Skip to main content
SpringerLink
Log in

Microbial diversity and autotrophic activity in Kamchatka hot springs

  • Original Paper
  • Published:
Extremophiles Aims and scope Submit manuscript

Abstract

Microbial communities of Kamchatka Peninsula terrestrial hot springs were studied using molecular, radioisotopic and cultural approaches. Analysis of 16S rRNA gene fragments performed by means of high-throughput sequencing revealed that aerobic autotrophic sulfur-oxidizing bacteria of the genus Sulfurihydrogenibium (phylum Aquificae) dominated in a majority of streamers. Another widely distributed and abundant group was that of anaerobic bacteria of the genus Caldimicrobium (phylum Thermodesulfobacteria). Archaea of the genus Vulcanisaeta were abundant in a high-temperature, slightly acidic hot spring, where they were accompanied by numerous Nanoarchaeota, while the domination of uncultured Thermoplasmataceae A10 was characteristic for moderately thermophilic acidic habitats. The highest rates of inorganic carbon assimilation determined by the in situ incubation of samples in the presence of 14C-labeled bicarbonate were found in oxygen-dependent streamers; in two sediment samples taken from the hottest springs this process, though much weaker, was found to be not dependent on oxygen. The isolation of anaerobic lithoautotrophic prokaryotes from Kamchatka hot springs revealed a wide distribution of the ability for sulfur disproportionation, a new lithoautotrophic process capable to fuel autonomous anaerobic ecosystems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Auchtung TA, Shyndriayeva G, Cavanaugh CM (2011) 16S rRNA phylogenetic analysis and quantification of Korarchaeota indigenous to the hot springs of Kamchatka, Russia. Extremophiles 15:105–116

    Article  CAS  PubMed  Google Scholar 

  • Baker BJ, Banfield JF (2003) Microbial communities in acid mine drainage. FEMS Microbiol Ecol 44:139–152

    Article  CAS  PubMed  Google Scholar 

  • Benson DA, Boguski MS, Lipman DJ, Ostell J, Ouellette BF, Rapp BA, Wheeler DL (1999) GenBank. Nucleic Acids Res 27:12–17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonch-Osmolovskaya EA (2004) Studies of thermophilic microorganisms at the Institute of Microbiology, Russian Academy of Sciences. Microbiology (English translation of Microbiologiia) 73:644–658

    Google Scholar 

  • Bonch-Osmolovskaya EA, Gorlenko VM, Karpov GA, Starynin DA (1987) Anaerobic destruction of the organic matter in microbial mats of the Thermofilny Spring (Uzon Caldera, Kamchatka). Microbiology (English translation of Microbiologiia) 56:812–818

    Google Scholar 

  • Bonch-Osmolovskaya EA, Sokolova TG, Kostrikina NA, Zavarzin GA (1990) Desulfurella acetivorans gen. nov., sp. nov., a new thermophilic sulfur-reducing bacterium. Arch Microbiol 153:151–155

    Article  Google Scholar 

  • 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 spring of Kamchatka. Microbiology (English translation of Microbiologiia) 68:398–406

    Google Scholar 

  • Burgess EA, Unrine JM, Mills GL, Romanek CS, Wiegel J (2012) Comparative geochemical and microbiological characteristization of two thermal pools in Uzon Caldera, Kamchatka, Russia. Microb Ecol 63:471–489

    Article  PubMed  Google Scholar 

  • Chao A (1984) Nonparametric estimation of the number of classes in a population. Scandinavian J Statistics 11:265–270

    Google Scholar 

  • Chernyh NA, Mardanov AV, Gumerov VM, Miroshnichenko ML, Lebedinsky AV, Merkel AY, Crowe D, Pimenov NV, Rusanov II, Ravin NV, Moran MA, Bonch-Osmolovskaya EA (2015) Microbial life in Bourlyashchy, the hottest thermal pool of Uzon Caldera, Kamchatka. Extremophiles 19:1157–1171

