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Occurrence, diversity, and abundance of methanogenic archaea in terrestrial hot springs of Kamchatka and Saõ Miguel Island

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Abstract

Detection and analysis of the mcrA gene encoding methyl-coenzyme M reductase, the key enzyme of methanogenesis, was used to assess occurrence and diversity of methanogenic archaea in terrestrial hot springs of Kamchatka and Sa~o Miguel Island (the Azores). For this analysis, phylogeny of methanogens was initially reconstructed based on available sequences of the mcrA gene, which is a common functional and phylogenetic marker for this physiological group of prokaryotes. Methanogens were revealed in most of the studied terrestrial hot springs with temperatures from 51 to 89°C, although they constituted an insignificant portion of the microbial population. The mcrA gene sequences revealed in the samples belonged to members of the genera Methanothermobacter, Methanothermus, and Methanothrix, previously detected in hot springs, as well as to methanogens not found earlier in these environments. The latter belonged to Methanomassiliicoccales, Methanocellales, and Methanomethylovorans, as well as to MCR-2a, the new deep phylogenetic cluster of uncultured methanogenic archaea; its phylotypes were present in all springs where the mcrA gene was detected. Our results indicate high diversity of the thermophilic methanogens inhabiting terrestrial hot springs and the presence among them of new groups with yet unknown substrate specificity.

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References

  1. Hedderich, R. and Whitman, W., Physiology and biochemistry of the methane-producing Archaea, in The Prokaryotes, 3rd ed., 2006, vol. 2, pp. 1050–1079.

    Article  Google Scholar 

  2. Lelieveld, J., Crutzen, P.J., and Dentener, F.J., Changing concentrations, lifetime and climate forcing of atmospheric methane, Tellus, 1998, vol. 50B, pp. 128–150.

    Article  CAS  Google Scholar 

  3. Wang, J.S., Logan, J.A., McElroy, M.B., Duncan, B.N., Megretskaia, I.A., and Yantosca, R.M., A 3-D model analysis of the slowdown and interannual variability in the methane growth rate from 1988 to 1997, Global Biogeochem. Cycles, 2004, vol. 18, p. GB3011.

    Article  Google Scholar 

  4. Conrad, R., The global methane cycle: recent advances in understanding the microbial processes involved, Environ. Microbiol. Rep., 2009, vol. 1, no. 5, pp. 285–292.

    Article  CAS  PubMed  Google Scholar 

  5. Bapteste, E., Brochier, C., and Boucher, Y., Higherlevel classification of the Archaea: evolution of methanogenesis and methanogens, Archaea, 2005, vol. 1, pp. 353–363.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  6. Knittel, K. and Boetius, A., Anaerobic oxidation of methane: progress with an unknown process, Annu. Rev. Microbiol., 2009, vol. 63, pp. 311–334.

    Article  CAS  PubMed  Google Scholar 

  7. Springer, E., Sachs, M.S., Woese, C.R., and Boone, D.R., Partial gene sequences for the A subunit of methyl-coenzyme M reductase (mcrI) as a phylogenetic tool for the family Methanosarcinaceae, Int. J. Syst. Bacteriol., 1995, vol. 45, no. 3, pp. 554–559.

    Article  CAS  PubMed  Google Scholar 

  8. Hales, B.A., Edwards, C., Ritchie, D.A., Hall, G., Pickup, R.W., and Saunders, J.R., Isolation and identification of methanogen-specific DNA from blanket bog peat by PCR amplification and sequence analysis, Appl. Environ. Microbiol., 1996, vol. 62, pp. 668–675.

    CAS  PubMed Central  PubMed  Google Scholar 

  9. Luton, P.E., Wayne, J.M., Sharp, R.J., and Riley, P.W., The mcrA gene as an alternative to 16s rRNA in the phylogenetic analysis of methanogen populations in landfill, Microbiology (UK), 2002, vol. 148, pp. 3521–3530.

