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

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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.

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References

  • 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 25:3389–3402

    PubMed  Google Scholar 

  • 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 46:265–269

    PubMed  Google Scholar 

  • Balch WE, Fox GE, Magrum LJ, Woese CR, Wolfe RS (1979) Methanogens: reevaluation of a unique biological group. Microbiol Rev 43:260–296

    CAS  PubMed  Google Scholar 

  • Benson DA, Boguski MS, Lipman DJ, Ostell J, Ouellette BFF (1998) GenBank. Nucleic Acids Res 26:1–7

    Article  CAS  PubMed  Google Scholar 

  • Bodrossy L, Kovács KL, McDonald IR, Murrell JC (1999) A novel thermophilic methane-oxidising γ-Proteobacterium. FEMS Microbiol Lett 170:335–341

    CAS  Google Scholar 

  • Brun YV (2001) Global analysis of a bacterial cell cycle: tracking down necessary functions and their regulators. Trend Microbiol 9:405–407

    Article  CAS  Google Scholar 

  • 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 20:301–309

    Google Scholar 

  • Cho J–G, Kim S-G (2000) Increase in bacterial community diversity in subsurface aquifers receiving livestock wastewater input. Appl Environ Microbiol 66:956–965

    Article  CAS  PubMed  Google Scholar 

  • DeLong EF (1992) Archaea in coastal marine environments. Proc Natl Acad Sci USA 89:5685–5689

    CAS  PubMed  Google Scholar 

  • 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 64:119–125

    CAS  PubMed  Google Scholar 

  • 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 63:1498–1504

    CAS  PubMed  Google Scholar 

  • 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 42:568–576

    CAS  PubMed  Google Scholar 

  • Giovannoni SJ, Britschgi TB, Moyer CL, Field FG (1990) Genetic diversity of Sargasso Sea bacterioplankton. Nature 345:60–63

    CAS  PubMed  Google Scholar 

  • 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 3:55–62

    Article  CAS  PubMed  Google Scholar 

  • 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 49:783–786

    PubMed  Google Scholar 

  • Hugenholtz P, Pitulle C, Hershberger KL, Pace NR (1998) Novel division level bacterial diversity in a Yellowstone hot spring. J Bacteriol 180:366–376

    CAS  PubMed  Google Scholar 

  • 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 5:385–392

    CAS  PubMed  Google Scholar 

  • 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 19:535–552

    Article  CAS  Google Scholar 

  • 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 4:277–286

    CAS  PubMed  Google Scholar 

  • 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 36:1–56

    Article  CAS  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions though comparative studies of nucleotide sequence. J Mol Evol 16:111–120

    PubMed  Google Scholar 

  • Krumholz LR, McKinley JP, Ulrich GA, Sufita JM (1997) Confined subsurface microbial communities in Cretaceous rock. Nature 386:64–66

    CAS  Google Scholar 

  • 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 37:197–207

    Article  PubMed  Google Scholar 

  • 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 67:4242–4248

    Article  CAS  PubMed  Google Scholar 

  • Matsushima Y, Aoki M (1994) Temperature and oxygen isotope variations during formation of the Hishikari epithermal gold-silver veins, southern Kyushu, Japan. Ecol Geol 89:1608–1613

    Google Scholar 

  • McKinley JP, Stevens TO, Westall F (2000) Microfossils and paleoenvironments in deep subsurface basalt samples. Geomicrobiol J 17:43–54

    CAS  Google Scholar 

  • 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 46:1042–1055

    Google Scholar 

  • Pace NR (1997) A molecular view of microbial diversity and the biosphere. Science 276:734–740

    CAS  PubMed  Google Scholar 

  • 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 371:410–413

    Google Scholar 

  • Pedersen K (1997) Microbial life in deep granitic rock. FEMS Microbiol Rev 20:399–414

    Article  CAS  Google Scholar 

  • Porter KG, Feig YS (1980) The use of DAPI for identifying and counting microflora. Limnol Oceanogr 25:943–948

    Google Scholar 

  • 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 42:951–957

    CAS  PubMed  Google Scholar 

  • 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 44:846–849

    CAS  Google Scholar 

  • Stevens TO, McKinley JP (1995) Lithoautotrophic microbial ecosystems in deep basalt aquifers. Science 270:450–454

    CAS  Google Scholar 

  • Takai K, Horikoshi K (1999a) Genetic diversity of archaea in deep-sea hydrothermal vent environments. Genetics 152:1285–1297

    CAS  PubMed  Google Scholar 

  • 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 65:5586–5589

    CAS  PubMed  Google Scholar 

  • 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 51:1425–1435

    CAS  PubMed  Google Scholar 

  • Takai K, Moser DP, Deflaun M, Onstott TC, Fredrickson JK (2001b) Archaeal diversity in waters from deep South African gold mines. Appl Environ Microbiol 67:5750–5760

    Article  CAS  PubMed  Google Scholar 

  • Takai K, Komatsu T, Inagaki F, Horikoshi K (2001c) Distribution of Archaea in a black smoker chimney structure. Appl Environ Microbiol 67:3618–3629

    CAS  PubMed  Google Scholar 

  • 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 68:3046–3054

    PubMed  Google Scholar 

  • 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 52:1089–1095

    Article  CAS  PubMed  Google Scholar 

  • 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 25:4876–4882

    CAS  PubMed  Google Scholar 

  • 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 65:4375–4384

    CAS  PubMed  Google Scholar 

  • Warthmann R, Lith van Y, Vasconcelos C, McKenzie JA, Karpoff AM (2000) Bacterially induced dolomite precipitation in anoxic culture experiments. Geology 28:1091–1094

    Article  CAS  Google Scholar 

  • Whitman WB, Coleman DC, Wiebe WJ (1998) Prokaryotes: the unseen majority. Proc Natl Acad Sci USA 95:6578–6583

    CAS  PubMed  Google Scholar 

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Acknowledgments

We are grateful to the management of the Sumitomo Metal Mining Company for its cooperation in and understanding of our research.

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Authors and Affiliations

  1. Subground Animalcule Retrieval (SUGAR) Project, Frontier Research System for Extremophiles, Japan Marine Science and Technology Center (JAMSTEC) , Yokosuka 237-0061, Japan

    Fumio Inagaki, Ken Takai, Hisako Hirayama, Kenneth H. Nealson & Koki Horikoshi

  2. Sumitomo Metal Mining Company, Kagoshima, Japan

    Yu Yamato

  3. Department of Earth Sciences, University of Southern California, Los Angeles, CA, USA

    Kenneth H. Nealson

Authors
  1. Fumio Inagaki
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  2. Ken Takai
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  3. Hisako Hirayama
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  4. Yu Yamato
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  5. Kenneth H. Nealson
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  6. Koki Horikoshi
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Correspondence to Fumio Inagaki.

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Communicated by W.D. Grant

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Inagaki, F., Takai, K., Hirayama, H. et al. Distribution and phylogenetic diversity of the subsurface microbial community in a Japanese epithermal gold mine. Extremophiles 7, 307–317 (2003). https://doi.org/10.1007/s00792-003-0324-9

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