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Diversity of methanogenic archaea from the 2012 terrestrial hot spring (Valley of Geysers, Kamchatka)

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Abstract

Archaeal diversity in the 2012 terrestrial hot spring (Valley of Geysers, Kronotsky Nature Reserve, Kamchatka, Russia) was investigated using molecular and cultivation-based approaches. Analysis of the 16S rRNA gene sequences revealed predominance among archaea of uncultured microorganisms of the pSL12 and THSCG clusters. Analysis of the mcrA genes revealed that members of the order Methanomassiliicoccales were predominant (68%) among methanogens; the latter constituted 0.15% of the total number of archaea. Five stable thermophilic methanogenic associations utilizing hydrogen, formate, acetate, or methanol as substrates were obtained from the sediments of spring 2012. The diversity of cultured methanogens was limited to members of the genera Methanothermobacter, Methanothrix, and Methanomethylovorans. The association growing at 65°C and producing methane from methanol contained two components, which probably formed a syntrophic relationship: a Methanothermobacter methanogenic archaeon and a bacterium representing an separate cluster within the Firmicutes phylum, which was phylogenetically related to the genera Thermacetogenium and Syntrophaceticus. These data indicate high diversity of methanogens, notwithstanding their low abundance among archaea. The group of thermophilic Methanomassiliicoccales, which predominated among methanogens, is of special interest.

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References

  • 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  PubMed Central  Google Scholar 

  • Borrel, G., Harris, H.M.B., Parisot, N., Gaci, N., Tottey, W., Mihajlosvki, A., Deane, J., Gribaldo, S., Bardot, O., Peyretaillade, E., Peyret, P., O’Toole, P.W., and Brugère, J.-F., Genome sequence of “Candidatus Methanomassiliicoccus intestinalis” Issoire-Mx1, a third Thermoplasmatalesrelated methanogenic archaeon from human feces, Genome Announc., 2013, vol. 1, no. 4, pp. e00453–13.

    Article  PubMed  PubMed Central  Google Scholar 

  • Borrel, G., Harris, H.M.B., Tottey, W., Mihajlovski, A., Parisot, N., Peyretaillade, E., Peyret, P., O’Toole, P.W., and Brugere, J.F., Genome sequence of “Candidatus Methanomethylophilus alvus” Mx1201, a methanogenic archaea from the human gut belonging to a seventh order of methanogens, J. Bacteriol., 2012, vol. 194, pp. 6944–6945.

    CAS  PubMed  Google Scholar 

  • 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 

  • 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 

  • 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 

  • Chernyh, N.A., Mardanov, A.V., Gumerov, V.M., Miroshnichenko, M.L., Lebedinsky, A.V., Merkel, A.Y., Growe, 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, Extremophiles, 2015, vol. 19, no. 6, pp. 1157–1171.

    CAS  PubMed  Google Scholar 

  • Chojnacka, A., Szczesny, P., Blaszczyk, M.K., Zielenkiewicz, U., Detman, A., Salamon, A., and Sikora, A., Noteworthy facts about a methane-producing microbial community processing acidic effluent from sugar beet molasses fermentation, PLoS One, 2015, vol. 10, no. 5. e0128008.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 

  • Flores, G.E., Shakya, M., Meneghin, J., Yang, Z.K., Seewald, J.S., Geoff Wheat, C., Podar, M., and Reysenbach, A.L., Inter-field variability in the microbial communities of hydrothermal vent deposits from a back-arc basin, Geobiology, 2012, vol. 10, no. 4, pp. 333–346.

    Article  CAS  PubMed  Google Scholar 

  • Gumerov, V.M., Mardanov, A.V., Beletsky, A.V., Bonch-Osmolovskaya, E.A., and Ravin, N.V., Molecular analysis of microbial diversity in the Zavarzin Spring, Uzon caldera, Kamchatka, Microbiology (Moscow), 2011, vol. 80, no. 2, pp. 244–251.

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Hattori, S., Kamagata, Y., Hanada, S., and Shoun H., Thermacetogenium phaeum gen. nov., sp. nov., a strictly anaerobic, thermophilic, syntrophic acetate-oxidizing bacterium, Int. J. Syst. Evol. Microbiol., 2000, vol. 50, pp. 1601–1609.

