Extremophiles

, Volume 7, Issue 4, pp 307–317 | Cite as

Distribution and phylogenetic diversity of the subsurface microbial community in a Japanese epithermal gold mine

  • Fumio Inagaki
  • Ken Takai
  • Hisako Hirayama
  • Yu Yamato
  • Kenneth H. Nealson
  • Koki Horikoshi
Original Paper

Abstract

Distribution and phylogenetic diversity of microbial communities in hot, deep underground environments in the Hishikari epithermal gold mine, southern part of Kyushu, Japan, were evaluated using molecular phylogenetic analyses. Samples included drilled cores such as andesitic volcanic rock (0.95–1.78 Ma) and the oceanic sedimentary basement rock of Shimanto-Supergroup (100 Ma), as well as geothermal hot aquifer waters directly collected from two different sites: AW-site (71.5°C, pH 6.19) and XW-site (85.0°C, pH 6.80) at a depth of 350 mbls (meters below land surface). Based on PCR-amplified 16S rRNA gene clone analysis, the microbial communities in the drilled cores and the hot aquifer water from the XW-site consisted largely of the 16S rRNA gene sequences, closely related to the sequences often found in marine environments, while the aquifer water from the AW-site contained 16S rRNA gene sequences representing members of Aquificales, thermophilic methanotrophs within the γ-subdivision of the Proteobacteria and uncultivated strains within the β-subdivision of Proteobacteria. The cultivable microbial community detected by enrichment cultivation analysis largely matched that detected by the culture-independent molecular analysis.

