Abstract
Arkashin Schurf (Arkashin) and Zavarzin Spring (Zavarzin), two active thermal pools in the Uzon Caldera, Kamchatka, Russia, were studied for geochemical and microbiological characterization. Arkashin, the smaller of the two pools, had broader temperature and pH ranges, and the sediments had higher concentrations of total As (4,250 mg/kg) relative to Zavarzin (48.9 mg/kg). Glycerol dialkyl glycerol tetraether profiles represented distinct archaeal communities in each pool and agreed well with previous studies of these pools. Although no archaeal 16S rRNA sequences were recovered from Arkashin, sequences recovered from Zavarzin were mostly representatives of the Crenarchaeota and “Korarchaeota,” and 13% of the sequences were unclassifiable. The bacterial community in Arkashin was dominated by uncultured “Bacteroidetes,” Hydrogenobaculum of the Aquificales and Variovorax of the Betaproteobacteria, and 19% of the sequences remained unclassified. These results were consistent with other studies of As-rich features. The most abundant members of the Zavarzin bacterial community included the Chloroflexi, as well as members of the classes Deltaproteobacteria and Clostridia. In addition, 24% of the sequences were unclassified and at least 5% of those represent new groups among the established Bacterial phyla. Ecological structure in each pool was inferred from taxonomic classifications and bulk stable isotope δ values of C, N, and S. Hydrogenobaculum was responsible for primary production in Arkashin. However, in Zavarzin, the carbon source appeared to be allochthonous to the identified bacterial community members. Additionally, sequences related to organisms expected to participate in N and S cycles were identified from both pools.
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References
Barns SM, Fundyga RE, Jefferies MW, Pace NR (1994) Remarkable archaeal diversity detected in a Yellowstone National Park hot spring environment. Proc Natl Acad Sci 91:1609–1613
Belousov VI, Grib EN, Leonov VL (1984) The geological setting of the hydrothermal systems in the Geysers valley and Uzon caldera. Volc Seis 5:67–81
Blank CE, Cady SL, Pace NR (2002) Microbial composition of near-boiling silica-depositing thermal springs throughout Yellowstone National Park. Appl Environ Microbiol 68:5123–5135
Bonch-Osmolovskaya EA (1994) Bacterial sulfur reduction in hot vents. FEMS Microbiol Rev 15:54–77
Bonch-Osmolovskaya EA (2004) Studies of thermophilic microorganisms at the Institute of Microbiology, Russian Academy of Sciences. Microbiology 73:551–564
Cann IKO, Stroot PG, Mackie KR, White BA, Mackie RI (2001) Characterization of two novel saccharolytic, anaerobic thermophiles, Thermoanaerobacterium polysaccharolyticum sp. nov. and Thermoanaerobacterium zeae sp. nov., and emendation of the genus Thermoanaerobacterium. Int J Syst Evol Microbiol 51:293–302
Cleverley JS, Benning LG, Mountain BW (2003) Reaction path modelling in the As-S system: a case study for geothermal As transport. Appl Geochem 18:1325–1345
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
Colwell RK (2006) Estimate S: statistical estimation of species richness and shared species from samples. University of Connecticut, Storrs, Department of Ecology and Evolutionary Biology
Connon SA, Koski AK, Neal AL, Wood SA, Magnuson TS (2008) Ecophysiology and geochemistry of microbial arsenic oxidation within a high arsenic, circumneutral hot spring system of the Alvord Desert. FEMS Microbiol Ecol 64:117–128