    Article  CAS  PubMed  Google Scholar 

  • Dobretsov NI, Lazareva EV, Zhmodik SM, Bryanskaya AV, Morozova VV, Tikunova NV, Peltek SE, Karpov GA, Taran OP, Ogorodmikova OL, Kirichenko IS, Rozanov AS, Babkin IV, Shyvaeva OV, Chebykin EP (2015) Geological, hydrochemical and microbiological characteristics of the Oil site of the Uzon Caldera (Kamchatka). Russ Geol Geophys 56:39–63

    Article  Google Scholar 

  • Fadrosh DW, Ma B, Gajer P, Sengamalay N, Ott S, Brotman RM, Ravel J (2014) An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform. Microbiome 2(1):6

    Article  PubMed  PubMed Central  Google Scholar 

  • Frolov EN, Merkel AYu, Pimenov NV, Kvashchevskaya AA, Bonch-Osmolovskaya EA, Chernyh NA (2016a) Sulfate reduction and inorganic carbon assimilation in acidic thermal springs of the Kamchatka Peninsula. Microbiology (English translation of Microbiologiia) 85:471–480

    CAS  Google Scholar 

  • Frolov EN, Kublanov IV, Toshchakov S, Bonch-Osmolovskaya EA, Novikov AA, Chernyh NA (2016b) Thermodesulfobium acidiphilum sp. nov., a new thermoacidophilic sulfate-reducing chemoautotrophic bacterium from a Kamchatkan thermal site. Int J Syst Evol Microbiol. doi:10.1099/ijsem.0.001745

  • Gorlenko VM, Kachalkin VA, Bonch-Osmolovskaya EA, Starynin DA (1987) Production processes in microbial cenoses of the Thermofilnyi hot spring. Microbiology (English translation of Microbiologiia) 56:692–697

    Google Scholar 

  • Gumerov VM, Mardanov AV, Beletsky AV, Bonch-Osmolovskaya EA, Ravin NV (2011) Molecular analysis of microbial diversity in Zavarzin Spring, the Uzon Caldera, Kamchatka. Microbiology (English translation of Microbiologiia) 80:244–251

    CAS  Google Scholar 

  • Hetzer A, Morgan HW, McDonald IR, Daughney CJ (2007) Microbial life in Champagne Pool, a geothermal spring in Waiotapu, New Zealand. Extremophiles 11:605–614

    Article  PubMed  Google Scholar 

  • Hohn MJ, Hedlund 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

    Article  CAS  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  PubMed Central  Google Scholar 

  • Inskeep WP, Jay ZJ, Tringe SG, Herrgård MJ, Rusc DB (2013) The YNP metagenome project: environmental parameters responsible for microbial distribution in the Yellowstone geothermal ecosystem. Front Microbiol 4:67

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kato S, Itoh T, Yamagishi A (2011) Archaeal diversity in a terrestrial acidic spring field revealed by a novel PCR primer targeting archaeal 16S rRNA genes. FEMS Microbiol Lett 319(1):34–43

    Article  CAS  PubMed  Google Scholar 

  • Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS, Lee JH, Yi H, Won S, Chun J (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–717

    Article  CAS  PubMed  Google Scholar 

  • Kochetkova TV, Rusanov II, Pimenov NV, Kolganova TV, Lebedinsky AV, Bonch-Osmolovskaya EA, Sokolova TG (2011) Anaerobic transformation of carbon monoxide by microbial communities of Kamchatka hot springs. Extremophiles 15:319–325

    Article  CAS  PubMed  Google Scholar 

  • Kojima H, Umezawa K, Fukui M (2016) Caldimicrobium thiodismutans sp. nov., a sulfur-disproportionating bacterium isolated from a hot spring, and emended description of the genus Caldimicrobium. Int J Syst Evol Microbiol 66:1828–1831

