Microbiology

, Volume 86, Issue 6, pp 765–772 | Cite as

Variability of the composition of the microbial community of the deep subsurface thermal aquifer in Western Siberia

  • V. V. Kadnikov
  • Yu. A. Frank
  • A. V. Mardanov
  • A. V. Beletsky
  • D. A. Ivasenko
  • N. V. Pimenov
  • O. V. Karnachuk
  • N. V. Ravin
Experimental Articles

Abstract

The deep subsurface biosphere is one of the least studied ecosystems on Earth, containing communities of extremophilic microorganisms. The present work was aimed at molecular genetic characterization of microbial communities of underground thermal waters in Western Siberia, lying at depths of 2–3 km. Water samples were collected from the 5P oil-exploration well, drilled to a depth of 2.8 km near the village Chazhemto (Tomsk region). The water had a temperature of about 20°C, a neutral pH and a low redox potential (–304 mV). Underground aquifers have a complex structure and may contain both planktonic microorganisms and those immobilized on the surface of rocks in the form of biofilms, which may be washed out and detected in the water flowing out of the well. Community composition was analyzed by amplification and pyrosequencing of the 16S rRNA gene fragments in seven water samples taken at different times during 26 hours. Bacteria, which constituted about half of the community, were represented mainly by uncultured lineages of the phyla Firmicutes, Ignavibacteria, Chloroflexi, Bacteroidetes, and Proteobacteria. Archaea belonged mainly to known methanogens of the genera Methanothermobacter, Methanosaeta, and Methanomassiliicoccus. Analysis of the samples taken at different times revealed large variations in the content of most groups of bacteria, with a decrease in Firmicutes abundance accompanied by an increase in the shares of Ignavibacteria and Chloroflexi. The share of archaea of the genus Methanothermobacter varied slightly during the day, while significant variations were observed for the phylotypes assigned to Methanosaeta and Methanomassiliicoccus. Hydrogenotrophic archaea of the genus Methanothermobacter are probably a permanent component of the microbial community occurring in the planktonic state, while most of the identified groups of bacteria are present in biofilms or spatially localized parts of the underground water reservoir, the material of which accidentally enters the well.