    CAS  Google Scholar 

  10. Hallam, S.J., Girguis, P.R., Preston, C.M., Richardson, P.M., and DeLong, E.F., Identification of methylcoenzyme M reductase A (mcrA) genes associated with methane-oxidizing archaea, Appl. Environ. Microbiol., 2003, vol. 69, pp. 5483–5491.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  11. Teske, A., Hinrichs, K.U., Edgcomb, V., de Vera Gomez, A., Kysela, D., Sylva, S.P., Sogin, M.L., and Jannasch, H.W., Microbial diversity of hydrothermal sediments in the Guaymas Basin: evidence for anaerobic methanotrophic communities, Appl. Environ. Microbiol., 2002, vol. 68, no. 4, pp. 1994–2007.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. Dhillon, A., Lever, M., Lloyd, K.G., Albert, D.B., Sogin, M.L., and Teske, A., Methanogen diversity evidenced by molecular characterization of methyl coenzyme M reductase A (mcrA) genes in hydrothermal sediments of the Guaymas Basin, Appl. Environ. Microbiol., 2005, vol. 71, no. 8, pp. 4592–4601.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  13. Jeanthon, C., Nercessian, O., Corre, E., and Grabowski-Lux, A., Hyperthermophilic and methanogenic Archaea in oil fields, in Petroleum Microbiology, Ollivier, B. and Magot, M., Eds., Washington, DC: ASM, 2005, pp. 55–69.

    Chapter  Google Scholar 

  14. Miroshnichenko, M.L. and Bonch-Osmolovskaya, E.A., Recent developments in the thermophilic microbiology of deep-sea hydrothermal vents, Extremophiles, 2006, vol. 10, pp. 85–96.

    Article  PubMed  Google Scholar 

  15. Ollivier, B. and Cayol, J.-L., Thermophilic methanoarchaea inhabiting hot ecosystems, in Handbook of Hydrocarbon Microbiology: Microbial Interactions with Hydrocarbons, Oils, Fats and Related Hydrophobic Substrates and Products, Berlin: Springer, 2010, pp. 681–691.

    Chapter  Google Scholar 

  16. Zeikus, J.G., The biology of methanogenic bacteria, Bacteriol. Rev., 1977, vol. 41, pp. 514–541.

    CAS  PubMed Central  PubMed  Google Scholar 

  17. Stetter, K.O., Thomm, M., Winter, J., Wildgruber, G., Huber, H., Zillig, W., Janecovic, D., Konig, H., Palm, P., and Wunderl, S., Methanothermus fervidus sp. nov., a novel extremely thermophilic methanogen isolated from an Icelandic hot spring, Zentralbl. Mikrobiol. Parasitenkd. Infektionskr. Hyg. Abt. 1 Orig., 1981, vol. 2, pp. 166–178.

    CAS  Google Scholar 

  18. Lauerer, G., Kristjansson, J.K., Langworthy, T.A., König, H., and Stetter, K.O., Methanothermus sociabilis sp. nov., a second species within the Methanothermaceae growing at 97°C, Syst. Appl. Microbiol., 1986, vol. 8, pp. 100–105.

    Article  Google Scholar 

  19. Bonch-Osmolovskaya, E.A. and Karpov, G.A., Microbial methane formation in Uzon caldera hydrothermal vents, Mikrobiologiya, 1987, vol. 56, no. 3, pp. 516–518.

    CAS  Google Scholar 

  20. Bonch-Osmolovskaya, E.A., Gorlenko, V.M., Karpov, G.A., and Starynin, D.A., Anaerobic destruction of organic matter in cyanobacterial mats of Thermophilny spring (Uzon, Kamchatka), Mikrobiologiya, 1987, vol. 56, no. 6, pp. 1022–1029.

    CAS  Google Scholar 

  21. Bonch-Osmolovskaya, E.A., Miroshnichenko, M.L., Slobodkin, A.I., Sokolova, T.G., Karpov, G.A., Kostrikina, N.A., Zavarzina, D.G., Prokof’eva, M.I., Rusanov I.I., and Pimenov, N.V., Biodiversity of anaerobic lithotrophic prokaryotes in terrestrial hot springs of Kamchatka, Microbiology (Moscow), 1999, vol. 68, no. 3, pp. 343–352.

    CAS  Google Scholar 

  22. Nozhevnikova, A.N. and Yagodina, T.G., A thermophilic acetate-consuming methane-producing bacterium, Mikrobiologiya, 1982, vol. 51, no. 6, pp. 642–647.

    CAS  Google Scholar 

  23. Maniatis, T., Fritsch, E.F., and Sambrook, J., Molecular Cloning. A Laboratory Manual, New York: Cold Spring Harbor Laboratory, 1982.

    Google Scholar 

  24. Tsai, Y.L. and Olson, B.H., Rapid method for direct extraction of DNA from soil and sediments, Appl. Environ. Microbiol., 1991, vol. 57, pp. 1070–1074.