Keywords

Gold mine Microbial diversity 16S rRNA gene Subsurface biosphere 

References

  1. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedGoogle Scholar
  2. Anderews KT, Partel BK (1996) Fervidobacterium gondwanense sp. nov., a new thermophilic anaerobic bacterium isolated from nonvolcanically heated geothermal waters of the Great Artesian Basin of Australia. Int J Syst Bacteriol 46:265–269PubMedGoogle Scholar
  3. Balch WE, Fox GE, Magrum LJ, Woese CR, Wolfe RS (1979) Methanogens: reevaluation of a unique biological group. Microbiol Rev 43:260–296PubMedGoogle Scholar
  4. Benson DA, Boguski MS, Lipman DJ, Ostell J, Ouellette BFF (1998) GenBank. Nucleic Acids Res 26:1–7CrossRefPubMedGoogle Scholar
  5. Bodrossy L, Kovács KL, McDonald IR, Murrell JC (1999) A novel thermophilic methane-oxidising γ-Proteobacterium. FEMS Microbiol Lett 170:335–341Google Scholar
  6. Brun YV (2001) Global analysis of a bacterial cell cycle: tracking down necessary functions and their regulators. Trend Microbiol 9:405–407CrossRefGoogle Scholar
  7. Buchholz-Cleven BEE, Rattunde B, Straub KL (1997) Screening for genetic diversity of isolates of anaerobic Fe(II)-oxidizing bacteria using DGGE and whole-cell hybridization. Syst Appl Microbiol 20:301–309Google Scholar
  8. Cho J–G, Kim S-G (2000) Increase in bacterial community diversity in subsurface aquifers receiving livestock wastewater input. Appl Environ Microbiol 66:956–965CrossRefPubMedGoogle Scholar
  9. DeLong EF (1992) Archaea in coastal marine environments. Proc Natl Acad Sci USA 89:5685–5689PubMedGoogle Scholar
  10. Finster K, Liesack W, Thamdrup B (1998) Elemental sulfur and thiosulfate disproportionation by Desulfocapsa sulfoexigens sp. nov., a new anaerobic bacterium isolated from marine surface sediment. Appl Environ Microbiol 64:119–125PubMedGoogle Scholar
  11. Fry NK, Fredrickson JK, Fishbain S, Wagner M, Stahl D (1997) Population structure of microbial communities associated with two deep, anaerobic, alkaline aquifers. Appl Environ Microbiol 63:1498–1504PubMedGoogle Scholar
  12. Gauthier MJ, Lafay B, Christen R, Fernandez L, Acquaviva M, Bonin P, Bertrand JC (1992) Marinobacter hydrocarbonoclasticus gen. nov., sp. nov., a new, extremely halotolerant hydrocarbon-degrading marine bacterium. Int J Syst Bacteriol 42:568–576PubMedGoogle Scholar
  13. Giovannoni SJ, Britschgi TB, Moyer CL, Field FG (1990) Genetic diversity of Sargasso Sea bacterioplankton. Nature 345:60–63PubMedGoogle Scholar
  14. Grote R, Li L, Tamaoka J, Kato C, Horikoshi K, Antranikian G (1999) Thermococcus siculi sp. nov., a novel hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent at the Mid-Okinawa Trough. Extremophiles 3:55–62CrossRefPubMedGoogle Scholar
  15. Hayashi NR, Ishida T, Yokoya A, Kodama T, Igarashi Y (1999) Hydrogenophilus thermoluteolus gen. nov., sp. nov., a thermophilic, facultatively chemolithoautotrophic, hydrogen-oxidizing bacterium. Int J Syst Bacteriol 49:783–786PubMedGoogle Scholar
  16. Hugenholtz P, Pitulle C, Hershberger KL, Pace NR (1998) Novel division level bacterial diversity in a Yellowstone hot spring. J Bacteriol 180:366–376PubMedGoogle Scholar
  17. Inagaki F, Takai K, Komatsu T, Kanamatsu T, Fujioka K, Horikoshi K (2001) Archaeology of Archaea: geomicrobiological record of Pleistocene thermal events concealed in a deep-sea subseafloor environment. Extremophiles 5:385–392PubMedGoogle Scholar
  18. Inagaki F, Sakihama Y, Takai K, Komatsu T, Inoue A, Horikoshi K (2002a) Transition in microbial community structures and presence of unusual microorganisms in a deep-sea rock. Geomicrobiol J 19:535–552CrossRefGoogle Scholar
  19. Inagaki F, Sakihama Y, Inoue A, Kato C, Horikoshi K (2002b) Molecular phylogenetic analyses of reverse-transcribed bacterial rRNA obtained from deep-sea cold seep sediments. Environ Microbiol 4:277–286PubMedGoogle Scholar
  20. Izawa E, Urashima Y, Ibaraki K, Suzuki R, Yokoyama T, Kawasaki K, Koga A, Taguchi S (1990) The Hishikari gold deposit: high-grade epithermal veins in Quaternary volcanics of southern Kyushu, Japan. J Geochem Explor 36:1–56CrossRefGoogle Scholar
  21. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions though comparative studies of nucleotide sequence. J Mol Evol 16:111–120PubMedGoogle Scholar
  22. Krumholz LR, McKinley JP, Ulrich GA, Sufita JM (1997) Confined subsurface microbial communities in Cretaceous rock. Nature 386:64–66Google Scholar
  23. Ludvigen L, Albrechtsen H-J, Ringelberg DB, Ekelund F, Christensen TH (1999) Distribution and composition of microbial populations in a landfill leachate contaminated aquifer (Grindsted, Denmark). Microb Ecol 37:197–207CrossRefPubMedGoogle Scholar