    Article  CAS  PubMed  Google Scholar 

  • Lebedeva EV, Hatzenpichler R, Pelletier E, Schuster N, Hauzmayer S, Bulaev A, Grigor’eva NV, Galushko A, Schmid M, Palatinszky M, Le Paslier D, Daims H, Wagner M (2013) Enrichment and genome sequence of the group I.1a ammonia-oxidizing Archaeon “Ca. Nitrosotenuis uzonensis” representing a clade globally distributed in thermal habitats. PLoS ONE 8(11):e80835

    Article  PubMed  PubMed Central  Google Scholar 

  • Lever MA, Torti A, Eickenbusch P, Michaud AB, Šantl-Temkiv T, Jørgensen BB (2015) A modular method for the extraction of DNA and RNA, and the separation of DNA pools from diverse environmental sample types. Front Microbiol 16:476

    Google Scholar 

  • Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mardanov AV, Gumerov VM, Beletsky AV, Perevalova AA, Karpov GA, Bonch-Osmolovskaya EA, Ravin NA, Skryabin KG (2011) Uncultured archaea dominate in the thermal groundwater of Uzon Caldera, Kamchatka. Extremophiles 15:365–372

    Article  PubMed  Google Scholar 

  • Menzel P, Gudbergsdottir SR, Rike AG, Lin L, Zhang Q, Contursi P, Moracci M, Krostjansson JK, Bolduc B, Gavrilov S, Ravin N, Mardanov A, Bonch-Osmolovskaya E, Young M, Krogh A, Peng X (2015) Comparative metagenomic of eight geographically remote terrestrial hot springs. Microb Ecol 70:411–424

    Article  PubMed  Google Scholar 

  • Merkel AY, Podosokorskaya OA, Chernyh NA, Bonch Osmolovskaya EA (2015) Occurrence, diversity, and abundance of methanogenic archaea in terrestrial hot springs of Kamchatka and Sao Miguel Island. Microbiology (English translation of Microbiologiia) 84:577–583

    CAS  Google Scholar 

  • Miroshnichenko ML, Kostrikina NA, Rainey FA, Hippe H, Bonch-Osmolovskaya EA (1998) Desulfurella kamchatkensis sp. nov. and Desulfurella propionica sp. nov., new thermophilic sulfur-reducing bacteria from Kamchatka hot vents. Int J Syst Bacteriol 48:475–479

    Article  PubMed  Google Scholar 

  • Miroshnichenko ML, Tourova TP, Kolganova TP, Kostrikina NA, Bonch-Osmolovskaya EA (2008) Ammonifex thiophilus sp. nov., a hyperthermophilic anaerobic bacterium from a Kamchatka hot spring. Int J Syst Evol Microbiol 58:2935–2938

    Article  CAS  PubMed  Google Scholar 

  • Miroshnichenko ML, Lebedinsky AV, Chernyh NA, Tourova TP, Kolganova TV, Spring S, Bonch-Osmolovskaya EA (2009) Caldimicrobium rimae gen. nov., sp. nov., a novel extremely thermophilic facultatively lithoautotrophic anaerobic bacterium from the Uzon Caldera. Kamchatka. Int J Syst Evol Microbiol 59:1040–1044

    Article  CAS  PubMed  Google Scholar 

  • Nakagawa T, Fukui M (2003) Molecular characterization of community structures and sulfur metabolism within microbial streamers in Japanese Hot Springs. Appl Environ Microbiol 69:7044–7057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Neill A, Liu Y, Ferrera I, Beveridge TJ, Reysenbach A-L (2008) Sulfurihydrogenibium rodmanii sp. nov., a sulfur-oxidizing chemolithoautotroph from Uzon Caldera, Kamchatka Peninsula, Russia, and emended description of genus Sulfurihydrogenibium. Int J Syst Evol Microbiol 58:1147–1152

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perevalova AA, Kublanov IV, Baslerov RV, Bonch-Osmolovskaya EA (2013) Brockia lithotrophica gen. nov., sp. nov., a novel anaerobic thermophilic bacterium from a terrestrial hot spring. Intern. J Syst Evol Microbiol 63:479–483