    CAS  PubMed Central  PubMed  Google Scholar 

  25. Saiki, R.K., The design and optimization of the PCR, in PCR Technology: Principles and Applications for DNA Amplification, Erlich, H.A., Ed., New York: Stockton, 1989, pp. 7–16.

    Google Scholar 

  26. Muyzer, G., Brinkhoff, T., Nübel, U., Santegoeds, C., Schäfer, H., and Wawer, C., Denaturing gradient gel electrophoresis (DGGE) in microbial ecology, in Molecular Microbial Ecology Manual, Akkermans, A.D.L., van Elsas, J.D., and Bruijn, F.J., Eds., Dordrecht: Kluwer Academic Publishers, 1998, pp. 1–27.

    Google Scholar 

  27. Kubista, M., Andrade, J.M., Bengtsson, M., Forootan, A., Jonák, J., Lind, K., Sindelka, R., Sjöback, R., Sjögreen, B., Strömbom, L., Ståhlberg, A., and Zoric, N., The real-time polymerase chain reaction, Mol. Aspects Med., 2006, vol. 27, pp. 95–125

    Article  CAS  PubMed  Google Scholar 

  28. Steinberg, L.M. and Regan, J.M., Phylogenetic comparison of the methanogenic communities from an acidic, oligotrophic fen and an anaerobic digester treating municipal wastewater sludge, Appl. Environ. Microbiol., 2008, vol. 74, pp. 6663–6671.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. Lane, D., 16S/23S rRNA sequencing, in Nucleic Acid Techniques in Bacterial Systematics, Stackebrandt, E. and Goodfellow, M., Eds., West Sussex: Wiley, 1991, pp. 115–175.

    Google Scholar 

  30. Blank, C.E., Cady, S.L., and Pace, N.R., Microbial composition of near-boiling silica-depositing thermal springs throughout Yellowstone National Park, Appl. Environ. Microbiol., 2002, vol. 68, pp. 5123–5135.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. Einen, J., Thorseth, I.H., and Ovreas, L., Enumeration of Archaea and Bacteria in seafloor basalt using realtime quantitative PCR and fluorescence microscopy, FEMS Microbiol. Lett., 2008, vol. 282, pp. 182–187.

    Article  CAS  PubMed  Google Scholar 

  32. Hall, T.A., BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT, Nucleic Acids Symp. Ser., 1999, vol. 41, pp. 95–98.

    CAS  Google Scholar 

  33. Thompson, J.D., Higgins, D.G., and Gibson, T.J., CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice, Nucleic Acids Res., 1994, vol. 22, no. 22, pp. 4673–4680.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  34. Li, W. and Godzik, A., Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences, Bioinformatics, 2006, vol. 22, no. 13, pp. 1658–1659.

    Article  CAS  PubMed  Google Scholar 

  35. Ashelford, K.E., Chuzhanova, N.A., Fry, J.C., Jones, A.J., and Weightman, A.J., At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies, Appl. Environ. Microbiol., 2005, vol. 71, no. 12, pp. 7724–7736.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  36. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, Buchner, A., Lai, T., Steppi, S., Jobb, G., Förster, W., Brettske, I., Gerber, S., Ginhart, A.W., Gross, O., Grumann, S., Hermann, S., Jost, R., König, A., Liss, T., Lüssmann, R., May, M., Nonhoff, B., Reichel, B., Strehlow, R., Stamatakis, A., Stuckmann, N., Vilbig, A., Lenke, M., Ludwig, T., Bode, A., and Schleifer, K.H., ARB: a software environment for sequence data, Nucleic Acids Res., 2004, vol. 32, no. 4, pp. 1363–1371.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  37. Steinberg, L.M. and Regan, J.M., mcrA-Targeted realtime quantitative PCR method to examine methanogen communities, Appl. Environ. Microbiol., 2009, vol. 75, no. 13 P, pp. 4435–4442.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. Zhilina, T.N., Chudina, V.J., Ilarionov, S.A., and Bonch-Osmolovskaya, E.A., Thermophilic methaneproducing bacteria from “Methanobacillus kuzneceovii” methylotrophic associations, Mikrobiologiya, 1983, vol. 52, no. 2, pp. 328–335.

    CAS  Google Scholar 

  39. Ilarionov, S.A. and Bonch-Osmolovskaya, E.A., Methane formation from methanol by associations of microorganisms, Mikrobiologiya, 1986, vol. 55, no. 2, pp. 282–289.