    CAS  PubMed  Google Scholar 

  • Iino, T., Tamaki, H., Tamazawa, S., Ueno, Y., Ohkuma, M., Suziki, 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  PubMed Central  Google Scholar 

  • Jones, W.J., Leigh, J.A., Mayer, F., Woese, C.R., and Wolfe, R.S., Methanococcus jannaschii sp. nov., an extremely thermophilic methanogen from a submarine hydrothermal vent, Arch. Microbiol., 1983, vol. 136, pp. 254–261.

    CAS  Google Scholar 

  • Kurr, M., Huber, R., König, H., Jannasch, H.W., Fricke, H., Trincone, A., Kristjansson, J.K., and Stetter, K.O., Methanopyrus kandleri, gen. and sp. nov. represents a novel group of hyperthermophilic methanogens, growing at 110°C, Arch. Microbiol., 1991, vol. 156, pp. 239–247.

    CAS  Google Scholar 

  • Lang, K., Schuldes, J., Klingl, A., Poehlein, A., Daniel, R., and Brunea, A., New mode of energy metabolism in the seventh order of methanogens as revealed by comparative genome analysis of “Candidatus Methanoplasma termitum,” Appl. Environ. Microbiol., 2015, vol. 81, no. 4, pp. 1338–1352.

  • 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.

    Google Scholar 

  • Lever, M.A. and Teske, A.P., Diversity of methane-cycling archaea in hydrothermal sediment investigated by general and group-specific PCR primers, Appl. Environ. Microbiol., 2015, vol. 81, no. 4, pp. 1426–1441.

    Article  PubMed  Google Scholar 

  • 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 

  • Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Buchner, A., Lai, T., Steppi, S., Jobb, G., Förster, W., Brettske, I., Gerber, S., Ginhart, A.W., Gross, O., et al., ARB: a software environment for sequence data, Nucleic Acids. Res., 2004, vol. 32, no. 4, pp. 1363–1371.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mardanov, A.V., Gumerov, V.M., Beletsky, A.V., Bonch-Osmolovskaya, E.A., Ravin, N.V., and Skryabin, K.G., Characteristic of biodiversity of thermophilic microbial community by parallel pyrosequencing method, Dokl. Biochem. Biophys., 2010, vol. 432, pp. 110–113.

    Article  CAS  PubMed  Google Scholar 

  • Merkel, A.Y., Podosokorskaya, O.A., Chernyh, N.A., and Bonch-Osmolovskaya, E.A., Occurrence, diversity, and abundance of methanogenic Archaea in terrestrial hot springs of Kamchatka and Sao Miguel island, Microbiology (Moscow), 2015a, vol. 84, no. 4, pp. 577–583.

    CAS  Google Scholar 

  • Merkel, A.Y., Korneeva, V.A., Tarnovetskii, I.Yu., Bryukhanov, A.L., Chasovnikov, V.K., Taranov, E.A., Toshchakov, S.V., and Pimenov N.V., Structure of the archaeal community in the Black Sea photic zone, Microbiology (Moscow), 2015b, vol. 84, no. 4, pp. 570–576.

    Article  CAS  Google Scholar 

  • 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 

  • Nozhevnikova, A.N. and Chudina, V.I., Morphology of the thermophilic acetate bacterium Methanothrix thermoacetophila sp. nov., Mikrobiologiya, 1984, vol. 53, no. 5, pp. 756–760.

    Google Scholar 

  • Nozhevnikova, A.N. and Yagodina, T.G., A thermophilic acetate-consuming methane-producing bacterium, Mikrobiologiya, 1982, vol. 51, no. 4, pp. 642–649.

    CAS  Google Scholar 

  • 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 

  • Rozanov, A.S., Bryanskaya, A.V., Malup, T.K., Meshcheryakova, I.A., Lazareva, E.V., Taran, O.P., Ivanisenko, T.V., Ivanisenko, V.A., Zhmodik, S.M., Kolchanov, N.A., and Peltek, S.E., Molecular analysis of the benthos microbial community in Zavarzin thermal spring (Uzon Caldera, Kamchatka, Russia), BMC Genomics, 2014, vol. 15. Suppl. 12. S12.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sandbeck, K.A. and Ward, D.M., Fate of immediate methane precursors in low-sulfate, hot-spring algal-bacterial mats, Appl. Environ. Microbiol., 1981, vol. 41, no. 3, pp. 775–782.