    Article  CAS  Google Scholar 

  • Prokofeva MI, Rusanov II, Pimenov NV (2006) Organotrophic activity in Kamchatka hot springs with low pH. Microbiology (English translation of Microbiologiia) 75:237–239

    CAS  Google Scholar 

  • Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucl Acids Res 41:D590–D596

    Article  CAS  PubMed  Google Scholar 

  • Reysenbach AL, Ehringer M, Hershberger K (2000) Microbial diversity at 83 degrees C in Calcite Springs, Yellowstone National Park: another environment where the Aquificales and “Korarchaeota” coexist. Extremophiles 4:61–67

    CAS  PubMed  Google Scholar 

  • Rozanov AS, Bryanskaya AV, Malup TK, Lazareva EV, Taran OP, Ivanisenko TV, Zhmodik SM, Kolchanov NA, Peltek SE (2014) Molecular analysis of the benthos microbial community in Zavarzin thermal spring (Uzon Caldera, Kamchatka, Russia). BMC Genom 15(Suppl. 12):S12

    Article  Google Scholar 

  • Sahm K, John P, Nacke H, Wemheuer B, Grote R, Daniel R, Antranikian (2013) High abundance of heterotrophic prokaryotes in hydrothermal springs of the Azores as revealed by a network of 16S rRNA gene-based methods. Extremophiles 17:649–662

    Article  CAS  PubMed  Google Scholar 

  • Slobodkin AI, Reysenbach A-L, Slobodkina GB, Baslerov RV, Kostrikina NA, Wagner ID, Bonch-Osmolovskaya EA (2012) Thermosulfurimonas dismutans gen. nov., sp. nov. a novel extremely thermophilic sulfur-disproportionating bacterium from a deep-sea hydrothermal vent. Int J Syst Evol Microbiol 62:2565–2571

    Article  CAS  PubMed  Google Scholar 

  • Slobodkin AI, Slobodkina GB, Panteleeva AN, Chernyh NA, Novikov AA, Bonch-Osmolovskaya EA (2016) Dissulfurimicrobium hydrothermale gen. nov., sp. nov., a thermophilic, auorophic, sulfur-disproporionating deltaproteobacterium isolated from a hydrothermal pond. Int J Syst Evol Microbiol 66:1022–1026

    Article  CAS  Google Scholar 

  • Slobodkina GB, Panteleeva AN, Sokolova TG, Bonch-Osmolovskaya EA, Slobodkin AI (2012) Carboxydocella manganica sp. nov., a thermophilic, dissimilatory Mn(IV)- and Fe(III)-reducing bacterium from a Kamchatka hot spring. Int J Syst Evol Microbiol 62:890–894

    Article  CAS  PubMed  Google Scholar 

  • Sokolova TG, Kostrikina NA, Chernyh NA, Tourova TP, Kolganova TV, Bonch-Osmolovskaya EA (2002) Carboxydocella thermoautotrophica gen. nov., sp. nov., a novel anaerobic CO-utilizing thermophile from a Kamchatkan hot spring. Int J Syst Evol Microbiol 52:1961–1967

    CAS  PubMed  Google Scholar 

  • Spear JR, Walker JJ, McCollom TM, Pace NR (2005) Hydrogen and bioenergetics in the Yellowstone geothermal ecosystem. Proc Natl Acad Sci USA 102:2555–2560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sunna A, Bergquist PL (2003) A gene encoding a novel extremely thermostable 1,4-beta-xylanase isolated directly from an environmental DNA sample. Extremophiles 7:63–70

    CAS  PubMed  Google Scholar 

  • Takacs-Vesbach C, Inskeep WP, Jay ZJ, Herrgard MJ, Rusch DB, Tringe SG, Kozubal MA, Hamamura N, Macur RE, Fouke BW, Reysenbach A-L, McDermott TR, Jennings RM, Hengartner NW, Xie G (2013) Metagenome sequence analysis of filamentous microbial communities obtained from geochemically distinct geothermal channels reveals specialization of three Aquificales lineages. Front Microbiol 4:84

