Abstract
The thermoacidophilic microbial community inhabiting the groundwater with pH 4.0 and temperature 50°C at the East Thermal Field of Uzon Caldera, Kamchatka, was examined using pyrosequencing of the V3 region of the 16S rRNA gene. Bacteria comprise about 30% of microorganisms and are represented primarily by aerobic lithoautotrophs using the energy sources of volcanic origin—thermoacidophilic methanotrophs of the phylum Verrucomicrobia and Acidithiobacillus spp. oxidising metals and reduced sulfur compounds. More than 70% of microbial population in this habitat were represented by archaea, in majority affiliated with “uncultured” lineages. The most numerous group (39% of all archaea) represented a novel division in the phylum Euryarchaeota related to the order Thermoplasmatales. Another abundant group (33% of all archaea) was related to MCG1 lineage of the phylum Crenarchaeota, originally detected in the Yellowstone hot spring as the environmental clone pJP89. The organisms belonging to these two groups are widely spread in hydrothermal environments worldwide. These data indicate an important environmental role of these two archaeal groups and should stimulate the investigation of their metabolism by cultivation or metagenomic approaches.
This is a preview of subscription content, access via your institution.




References
Barns SM, Fundyga RE, Jeffries MW, Pace NR (1994) Remarkable archaeal diversity detected in a Yellowstone National Park hot spring environment. Proc Natl Acad Sci USA 91:1609–1613
Barns SM, Delwiche CF, Palmer JD, Pace NR (1996) Perspectives on archaeal diversity, thermophily and monophyly from environmental rRNA sequences. Proc Natl Acad Sci USA 93:9188–9193
Bazhenova OK, Arefiev OA, Frolov EB (1998) Oil of the volcano Uzon caldera, Kamchatka. Org Geochem 29:421–428
Bonch-Osmolovskaya EA (2004) Studies of thermophilic microorganisms at the Institute of Microbiology, Russian Academy of Sciences. Mikrobiologiia 73:644–658
Bonch-Osmolovskaya EA, Sokolova TG, Kostrikina NA, Zavarzin GA (1990) Desulfurella acetivorans gen. nov. and sp. nov.—a new thermophilic sulfur-reducing eubacterium. Arch Microbiol 153:151–155
Bonch-Osmolovskaya EA, Miroshnichenko ML, Slobodkin AI, Sokolova TG, Karpov GA, Kostrikina NA, Zavarzina DG, Prokofeva MI, Rusanov II, Pimenov NV (1999) Biodiversity of anaerobic lithotrophic prokaryotes in terrestrial hot springs of Kamchatka. Mikrobiologiia 68:398–406
Chao A (1984) Non-parametric estimation of the number of classes in a population. Scand J Statist 11:265–270
Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–D145
Dunfield PF, Yuryev A, Senin P, Smirnova AV, Stott MB, Hou S, Ly B, Saw JH, Zhou Z, Ren Y, Wang J, Mountain BW, Crowe MA, Weatherby TM, Bodelier PLE, Liesack W, Feng L, Wang L, Alam M (2007) Methane oxidation by an extremely acidophilic bacterium of the phylum Verrucomicrobia. Nature 450:879–882
Godon JJ, Zumstein E, Dabert P, Habouzit F, Moletta R (1997) Molecular microbial diversity of an anaerobic digestor as determined by small-subunit rDNA sequence analysis. Appl Environ Microbiol 63:2802–2813
Hohn M, Headlund BP, Huber H (2002) Detection of 16S rDNA sequences representing the novel phylum “Nanoarchaeota”: indication for a wide distribution in high temperature biotopes. Syst Appl Microbiol 25:551–554