    CAS  PubMed  Google Scholar 

  • Schink, B. and Zeikus. J.G., Microbial methanol formation: a major end product of pectin metabolism, Curr. Microbiol., 1980, vol. 4, pp. 387–389.

    Article  CAS  Google Scholar 

  • 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, no. 21, pp. 6663–6671.

    CAS  PubMed  Google Scholar 

  • 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, Ztbl. Mikrobiol. Parasitenkd. Infektionskr. Hyg. Abt. 1 Orig., 1981, vol. 2, pp. 166–178.

    CAS  Google Scholar 

  • Stewart, L.C., Jung, J.H., Kim, Y.T., Kwon, S.W., Park, C.S., and Holden, J.F., Methanocaldococcus bathoardescens sp. nov., a hyperthermophilic methanogen isolated from a volcanically active deep-sea hydrothermal vent, Int. J. Syst. Evol. Microbiol., 2015, vol. 65, pp. 1280–1283.

    CAS  PubMed  Google Scholar 

  • Takai, K., Nealson, K.H., and Horikoshi, K., Methanotorris formicicus sp. nov., a novel extremely thermophilic, methane-producing archaeon isolated from a black smoker chimney in the Central Indian Ridge, Int. J. Syst. Evol. Microbiol., 2004, vol. 54, pp. 1095–1100.

    CAS  PubMed  Google Scholar 

  • 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  PubMed Central  Google Scholar 

  • Tveit, A.T., Urich, T., Frenzel, P., and Svenning, M.M., Metabolic and trophic interactions modulate methane production by Arctic peat microbiota in response to warming, Proc. Natl. Acad. Sci. U. S. A., 2015, pp. E2507–E2516.

    Google Scholar 

  • Ward, D.M. and Olson, G.J., Terminal processes in the anaerobic degradation of an algal-bacterial mat in a highsulfate hot spring, Appl. Environ. Microbiol., 1980, vol. 40, no. 1, pp. 67–74.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Watanabe, T., Kimura, M., and Asakawa, S., Distinct members of a stable methanogenic archaeal community transcribe mcrA genes under flooded and drained conditions in Japanese paddy field soil, Soil Biol. Biochem., 2009, vol. 41, pp. 276–285.

    Article  CAS  Google Scholar 

  • Westerholm, M., Roos, S., and Schnürer, A., Syntrophaceticus schinkii gen. nov., sp. nov., an anaerobic, syntrophic acetate-oxidizing bacterium isolated from a mesophilic anaerobic filter, FEMS Microbiol. Lett., 2010, vol. 309, no. 1, pp. 100–104.

    CAS  PubMed  Google Scholar 

  • Yarza, P., Yilmaz, P., Pruesse, E., Glöckner, F.O., Ludwig, W., Schleifer, K.H., Whitman, W.B., Euzéby, J., Amann, R., and Rosselló-Móra, R., Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences, Nat. Rev. Microbiol., 2014, vol. 12, no. 9, pp. 635–645.

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zeikus, J.G. and Wolfe, R.S., Methanobacterium thermoautotrophicus sp. n., an anaerobic, autotrophic, extreme thermophile, J. Bacteriol., 1972, vol. 109, pp. 707–713.

    CAS  PubMed  Google Scholar 

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Correspondence to A. Y. Merkel.

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Original Russian Text © A.Y. Merkel, O.A. Podosokorskaya, T.G. Sokolova, E.A. Bonch-Osmolovskaya, 2016, published in Mikrobiologiya, 2016, Vol. 85, No. 3, pp. 327–336.

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Merkel, A.Y., Podosokorskaya, O.A., Sokolova, T.G. et al. Diversity of methanogenic archaea from the 2012 terrestrial hot spring (Valley of Geysers, Kamchatka). Microbiology 85, 342–349 (2016). https://doi.org/10.1134/S0026261716030073

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