DeLong EF (1992) Archaea in coastal marine environments. Proc Natl Acad Sci, USA 89:5685–5689
Des Marais DJ (1996) Stable light isotope biogeochemistry of hydrothermal systems. In: Bock GR, Goode JA (eds) Evolution of hydrothermal ecosystems on Earth (and Mars?), vol. 202. Wiley, Chichester, pp 83–98
DeSantis TZ, Hugenholtz P, Keller K, Brodie EL, Larsen N, Piceno YM, Phan R, Andersen GL (2006) NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes. Nucleic Acids Res 34:W392–W399
Donahoe-Christiansen J, D'Imperio S, Jackson CR, Inskeep WP, McDermott TR (2004) Arsenite-oxidizing Hydrogenobaculum strain isolated from an acid-sulfate-chloride geothermal spring in Yellowstone National Park. Appl Environ Microbiol 70:1865–1868
EPA (1996) Method 3052: microwave assisted acid digestion of siliceous and organically based matrices. EPA, USA
Estep MLF (1984) Carbon and hydrogen isotopic compositions of algae and bacteria from hydrothermal environments, Yellowstone National Park. Geochim Cosmochim Acta 48:591–599
Estep MLF, Macko SA (1984) Nitrogen isotope biogeochemistry of thermal springs. Org Geochem 6:779–785
Euzeby JP (1997) List of bacterial names with standing in nomenclature: a folder available on the internet. Int J Syst Evol Microbiol 47:590–592
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Fouke BW, Bonheyo GT, Sanzenbacher B, Frias-Lopez J (2003) Partitioning of bacterial communities between travertine depositional faces at Mammoth Hot Springs, Yellowstone National Park, U.S.A. Can J Earth Sci 40:1531–1548
Habicht KS, Canfield DE (2001) The effect of sulfate concentration on the sulfur isotope fractionation during sulfate reduction by sulfate-reducing bacteria. Lunar and Planetary Institute, Houston
Hamamura N, Macur RE, Korf S, Ackerman G, Taylor WP, Kozubal M, Reysenbach A-L, Inskeep WP (2009) Linking microbial oxidation of arsenic with detection and phylogenetic analysis of arsenite oxidase genes in diverse geothermal environments. Environ Microbiol 11:421–431
Hanada S, Takaichi S, Matsuura K, Nakamura K (2002) Roseiflexus castenholzii gen. nov., sp. nov., a thermophilic, filamentous, photosynthetic bacterium that lacks chlorosomes. Int J Syst Evol Microbiol 52:187–193
Hayes JM (2001) Fractionation of carbon and hydrogen isotopes in biosynthetic processes. Rev Mineral Geochem 43:225–278
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
Hollingsworth ER (2006) Elemental and isotopic chemistry of the Uzon Caldera, M.S. thesis, University of Georgia
House CH, Schopf JW, Stetter KO (2003) Carbon isotopic fractionation by Archaeans and other thermophilic prokaryotes. Org Geochem 34:345–356
Huber T, Faulkner G, Hugenholtz P (2004) Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20:2317–2319
Hugenholtz P, Pitulle C, Hershberger KL, Pace NR (1998) Novel division level bacterial diversity in a Yellowstone hot spring. J Bacteriol 180:366–376
Iino T, Nakagawa T, Mori K, Harayama S, Suzuki K (2008) Calditerrivibrio nitroreducens gen. nov., sp. nov., a thermophilic, nitrate-reducing bacterium isolated from a terrestrial hot spring in Japan. Int J Syst Evol Microbiol 58:1675–1679
Jackson CR, Langner HW, Donahoe-Christiansen J, Inskeep WP, McDermott TR (2001) Molecular analysis of microbial community structure in an arsenite-oxidizing acidic thermal spring. Environ Microbiol 3:532–542
Jahnke LL, Eder W, Huber R, Hope JM, Hinrichs K-U, Hayes JM, Des Marais DJ, Cady SL, Summons RE (2001) Signature lipids and stable carbon isotope analysis of Octopus Spring hyperthermophilic communities compared with those of Aquificales representatives. Appl Environ Microbiol 67:5179–5189