Keywords

subsurface biosphere thermal waters microbial community molecular analysis methanogens 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Banks, D., An Introduction to Thermogeology: Ground Source Heating and Cooling, 2nd ed., Chichester: Wiley, 2012.CrossRefGoogle Scholar
  2. Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Peña, A.G., Goodrich, J.K., Gordon, J.I., Huttley, G.A., Kelley, S.T., Knights, D., Koenig, J.E., Ley, R.E., et al., QIIME allows analysis of high-throughput community sequencing data, Nat. Methods, 2010, vol. 7, no. 5, pp. 335–336.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Chen, S., Liu, X., and Dong, X., Syntrophobacter sulfatireducens sp. nov., a novel syntrophic, propionate-oxidizing bacterium isolated from UASB reactors, Int. J. Syst. Evol. Microbiol., 2005, vol. 55, no. 3, pp. 1319–1324.CrossRefPubMedGoogle Scholar
  4. Chivian, D., Alm, E., Brodie, E., Culley, D., Dehal, P., DeSantis, T., Gihring, T., Lapidus, A., Lin, L.-H., Lowry, S., Moser, D., Richardson, P., Southam, G., Wanger, G., Pratt, L., et al., Environmental genomics reveals a single species ecosystem deep within the Earth, Science, 2008, vol. 322, pp. 275–278.CrossRefPubMedGoogle Scholar
  5. Cole, J.R., Wang, Q., Cardenas, E., Fish, J., Chai, B., Farris, R.J., Kulam-Syed-Mohideen, A.S., McGarrell, D.M., Marsh, T., Garrity, G.M., and Tiedje, J.M., The Ribosomal Database Project: improved alignments and new tools for rRNA analysis, Nucleic Acids Res., 2009, vol. 37, pp. 141–145.CrossRefGoogle Scholar
  6. Dridi, B., Fardeau, M.L., Ollivier, B., Raoult, D., and Drancourt, M., Methanomassiliicoccus luminyensis gen. nov., sp. nov., a methanogenic archaeon isolated from human faeces, Int. J. Syst. Evol. Microbiol., 2012, vol. 62, no. 8, pp. 1902–1907.CrossRefPubMedGoogle Scholar
  7. Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C., and Knight, R., UCHIME improves sensitivity and speed of chimera detection, Bioinformatics, 2011, vol. 27, no. 16, pp. 2194–2200.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Edwards, K.J., Becker, K., and Colwell, F., The deep, dark energy biosphere: intraterrestrial life on earth, Annu. Rev. Earth Planet Sci., 2012, vol. 40, pp. 551–568.CrossRefGoogle Scholar
  9. Frank, Y.A., Kadnikov, V.V., Gavrilov, S.N., Banks, D., Gerasimchuk, A.L., Podosokorskaya, O.A., Merkel, A.Yu., Chernyh, N.A., Mardanov, A.V., Ravin, N.V., Karnachuk, O.V., and Bonch-Osmolovskaya, E.A., Stable and variable parts of microbial community in Siberian deep subsurface thermal aquifer system revealed in a long-term monitoring study, Front. Microbiol., 2016, vol. 7: 2101.Google Scholar
  10. Garrity, G.M., Brenner, D.J., Krieg, N.R., and Staley, J.T., The Proteobacteria: The Alpha-, Beta-, Delta-, and Epsilonproteobacteria, in Bergey’s Manual of Systematic Bacteriology, 2nd ed. New York: Springer, 2005, vol. 2, Part C.Google Scholar
  11. Gihring, T.M., Moser, D.P., Lin, L-H., Davidson, M., Onstott, T.C., Morgan, L., Millesson, M., Kieft, T.L., Trimarco, E., Balkwill, D.L., and Dollhopf, M.E., The distribution of microbial taxa in the subsurface water of the Kalahari Shield, South Africa, Geomicrobiol. J., 2006, vol. 23, pp. 415–430.CrossRefGoogle Scholar
  12. Hallbeck, L. and Pedersen, K. Characterization of microbial processes in deep aquifers of the Fennoscandian Shield, Appl. Geochem., 2008, vol. 23, pp. 1796–1819.CrossRefGoogle Scholar
  13. Jørgensen, B.B., Shrinking majority of the deep biosphere, Proc. Natl. Acad. Sci. U. S. A., 2012, vol. 109, pp. 15976–15977.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Kadnikov, V.V., Frank, Y.A., Mardanov, A.V., Beletsky, A.V., Ivasenko, D.A., Pimenov, N.V., Karnachuk, O.V., and Ravin, N.V., Uncultured bacteria and methanogenic archaea predominate in the microbial community of Western Siberian deep subsurface aquifer, Microbiology (Moscow), 2017, vol. 68, no. 3, pp. 412–415.CrossRefGoogle Scholar
  15. Kadnikov, V.V., Mardanov, A.V., Podosokorskaya, O.A., Gavrilov, S.N., Kublanov, I.V., Beletsky, A.V., Bonch-Osmolovskaya, E.A., and Ravin, N.V., Genomic analysis of Melioribacter roseus, facultatively anaerobic organotrophic bacterium representing a novel deep lineage within Bacteriodetes/Chlorobi group, PLoS One, 2013, vol. 8, no. 1, e53047.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Lever, M.A., Rogers, K.L., Lloyd, K. G., Overmann, J., Schink, B., Thauer, R.K., Hoehler, T.M., and Jørgensen, B.B., Life under extreme energy limitation: a synthesis of laboratory- and field-based investigations, FEMS Microbiol. Rev., 2015, vol. 39, pp. 688–728.CrossRefPubMedGoogle Scholar
