Advertisement

Extremophiles

, Volume 21, Issue 2, pp 307–317 | Cite as

Microbial diversity and autotrophic activity in Kamchatka hot springs

  • 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
Original Paper

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.

Keywords

Terrestrial hot springs Lithoautotrophs Carbon assimilation Sulfur disproportionation Sulfurihydrogenibium Caldimicrobium Archaea 

Notes

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.

Conflict of interest

We state no conflicts of interest.

References

  1. Auchtung TA, Shyndriayeva G, Cavanaugh CM (2011) 16S rRNA phylogenetic analysis and quantification of Korarchaeota indigenous to the hot springs of Kamchatka, Russia. Extremophiles 15:105–116CrossRefPubMedGoogle Scholar
  2. Baker BJ, Banfield JF (2003) Microbial communities in acid mine drainage. FEMS Microbiol Ecol 44:139–152CrossRefPubMedGoogle Scholar
  3. Benson DA, Boguski MS, Lipman DJ, Ostell J, Ouellette BF, Rapp BA, Wheeler DL (1999) GenBank. Nucleic Acids Res 27:12–17CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bonch-Osmolovskaya EA (2004) Studies of thermophilic microorganisms at the Institute of Microbiology, Russian Academy of Sciences. Microbiology (English translation of Microbiologiia) 73:644–658Google Scholar
  5. 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) 56:812–818Google Scholar
  6. Bonch-Osmolovskaya EA, Sokolova TG, Kostrikina NA, Zavarzin GA (1990) Desulfurella acetivorans gen. nov., sp. nov., a new thermophilic sulfur-reducing bacterium. Arch Microbiol 153:151–155CrossRefGoogle Scholar
  7. 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) 68:398–406Google Scholar
  8. 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 63:471–489CrossRefPubMedGoogle Scholar
  9. Chao A (1984) Nonparametric estimation of the number of classes in a population. Scandinavian J Statistics 11:265–270Google Scholar
  10. 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 19:1157–1171CrossRefPubMedGoogle Scholar
  11. 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 56:39–63CrossRefGoogle Scholar
  12. 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):6CrossRefPubMedPubMedCentralGoogle Scholar
  13. 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) 85:471–480Google Scholar
  14. 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
  15. 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) 56:692–697Google Scholar
  16. 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) 80:244–251Google Scholar
  17. Hetzer A, Morgan HW, McDonald IR, Daughney CJ (2007) Microbial life in Champagne Pool, a geothermal spring in Waiotapu, New Zealand. Extremophiles 11:605–614CrossRefPubMedGoogle Scholar
  18. 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 25:551–554CrossRefPubMedGoogle Scholar
  19. Hugenholtz P, Pitulle C, Hershberger KL, Pace NR (1998) Novel division level bacterial diversity in a Yellowstone hot spring. J Bacteriol 180:366–376PubMedPubMedCentralGoogle Scholar
  20. 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 4:67PubMedPubMedCentralGoogle Scholar
  21. 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):34–43CrossRefPubMedGoogle Scholar
  22. 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 62:716–717CrossRefPubMedGoogle Scholar
  23. 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 15:319–325CrossRefPubMedGoogle Scholar
  24. 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 66:1828–1831CrossRefPubMedGoogle Scholar
  25. 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):e80835CrossRefPubMedPubMedCentralGoogle Scholar
  26. 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 16:476Google Scholar
  27. Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235CrossRefPubMedPubMedCentralGoogle Scholar
  28. 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 15:365–372CrossRefPubMedGoogle Scholar
  29. 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 70:411–424CrossRefPubMedGoogle Scholar
  30. 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) 84:577–583Google Scholar
  31. 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 48:475–479CrossRefPubMedGoogle Scholar
  32. 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 58:2935–2938CrossRefPubMedGoogle Scholar
  33. 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 59:1040–1044CrossRefPubMedGoogle Scholar
  34. Nakagawa T, Fukui M (2003) Molecular characterization of community structures and sulfur metabolism within microbial streamers in Japanese Hot Springs. Appl Environ Microbiol 69:7044–7057CrossRefPubMedPubMedCentralGoogle Scholar
  35. 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 58:1147–1152CrossRefPubMedGoogle Scholar
  36. 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 74:7620–7628CrossRefPubMedPubMedCentralGoogle Scholar
  37. 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 63:479–483CrossRefGoogle Scholar
  38. Prokofeva MI, Rusanov II, Pimenov NV (2006) Organotrophic activity in Kamchatka hot springs with low pH. Microbiology (English translation of Microbiologiia) 75:237–239Google Scholar
  39. 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–D596CrossRefPubMedGoogle Scholar
  40. 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 4:61–67PubMedGoogle Scholar
  41. 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):S12CrossRefGoogle Scholar
  42. 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 17:649–662CrossRefPubMedGoogle Scholar
  43. 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 62:2565–2571CrossRefPubMedGoogle Scholar
  44. 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 66:1022–1026CrossRefGoogle Scholar
  45. 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 62:890–894CrossRefPubMedGoogle Scholar
  46. 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 52:1961–1967PubMedGoogle Scholar
  47. Spear JR, Walker JJ, McCollom TM, Pace NR (2005) Hydrogen and bioenergetics in the Yellowstone geothermal ecosystem. Proc Natl Acad Sci USA 102:2555–2560CrossRefPubMedPubMedCentralGoogle Scholar
  48. Sunna A, Bergquist PL (2003) A gene encoding a novel extremely thermostable 1,4-beta-xylanase isolated directly from an environmental DNA sample. Extremophiles 7:63–70PubMedGoogle Scholar
  49. 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 4:84CrossRefPubMedPubMedCentralGoogle Scholar
  50. 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 70:121–129CrossRefPubMedGoogle Scholar
  51. Trüper HG, Schlegel HG (1964) Sulfur metabolism in Thiorodaceae. I. Quantitative measurements in growing cells of Chromatium okenii. Antonie van Leeuwenn hoek 30:225–238CrossRefGoogle Scholar
  52. 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 19:437–450CrossRefPubMedGoogle Scholar
  53. 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 4:169PubMedGoogle Scholar
  54. Whitaker RJ, Grogan DW, Taylor JW (2003) Geographic barriers isolate endemic populations of hyperthermophilic archaea. Science 301:976–978CrossRefPubMedGoogle Scholar
  55. Wolin EA, Wolin MJ, Wolfe RS (1963) Formation of methane by bacterial extracts. J Biol Chem 238:2882–2886PubMedGoogle Scholar
  56. 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 7:12115CrossRefPubMedPubMedCentralGoogle Scholar
  57. 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 62:1692–1697CrossRefPubMedGoogle Scholar

Copyright information

© Springer Japan 2016

Authors and Affiliations

  • Alexander Yu. Merkel
    • 1
  • Nikolay V. Pimenov
    • 1
  • Igor I. Rusanov
    • 1
  • Alexander I. Slobodkin
    • 1
  • Galina B. Slobodkina
    • 1
  • Ivan Yu. Tarnovetckii
    • 1
  • Evgeny N. Frolov
    • 1
  • Arseny V. Dubin
    • 1
  • Anna A. Perevalova
    • 1
  • Elizaveta A. Bonch-Osmolovskaya
    • 1
  1. 1.Winogradsky Institute of MicrobiologyResearch Center of Biotechnology of the Russian Academy of SciencesMoscowRussia

Personalised recommendations