Karpov GA (1992) Subsurface hydrothermal genesis of ores and minerals in recent hydrothermal system of Uzon caldera in Kamchatka, Russia. In: Kharaka Maest (ed) Water–rock interaction. Balkema, Rotterdam, pp 1593–1596
Karpov GA (1998) Uzon, a protected land. Logata, Kamchatprombank, Petropavlovsk-Kamchatskiy
Karpov GA, Naboko SI (1990) Metal contents of recent thermal waters, mineral precipitates and hydrothermal alteration in active geothermal fields, Kamchatka. J Geochem Explor 36:57–71
Katayama Y, Uxhino Y, Wood AP, Kelly DP (2006) Confirmation of Thiomonas delicata (formerly Thiobacillus delicatus) as a distinct species of the genus Thiomonas Moreira and Amils 1997 with comments on some species currently assigned to the genus. Int J Syst Evol Microbiol 56:2553–2557
Kublanov IV, Bidjieva SK, Mardanov AV, Bonch-Osmolovskaya EA (2009) Desulfurococcus kamchatkensis sp. nov., a novel hyperthermophilic protein-degrading archaeon isolated from a Kamchatka hot spring. Int J Syst Evol Microbiol 59:1743–1747
Kublanov IV, Perevalova AA, Slobodkina GB, Lebedinsky AV, Bidzhieva SK, Kolganova TV, Kaliberda EN, Rumsh LD, Haertle T, Bonch-Osmolovskaya EA (2009) Biodiversity of thermophilic prokaryotes with hydrolytic activities in hot springs of Uzon Caldera, Kamchatka (Russia). Appl Environ Microbiol 75:286–291
Kvist T, Ahring BK, Westermann AP (2007) Archaeal diversity in Icelandic hot springs. FEMS Microbiol Ecol 59:71–80
Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175
Lee Y-E, Jain MK, Lee C, Lowe SE, Zeikus JG (1993) Taxonomic distinction of saccharolytic thermophilic anaerobes: description of Thermoanaerobacterium xylanolyticum gen. nov., sp. nov., and Thermoanaerobacterium saccharolyticum gen. nov., sp. nov.; reclassification of Thermoanaerobium brockii, Clostridium thermosulfrogenes, and Clostridium thermohydrosulfuricum E100-69 as Thermanaerobacter brockii com. nov., Thermoanaerbacterium thermosulfurigenes comb. nov., and Thermoanaerobacter thermohydrosulfuricus comb. nov., respectively; and transfer of Clostridium thermohydrosulfuricum 39E to Thermoanaerobacter ethanolicus. Int J Syst Bacteriol 43:41–51
Li Y, Kawamura Y, Fujiwara N, Naka T, Liu H, Huang X, Kobayashi K, Ezaki T (2004) Sphingomonas yabuuchaie sp. nov. and Brevundimonas nasdae sp. nov., isolated from the Russian space laboratory Mir. Int J Syst Evol Microbiol 54:819–825
Macur RE, Langner HW, Kocar BD, Inskeep WP (2004) Linking geochemical processes with microbial community analysis: successional dynamics in an arsenic-rich, acid-sulfate-chloride geothermal spring. Geobiology 2:163–177
Mathur J, Bizzoco RW, Ellis DG, Lipson DA, Poole AW, Levine R, Kelley ST (2007) Effects of abiotic factors on the phylogenetic diversity of bacterial communities in acidic thermal springs. Appl Environ Microbiol 73:2612–2623
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
Migdisov AA, Bychkov AY (1998) The behaviour of metals and sulphur during the formation of hydrothermal mercury-antimony-arsenic mineralization, Uzon caldera, Kamchatka, Russia. J Volcanol Geotherm Res 84:153–171
Miller WP, Miller DM (1987) A micro-pipette method for soil mechanical analysis. Commun Soil Sci Plant Anal 18:1–15
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, Kostrikina NA, Hippe H, Slobodkin AI, Bonch-Osmolovskaya EA (1998) Biodiversity of thermophilic sulfur-reducing bacteria: new substrates and new habitats. Microbiology 67:563–568