Hugenholtz P, Pitulle C, Hershberger KL, Pace NR (1998) Novel division level bacterial diversity in a Yellowstone hot spring. J Bacteriol 180:366–376
Islam T, Jensen S, Reigstad LJ, Larsen O, Birkeland NK (2008) Methane oxidation at 55°C and pH 2 by a thermoacidophilic bacterium belonging to the Verrucomicrobia phylum. Proc Natl Acad Sci USA 105:300–304
Kletzin A (2007) General characteristics and important model organisms. In: Cavicchioli R (ed) Archaea: molecular and cellular biology. ASM Press, Washington, pp 14–92
Kublanov IV, Perevalova AA, Slobodkina GB, Lebedinsky AV, Bidzhieva SKh, Kolganova TV, Kaliberda EN, Rumsh LD, Haertlé T, Bonch-Osmolovskaya EA (2009) Biodiversity of thermophilic prokaryotes with hydrolytic activities in hot springs of Uzon Caldera, Kamchatka. Appl Environ Microbiol 75:286–291
Kvist T, Ahring BK, Westermann P (2007) Archaeal diversity in Icelandic hot springs. FEMS Microbiol Ecol 59:71–80
Meyer-Dombard DR, Shock EL, Amend JP (2005) Archaeal and bacterial communities in geochemically diverse hot springs of Yellowstone National Park, USA. Geobiology 3:211–227
Miller SR, Strong AL, Jones KL, Ungerer MC (2009) Bar-coded pyrosequencing reveals shared bacterial community properties along the temperature gradients of two alkaline hot springs in Yellowstone National Park. Appl Environ Microbiol 75:4565–4572
Miroshnichenko ML, Tourova TP, Kolganova TV, Kostrikina NA, Chernyh NA, Bonch-Osmolovskaya EA (2008) Ammonifex thiophilus sp. nov., a novel hyperthermophilic anaerobic bacterium from Kamchatka hot spring. Int J Syst Evol Microbiol 58:2935–2938
Miroshnichenko ML, Lebedinsky AV, Chernyh NA, Tourova TP, Kolganova TV, Spring S, Bonch-Osmolovskaya EA (2009) Caldimicrobium rimae gen. nov., sp. nov., an extremely thermophilic, facultatively lithoautotrophic, anaerobic bacterium from the Uzon Caldera, Kamchatka. Int J Syst Evol Microbiol 59:1040–1044
Nazina TN, Tourova TP, Poltaraus AB, Novikova EV, Grigoryan AA, Ivanova AE, Lysenko AM, Petrunyaka VV, Osipov GA, Belyaev SS, Ivanov MV (2001) Taxonomic study of aerobic thermophilic bacilli: descriptions of Geobacillus subterraneus gen. nov., sp. nov. and Geobacillus uzenensis sp. nov. from petroleum reservoirs and transfer of Bacillus stearothermophilus, Bacillus thermocatenulatus, Bacillus thermoleovorans, Bacillus kaustophilus, Bacillus thermoglucosidasius and Bacillus thermodenitrificans to Geobacillus as the new combinations G. stearothermophilus, G. thermocatenulatus, G. thermoleovorans, G. kaustophilus, G. thermoglucosidasius and G. thermodenitrificans. Int J Syst Evol Microbiol 51:433–446
Op den Camp HJM, Islam T, Stott MB, Harhangi HR, Hynes A, Schouten S, Jetten MSM, Birkeland N-K, Pol A, Dunfield PF (2009) Environmental, genomic and taxonomic perspectives on methanotrophic Verrucomicrobia. Environ Microbiol Rep 1:293–306
Perevalova AA, Kolganova TV, Birkeland NK, Schleper C, Bonch-Osmolovskaya EA, Lebedinsky AV (2008) Distribution of Crenarchaeota representatives in terrestrial hot springs of Russia and Iceland. Appl Environ Microbiol 74:7620–7628
Perevalova AA, Bidzhieva SK, Kublanov IV, Hinrichs KU, Liu XL, Mardanov AV, Lebedinsky AV, Bonch-Osmolovskaya EA (2010) Fervidicoccus fontis gen. nov., sp. nov., a novel anaerobic thermophilic crenarchaeote from hot springs in Kamchatka, and proposal of Fervidicoccaceae fam. nov. and Fervidicoccales ord. nov. Int J Syst Evol Microbiol 60:2082–2088