  17. Liu, Z., Frigaard, N.U., Vogl, K., Iino, T., Ohkuma, M., Overmann, J., and Bryant, D.A., Complete genome of Ignavibacterium album, a metabolically versatile, flagellated, facultative anaerobe from the phylum Chlorobi, Front. Microbiol., 2012, vol. 29. 3:185.Google Scholar
  18. McMahon, S. and Parnell, J., Weighing the deep continental biosphere, FEMS Microbiol. Ecol., 2014, vol. 87, pp. 113–120.CrossRefPubMedGoogle Scholar
  19. Moser, D.P., Gihring, T., Fredrickson, J.K., Brockman, F.J., Balkwill, D., Dollhopf, M.E., Sherwood-Lollar, B., Pratt, L.M., Boice, E., Southam, G., Wanger, G., Welty, A.T., Baker, B.J., and Onstott, T.C., Desulfotomaculum spp. and Methanobacterium spp. dominate a 4- to 5-kilometer deep fault, Appl. Environ. Microbiol., 2005, vol. 71, pp. 8773–8783.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Nealson, K.H., Inagaki, F., and Takai, K., Hydrogendriven subsurface lithoautotrophic microbial ecosystems (SLiMEs): do they exist and why should we care?, Trends Microbiol., 2005, vol. 13, pp. 405–410.CrossRefPubMedGoogle Scholar
  21. Paul, K., Nonoh, J.O., Mikulski, L., and Brune, A., “Methanoplasmatales,” Thermoplasmatales-related archaea in termite guts and other environments, are the seventh order of methanogens, Appl. Environ. Microbiol., 2012, vol. 78, no. 23, pp. 8245–8253.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Podosokorskaya, O.A., Kadnikov, V.V., Gavrilov, S.N., Mardanov, A.V., Merkel, A.Y., Karnachuk, O.V., Ravin, N.V., Bonch-Osmolovskaya, E.A., and Kublanov, I.V., Characterization of Melioribacter roseus gen. nov., sp. nov., a novel facultatively anaerobic thermophilic cellulolytic bacterium from the class Ignavibacteria, and a proposal of a novel bacterial phylum Ignavibacteriae, Environ. Microbiol., 2013, vol. 15, no. 6, pp. 1759–1771.CrossRefPubMedGoogle Scholar
  23. Sahl, J.W., Schmidt, R., Swanner, E.D., Mandernack, K.W., Templeton, A.S., Kieft, T.L., Smith, R.L., Sanford, W.E., Callaghan, R.L., Mitton, J.B., and Spear, J.R., Subsurface microbial diversity in deep granitic-fracture water in Colorado, Appl. Environ. Microbiol., 2008, vol. 74, pp. 143–152.CrossRefPubMedGoogle Scholar
  24. Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B., Lesniewski, R.A., Oakley, B.B., Parks, D.H., Robinson, C.J., Sahl, J.W., Stres, B., Thallinger, G.G., Van Horn, D.J., and Weber, C.F., Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities, Appl. Environ. Microbiol., 2009, vol. 75, no. 23, pp. 7537–7541.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Takai, K., Moser, D.P., DeFlaun, M.F., Onstott, T.C., and Fredrickson, J.K., Archaeal diversity in waters from deep South African gold mines, Appl. Environ. Microbiol., 2001, vol. 67, pp. 5750–5760.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Wanger, G., Southam, G., and Onstott, T.C., Structural and chemical characterization of a natural fracture surface from 2.8 kilometers below land surface: biofilms in the deep subsurface, Geomicrobiol. J., 2006, vol. 23, pp. 443–452.CrossRefGoogle Scholar
  27. Wilson, K., Preparation of genomic DNA from bacteria, in Current Protocols in Molecular Biology, 1987, pp. 2.4.1–2.4.5.Google Scholar
  28. Yamada, T., Sekiguchi, Y., Hanada, S., Imachi, H., Ohashi, A., Harada, H., and Kamagata, Y., Anaerolinea thermolimosa sp. nov., Levilinea saccharolytica gen. nov., sp. nov. and Leptolinea tardivitalis gen. nov., sp. nov., novel filamentous anaerobes, and description of the new classes Anaerolineae classis nov. and Caldilineae classis nov. in the bacterial phylum Chloroflexi, Int. J. Syst. Evol. Microbiol., 2006, vol. 56, no. 6, pp. 1331–1340.CrossRefPubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2017

Authors and Affiliations

  • V. V. Kadnikov
    • 1
    • 2
  • Yu. A. Frank
    • 3
  • A. V. Mardanov
    • 2
  • A. V. Beletsky
    • 2
  • D. A. Ivasenko
    • 3
  • N. V. Pimenov
    • 4
  • O. V. Karnachuk
    • 3
  • N. V. Ravin
    • 1
    • 2
  1. 1.Faculty of BiologyMoscow State UniversityMoscowRussia
  2. 2.Institute of Bioengineering, Research Center of BiotechnologyRussian Academy of SciencesMoscowRussia
  3. 3.Tomsk State UniversityTomskRussia
  4. 4.Winogradsky Institute of Microbiology, Research Center of BiotechnologyRussian Academy of SciencesMoscowRussia

Personalised recommendations