Miroshnichenko ML, Rainey FA, Hippe H, Chernyh NA, Kostrikina NA, Bonch-Osmolovskaya EA (1998) Desulfurella kamchatkensis sp. nov. and Desulfurella propionica sp. nov., new sulfur-respiring thermophilic bacteria from Kamchatka thermal environments. Int J Syst Bacteriol 48:475–479
Mori K, Kim H, Kakegawa T, Hanada S (2003) A novel lineage of sulfate-reducing microorganisms: Thermodesulfobiaceae fam. nov., Thermodesulfobium narugense, gen. nov., sp. nov., a new thermophilic isolate from a hot spring. Extremophiles 7:283–290
Mori K, Yamaguchi K, Sakiyama Y, Urabe T, Suzuki K-i (2009) Caldisericum exile gen. nov., sp. nov., an anaerobic, thermophilic, filamentous bacterium of a novel bacterial phylum, Caldiserica phyl. nov., originally called the candidate phylum OP5, and description of Caldisericaceae fam. nov., Caldisericales or. nov. and Caldisericia classis nov. Int J Syst Evol Microbiol 59:2894–2898
O'Neill AH, Liu Y, Ferrera I, Beveridge TJ, Reysenbach A-L (2008) Sulfurihydrogenibium rodmanii sp. nov., a sulfur-oxidizing chemolithoautotroph from the Uzon Caldera, Kamchakta Peninsula, Russia, and emended description of the genus Sulfurihydrogenibium. Int J Syst Evol Microbiol 58:1147–1152
Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York
Park S-J, Park B-J, Rhee S-K (2008) Comparative analysis of archaeal 16S rRNA and amoA genes to estimate the abundance and diversity of ammonia-oxidizing archaea in marine sediments. Extremophiles 12:605–615
Patel BKC (2011) Phylum XX. Dictyoglomi phyl. nov. In: Krieg NR, Staley JT, Brown DR, Hedlund BP, Paster BJ, Ward NL, Ludwig W, Whitman WB (eds) Bergey’s manual of systemic bacteriology, vol. 4. Springer, New York, pp 775–780
Pearson A, Pi Y, Zhao W, Li W, Li Y, Inskeep WP, Perevalova A, Romanek CS, Li S, Zhang CL (2008) Factors controlling the distribution of archaeal tetraethers in terrestrial hot springs. Appl Environ Microbiol 74:3523–3532
Perevalova AA, Kolganova TV, Birkeland N-K, 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
Reed MH, Palandri J (2006) Sulfide mineral precipitation from hydrothermal fluids. Rev Mineral Geochem 61:609–631
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
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
Ryba SA, Burgess RM (2002) Effects of sample preparation on the measurement of organic carbon, hydrogen, nitrogen, sulfur, and oxygen concentrations in marine sediments. Chemosphere 48:139–147
Saiki T, Kobayashi Y, Kawagoe K, Beppu T (1985) Dictyoglomus thermophilum gen. nov., sp. nov., a chemoorganotrophic, anaerobic, thermophilic bacterium. Int J Syst Bacteriol 35:253–259
Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1506
Schouten S, van der Meer MTJ, Hopmans EC, Rijpstra WIC, Reysenbach A, Ward DM, Dameste JSS (2007) Archaeal and bacterial glycerol dialkyl glycerol tetraether lipids in hot springs of Yellowstone National Park. Appl Environ Microbiol 73:6181–6191
Singleton DR, Furlong MA, Rathbun SL, Whitman WB (2001) Quantitative comparisons of 16S rRNA gene sequence libraries from environmental samples. Appl Environ Microbiol 67:4374–4376
Skirnisdottir S, Hreggvidsson GO, Hjorleifsdottir S, Marteinsson V, Petursdottir S, Holst O, Kristjansson JK (2000) Influence of sulfide and temperature on species composition and community structure of hot spring microbial mats. Appl Environ Microbiol 66:2835–2841
Spear JR, Walker JJ, McCollom TM, Pace NR (2005) Hydrogen and bioenergetics in the Yellowstone geothermal ecosystem. Proc Natl Acad Sci 102:2555–2560