  24. Marteinsson VT, Hauksdóttir S, Hobel CFV, Kristmannsdóttir H, Hreggvidsson GO, Kristjánsson JK (2001) Phylogenetic diversity analysis of subterranean hot spring in Iceland. Appl Environ Microbiol 67:4242–4248CrossRefPubMedGoogle Scholar
  25. Matsushima Y, Aoki M (1994) Temperature and oxygen isotope variations during formation of the Hishikari epithermal gold-silver veins, southern Kyushu, Japan. Ecol Geol 89:1608–1613Google Scholar
  26. McKinley JP, Stevens TO, Westall F (2000) Microfossils and paleoenvironments in deep subsurface basalt samples. Geomicrobiol J 17:43–54Google Scholar
  27. Nohynek LJ, Nurmiaho-Lassila EL, Suhonen EL, Busse HJ, Mohammadi M, Hantula J, Rainey F, Salkinoja-Salonen MS (1996) Description of chlorophenol-degrading Pseudomonas sp. strains KF1T, KF3, and NKF1 as a new species of the genus Sphingomonas, Sphingomonas subarctica sp. nov. Int J Syst Bacteriol 46:1042–1055Google Scholar
  28. Pace NR (1997) A molecular view of microbial diversity and the biosphere. Science 276:734–740PubMedGoogle Scholar
  29. Parkes RJ, Cragg BA, Bale SJ, Getliff JM, Goodman K, Rochelle PA, Fry JC, Weightman AJ, Harvey SM (1994) Deep bacterial biosphere in Pacific Ocean sediments. Nature 371:410–413Google Scholar
  30. Pedersen K (1997) Microbial life in deep granitic rock. FEMS Microbiol Rev 20:399–414CrossRefGoogle Scholar
  31. Porter KG, Feig YS (1980) The use of DAPI for identifying and counting microflora. Limnol Oceanogr 25:943–948Google Scholar
  32. Puhakka JA, Herwig RP, Koro PM, Wolfe GV, Ferguson JF (1995) Biodegradation of chlorophenols by mixed and pure cultures from a fluidized-bed reactor. Appl Microbiol Biotechnol 42:951–957PubMedGoogle Scholar
  33. Stackebrandt E, Goebel BM (1994) Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44:846–849Google Scholar
  34. Stevens TO, McKinley JP (1995) Lithoautotrophic microbial ecosystems in deep basalt aquifers. Science 270:450–454Google Scholar
  35. Takai K, Horikoshi K (1999a) Genetic diversity of archaea in deep-sea hydrothermal vent environments. Genetics 152:1285–1297PubMedGoogle Scholar
  36. Takai K, Horikoshi K (1999b) Molecular phylogenetic analysis of archaeal intron-containing genes coding for rRNA obtained from a deep-subsurface geothermal water pool. Appl Environ Microbiol 65:5586–5589PubMedGoogle Scholar
  37. Takai K, Komatsu T, Horikoshi K (2001a) Hydrogenobacter subterraneus sp. nov., an extremely thermophilic, heterotrophic bacterium unable to grow on hydrogen gas, from deep subsurface geothermal water. Int J Syst Evol Microbiol 51:1425–1435PubMedGoogle Scholar
  38. Takai K, Moser DP, Deflaun M, Onstott TC, Fredrickson JK (2001b) Archaeal diversity in waters from deep South African gold mines. Appl Environ Microbiol 67:5750–5760CrossRefPubMedGoogle Scholar
  39. Takai K, Komatsu T, Inagaki F, Horikoshi K (2001c) Distribution of Archaea in a black smoker chimney structure. Appl Environ Microbiol 67:3618–3629PubMedGoogle Scholar
  40. Takai K, Hirayama H, Sakihama Y, Inagaki F, Yamato Y, Horikoshi K (2002a) Isolation and metabolic characteristics of previously uncultured members of the order Aquificales in a subsurface gold mine. Appl Environ Microbiol 68:3046–3054PubMedGoogle Scholar
  41. Takai K, Inoue A, Horikoshi K (2002b) 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
  42. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882PubMedGoogle Scholar
  43. Vetriani C, Jannasch HW, MacGregor BJ, Stahl DA, Reysenbach A-L (1999) Population structure and phylogenetic characterization of marine benthic archaea in deep-sea sediments. Appl Environ Microbiol 65:4375–4384PubMedGoogle Scholar
  44. Warthmann R, Lith van Y, Vasconcelos C, McKenzie JA, Karpoff AM (2000) Bacterially induced dolomite precipitation in anoxic culture experiments. Geology 28:1091–1094CrossRefGoogle Scholar
  45. Whitman WB, Coleman DC, Wiebe WJ (1998) Prokaryotes: the unseen majority. Proc Natl Acad Sci USA 95:6578–6583PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • Fumio Inagaki
    • 1
  • Ken Takai
    • 1
  • Hisako Hirayama
    • 1
  • Yu Yamato
    • 2
  • Kenneth H. Nealson
    • 1
    • 3
  • Koki Horikoshi
    • 1
  1. 1.Subground Animalcule Retrieval (SUGAR) Project, Frontier Research System for ExtremophilesJapan Marine Science and Technology Center (JAMSTEC) Yokosuka 237-0061Japan
  2. 2.Sumitomo Metal Mining CompanyKagoshimaJapan
  3. 3.Department of Earth SciencesUniversity of Southern CaliforniaLos AngelesUSA

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