Pimenov NV, Bonch-Osmolovskaya EA (2006) In situ activities in thermal environments. In: Rainey F, Oren A (eds) Methods in microbiology, vol 14. Elsevier, Amsterdam
Pol A, Heijmans K, Harhangi HR, Tedesco D, Jetten MS, Op den Camp HJ (2007) Methanotrophy below pH 1 by a new Verrucomicrobia species. Nature 450:874–878
Prokofeva MI, Rusanov II, Pimenov NV, Bonch-Osmolovskaya EA (2006) Organotrophic activity in Kamchatka hot springs with low pH. Mikrobiologiia 75:284–286
Prokofeva MI, Kostrikina NA, Kolganova TV, Tourova TP, Lysenko AM, Lebedinsky AV, Bonch-Osmolovskaya EA (2009) Isolation of the anaerobic thermoacidophilic crenarchaeote Acidilobus saccharovorans sp. nov. and proposal of Acidilobales ord. nov., including Acidilobaceae fam. nov. and Caldisphaeraceae fam. nov. Int J Syst Evol Microbiol 59:3116–3122
Reigstad LJ, Richter A, Daims H, Urich T, Schwark L, Schleper C (2008) Nitrification in terrestrial hot springs of Iceland and Kamchatka. FEMS Microbiol Ecol 64:167–174
Reigstad LJ, Jorgensen SL, Schleper C (2010) Diversity and abundance of Korarchaeota in terrestrial hot springs of Iceland and Kamchatka. ISME J 4:346–356
Simoneit BRT, Deamer DW, Kompanichenko V (2009) Characterization of hydrothermally generated oil from the Uzon caldera, Kamchatka. Appl Geochem 24:303–309
Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM, Neal PR, Arrieta JA, Herndl GH (2006) Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci USA 103:12115–12120
Spear JR, Walker JJ, McCollom TM, Pace N (2005) Hydrogen and bioenergetics in the Yellowstone geothermal ecosystem. Proc Natl Acad Sci USA 102:2555–2560
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882
Valdes J, Pedroso I, Quatrini R, Dodson RJ, Tettelin H, Blake R, Eisen JA, Holmes DS (2008) Acidithiobacillus ferrooxidans metabolism: from genome sequence to industrial applications. BMC Genomics 9:597
Valdes J, Quatrini R, Hallberg K, Dopson M, Valenzuela PDT, Holmes DS (2009) Draft genome sequence of the extremely acidophilic bacterium Acidithiobacillus caldus ATCC 51756 reveals metabolic versatility in the genus Acidithiobacillus. J Bacteriol 191:5877–5878
Van de Peer Y, De Wachter R (1994) TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Comput Appl Biosci 10:569–570
Zaporozhenko EV, Slobodova NV, Bulygina ES, Kravchenko IK, Kuznetsov BB (2006) Method for rapid DNA extraction from bacterial communities of different soils. Mikrobiologiia 75:127–134
Acknowledgments
This work was supported by Russian Foundation for Basic Research (grant 08-04-01273) and Ministry of education and sciences of Russia (state programme “Research and educational specialists of innovative Russia”, contract P1049). Work of E.B.-O. and A.P. was funded by the Programs of RAS “Molecular and Cell Biology” and “The Origin and Evolution of Biosphere”.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by A. Oren.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Mardanov, A.V., Gumerov, V.M., Beletsky, A.V. et al. Uncultured archaea dominate in the thermal groundwater of Uzon Caldera, Kamchatka. Extremophiles 15, 365–372 (2011). https://doi.org/10.1007/s00792-011-0368-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00792-011-0368-1
Keywords
- Microbial community
- Thermoacidophiles
- Pyrosequencing
- Thermal groundwater
- Uncultured archaea
- Uzon Caldera