    CAS  Google Scholar 

  40. Sakai, S., Imachi, H., Hanada, S., Ohashi, A., Harada, H., and Kamagata, Y., Methanocella paludicola gen. nov., sp. nov., a methane-producing archaeon, the first isolate of the lineage “Rice Cluster I”, and proposal of the new archaeal order Methanocellales ord. nov., Int. J. Syst. Evol. Microbiol., 2008, vol. 58, no. 4, pp. 929–936.

    Article  PubMed  Google Scholar 

  41. Sakai, S., Conrad, R., Liesack, W., and Imachi, H., Methanocella arvoryzae sp. nov., a hydrogenotrophic methanogen isolated from rice field soil, Int. J. Syst. Evol. Microbiol., 2010, vol. 60, no. 12, pp. 2918–2923.

    Article  CAS  PubMed  Google Scholar 

  42. Lü, Z. and Lu, Y., Methanocella conradii sp. nov., a thermophilic, obligate hydrogenotrophic methanogen, isolated from Chinese rice field soil, PLoS One, 2012, vol. 7, no. 4, e35279.

    Article  PubMed Central  PubMed  Google Scholar 

  43. 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  44. 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, pp. 1902–1907.

    Article  CAS  PubMed  Google Scholar 

  45. Iino, T., Tamaki, H., Tamazawa, S., Ueno, Y., Ohkuma, M., Suzuki, K.-I., Igarashi, Y., and Haruta, S., Candidatus Methanogranum caenicola: a novel methanogen from the anaerobic digested sludge, and proposal of Methanomassiliicoccaceae fam. nov. and Methanomassiliicoccales ord. nov., for a methanogenic lineage of the class Thermoplasmata, Microbes Environ., 2013, vol. 28, no. 2, pp. 244–250.

    Article  PubMed Central  PubMed  Google Scholar 

  46. Chernyh, N.A., Mardanov, A.V., Gumerov, V.M., Miroshnichenko, M.L., Lebedinsky, A.V., Merkel, A.Y., Crowe, D., Pimenov, N.V., Rusanov, I.I., Ravin, N.V., Moran, M.A., and Bonch-Osmolovskaya, E.A., Microbial life in Bourlyashchy, the hottest thermal pool of Uzon caldera, Kamchatka, ISME J., 2015 (submitted).

    Google Scholar 

  47. Ver Eecke, H.C., Butterfield, D.A., Huber, J.A., Lilley, M.D., Olson, E.J., Roe, K.K., Evanse, L.J., Merkel, A.Y., Cantin, H.V., and Holden, J.F., Hydrogen-limited growth of hyperthermophilic methanogens at deep-sea hydrothermal vents, Proc. Natl. Acad. Sci. U. S. A., 2012, vol. 109, no. 34, pp. 1364–1367.

    Google Scholar 

  48. Fry, J.C., Horsfield, B., Sykes, R., Cragg, B.A., Heywood, C., Kim, G.T., Mangelsdorf, K., Mildenhall, D.C., Rinna, J., Vieth, A., Zink, K.G., Sass, H., Weightman, A.J., and Parkes, R.J., Prokaryotic populations and activities in an interbedded coal deposit, including a previously deeply buried section (1.6–2.3 km) above ±150 Ma basement rock, Geomicrobiol. J., 2009, vol. 26, no. 3, pp. 163–178.

    Article  CAS  Google Scholar 

  49. Schulze-Makuch, D., Haque, S., de Sousa Antonio, M.R., Ali, D., Hosein, R., Song, Y.C., Yang, J., Zaikova, E., Beckles, D.M., Guinan, E., Lehto, H.J., and Hallam, S.J., Microbial life in a liquid asphalt desert, Astrobiology, 2011, vol. 11, no. 3, pp. 241–258.

    Article  PubMed  Google Scholar 

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Original Russian Text © A.Y. Merkel, O.A. Podosokorskaya, N.A. Chernyh, E.A. Bonch-Osmolovskaya, 2015, published in Mikrobiologiya, 2015, Vol. 84, No. 4, pp. 485–492.

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Merkel, A.Y., Podosokorskaya, O.A., Chernyh, N.A. et al. Occurrence, diversity, and abundance of methanogenic archaea in terrestrial hot springs of Kamchatka and Saõ Miguel Island. Microbiology 84, 577–583 (2015). https://doi.org/10.1134/S002626171504013X

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