Stohr R, Waberski A, Volker H, Tindall BJ, Thomm M (2001) Hydrogenothermus marinus gen. nov., sp. nov., a novel thermophilic hydrogen-oxidizing bacterium, recognition of Calderobacterium hydrogenophilum as a member of the genus Hydrogenobacter and proposal of the reclassification of Hydrogenobacter acidophilus as Hydrogenobaculum acidophilum gen. nov., comb. nov., in the phylum Hydrogenobacter/Aquifex. Int J Syst Evol Microbiol 51:1853–1862
Summons RE, Jahnke LL, Simoneit BRT (1996) Lipid biomarkers for bacterial ecosystems: studies of cultured organisms, hydrothermal environments and ancient sediments. In: Bock GR, Goode JA (eds) Evolution of hydrothermal ecosystems on Earth (and Mars?), vol. 202. Wiley, Chichester, pp 174–194
Takai K, Kobayashi H, Nealson KH, Horikoshi K (2003) Sulfurihydrogenibium subterraneum gen. nov., sp. nov., from a subsurface hot aquifer. Int J Syst Evol Microbiol 53:823–827
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Ueda A, Krouse HR (1986) Direct conversion of sulphide and sulphate minerals to SO2 for isotope analysis. Geochem J 20:209–212
Vesteinsdottir H, Reynisdottir DB, Orlygsson J (2011) Thimonas islandica sp. nov., a moderately thermophilic, hydrogen- and sulfur-oxidizing betaproteobacterium isolated from a hot spring. Int J Syst Evol Microbiol 61:132–137
Wagner ID, Zhao W, Zhang CL, Romanek CS, Rohde M, Wiegel J (2008) Thermoanaerobacter uzonensis sp. nov., an anaerobic thermophilic bacterium isolated from a hot spring within the Uzon Caldera, Kamchatka, Far East Russia. Int J Syst Evol Microbiol 58:2565–2573
White DC, Ringelberg DB (1998) Signature lipid biomarker analysis. In: Burlage RS, Atlas RM, Stahl DA, Geesey GG, Sayler G (eds) Techniques in microbial ecology. Oxford University Press, New York, pp 255–272
Willems A, De Ley J, Gillis M, Kersters K (1991) Comamonadaceae, a new family encompassing the Acidovorans rRNA complex, including Variovorax paradoxus gen. nov., comb. nov., for Alcaligenes paradoxus (Davis 1969). Int J Syst Bacteriol 41:445–450
Zhang CL, Fouke BW, Bonheyo GT, Peacock A, White DC, Huang Y, Romanek CS (2004) Lipid biomarkers and carbon-isotopes of modern travertine deposits (Yellowstone National Park, USA): implications for biogeochemical dynamics in hot-spring systems. Geochim Cosmochim Acta 68:3157–3169
Zhao W (2008) Diversity and potential geochemical functions of prokaryotes in hot springs of the Uzon Caldera, Kamchatka, Ph.D. dissertation, University of Georgia
Acknowledgments
Assistance was provided by C. Hagen for clone library construction, N. Etheridge for PLFA analysis and draft editing, A. Pearson for GDGT analysis, T. Maddox for stable isotope ratio analysis, and H. McLeod for draft editing. Thank you also to members of the Kamchatka MO field expeditions and administrators of the Kronotsky National Park. This manuscript was improved through feedback from anonymous reviewers. Research funding sources included the National Science Foundation (MCB-MO 0238407), the US Civilian Research and Development Foundation, and the Savannah River Ecology Laboratory through the US Department of Energy and the University of Georgia (DE-FC09-07SR22506).
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Burgess, E.A., Unrine, J.M., Mills, G.L. et al. Comparative Geochemical and Microbiological Characterization of Two Thermal Pools in the Uzon Caldera, Kamchatka, Russia. Microb Ecol 63, 471–489 (2012). https://doi.org/10.1007/s00248-011-9979-4
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DOI: https://doi.org/10.1007/s00248-011-9979-4