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tan GL, Shu WS, Zhou WH, Li XL, Lan CY, Huang LN (2009) Seasonal and spatial variations in microbial community structure and diversity in the acid stream draining across an ongoing surface mining site. FEMS Microbiol Ecol 70:121–129

    Article  PubMed  Google Scholar 

  • Trüper HG, Schlegel HG (1964) Sulfur metabolism in Thiorodaceae. I. Quantitative measurements in growing cells of Chromatium okenii. Antonie van Leeuwenn hoek 30:225–238

    Article  Google Scholar 

  • Urbieta MS, González-Toril E, Bazán ÁA, Giaveno MA, Donati E (2015) Comparison of the microbial communities of hot springs waters and the microbial biofilms in the acidic geothermal area of Copahue (Neuquén, Argentina). Extremophiles 19:437–450

    Article  CAS  PubMed  Google Scholar 

  • Wagner ID, Varghese LB, Hemme CL, Wiegel J (2013) Multilocus sequence analysis of Thermoanaerobacter isolates reveals recombining, but differentiated, populations from geothermal springs of the Uzon Caldera, Kamchatka. Russia. Front Microbiol 4:169

    PubMed  Google Scholar 

  • Whitaker RJ, Grogan DW, Taylor JW (2003) Geographic barriers isolate endemic populations of hyperthermophilic archaea. Science 301:976–978

    Article  CAS  PubMed  Google Scholar 

  • Wolin EA, Wolin MJ, Wolfe RS (1963) Formation of methane by bacterial extracts. J Biol Chem 238:2882–2886

    CAS  PubMed  Google Scholar 

  • Wurch L, Giannone RG, Belisle BS, Swift C, Utturkar S, Hettich RL, Reysenbach AL, Podar M (2016) Genomics-informed isolation and characterization of a symbiotic Nanoarchaeota system from a terrestrial geothermal environment. Nat Commun 7:12115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoneda Y, Yoshida T, Kawaichi S, Daifuku T, Takabe K, Sako Y (2012) Carboxydothermus pertinax sp. nov., a thermophilic, hydrogenogenic, Fe(III)-reducing, sulfur-reducing Carboxydotrophic bacterium from an acidic hot spring. Int J Syst Evol Microbiol 62:1692–1697

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the grant of Russian Science Foundation #14-04-00165. We are grateful to the staff of Kronotsky Nature Reserve for their assistance in the organization of field studies in the Uzon Caldera. All authors have seen and approved the final version submitted. All local, national and international regulations and conventions as well as normal scientific ethical practices have been respected.

Author information

Authors and Affiliations

  1. Winogradsky Institute of Microbiology, Research Center of Biotechnology of the Russian Academy of Sciences, Leninsky Prospekt 33, Build. 2, Moscow, 119071, Russia

    Alexander Yu. Merkel, Nikolay V. Pimenov, Igor I. Rusanov, Alexander I. Slobodkin, Galina B. Slobodkina, Ivan Yu. Tarnovetckii, Evgeny N. Frolov, Arseny V. Dubin, Anna A. Perevalova & Elizaveta A. Bonch-Osmolovskaya

Authors
  1. Alexander Yu. Merkel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nikolay V. Pimenov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Igor I. Rusanov
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alexander I. Slobodkin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Galina B. Slobodkina
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ivan Yu. Tarnovetckii
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Evgeny N. Frolov
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Arseny V. Dubin
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Anna A. Perevalova
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Elizaveta A. Bonch-Osmolovskaya
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Elizaveta A. Bonch-Osmolovskaya.

Ethics declarations

Conflict of interest

We state no conflicts of interest.

Additional information

Communicated by A. Oren.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Merkel, A.Y., Pimenov, N.V., Rusanov, I.I. et al. Microbial diversity and autotrophic activity in Kamchatka hot springs. Extremophiles 21, 307–317 (2017). https://doi.org/10.1007/s00792-016-0903-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00792-016-0903-1

Keywords

Search

Navigation