hyg I Abt Orig 3: 304–311Google Scholar
  66. Zillig W, Gierl A, Schreiber S, Wunderl S, Janekovic D, Stetter KO, Klenk HP (1983) The archaebacterium Thermophilum pendens represents a novel genus of the thermophilic, anaerobic sulfur respiring Thermoproteales. Syst Appl Microbiol 4: 79–87Google Scholar
  67. Zillig W, Holz I, Klenk HP, Trent J, Wunderl S, Janekovic D, Imsel E, Haas B (1987) Pyrococcus woesei, sp. nov., an ultrathermophilic marine archaebacterium, representing a novel order, Thermococcales. Syst Appl Microbiol 9: 62–70Google Scholar
  68. Zillig W, Holz I, Janekovic D, Klenk HP, Imsel E, Trent J, Wunderl S, Forjaz VH, Coutinho R, Ferreira T (1990) Hyperthermus butylicus, a hyperthermophilic sulfur reducing archaebacterium that ferments peptides. J Bacteriol 172: 3959–3965Google Scholar

Copyright information

© Springer Verlag 1993

Authors and Affiliations

  • Gaël Erauso
    • 1
  • Anna-Louise Reysenbach
    • 2
  • Anne Godfroy
    • 3
  • Jean-Roch Meunier
    • 4
  • Byron Crump
    • 5
  • Frédéric Partensky
    • 1
  • John A. Baross
    • 5
  • Viggo Marteinsson
    • 1
  • Georges Barbier
    • 3
  • Norman R. Pace
    • 2
  • Daniel Prieur
  1. 1.Station BiologiqueCNRS UPR 4601RoscoffFrance
  2. 2.Department of BiologyIndiana UniversityBloomingtonUSA
  3. 3.IFREMER Centre de Brest: Environment ProfondPlouzanéFrance
  4. 4.Unité des entérobactériesInstitut PasteurParis CédexFrance
  5. 5.School of OceanographyUniversity of WashingtonSeattleUSA

Personalised recommendations