Skip to main content
Log in

Microbiology and geochemistry of great boiling and mud hot springs in the United States Great Basin

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

Abstract

A coordinated study of water chemistry, sediment mineralogy, and sediment microbial community was conducted on four >73°C springs in the northwestern Great Basin. Despite generally similar chemistry and mineralogy, springs with short residence time (~5–20 min) were rich in reduced chemistry, whereas springs with long residence time (>1 day) accumulated oxygen and oxidized nitrogen species. The presence of oxygen suggested that aerobic metabolisms prevail in the water and surface sediment. However, Gibbs free energy calculations using empirical chemistry data suggested that several inorganic electron donors were similarly favorable. Analysis of 298 bacterial 16S rDNAs identified 36 species-level phylotypes, 14 of which failed to affiliate with cultivated phyla. Highly represented phylotypes included Thermus, Thermotoga, a member of candidate phylum OP1, and two deeply branching Chloroflexi. The 276 archaeal 16S rDNAs represented 28 phylotypes, most of which were Crenarchaeota unrelated to the Thermoprotei. The most abundant archaeal phylotype was closely related to “Candidatus Nitrosocaldus yellowstonii”, suggesting a role for ammonia oxidation in primary production; however, few other phylotypes could be linked with energy calculations because phylotypes were either related to chemoorganotrophs or were unrelated to known organisms.

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

Access this article

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
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Amend JP, Shock EL (2001) Energetics of overall metabolic reactions of thermophilic and hyperthermophilic Archaea and Bacteria. FEMS Microbiol Rev 25:175–243

    Article  PubMed  CAS  Google Scholar 

  • Anderson JP (1978) A geochemical study of the southwest part of the Black Rock Desert and its geothermal areas; Washoe, Pershing, and Humboldt Counties, Nevada. Colo Sch Mines Q 73:15–22

    CAS  Google Scholar 

  • Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ, Weightman AJ (2005) At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies. Appl Environ Microbiol 71:7724–7736

    Article  PubMed  CAS  Google Scholar 

  • Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ, Weightman AJ (2006) New screening software shows that most recent large 16S rRNA gene clone libraries contain chimeras. Appl Environ Microbiol 72:5734–5741

    Article  PubMed  CAS  Google Scholar 

  • Balkwill DL, Kieft TL, Tsukuda T, Kostandarithes HM, Onstott TC, Macnaughton S, Bownas J, Fredrickson JK (2004) Identification of iron-reducing Thermus strains as Thermus scotoductus. Extremophiles 8:37–44

    Article  PubMed  CAS  Google Scholar 

  • Bazylinski DA, Garratt-Reed AJ, Frankel RB (1994) Electron microscopic studies of magnetosomes in magnetotactic bacteria. Microsc Res Tech 27:389–401

    Article  PubMed  CAS  Google Scholar 

  • Bjornsdottir SH, Blondal T, Hreggvidsson GO, Eggertsson G, Petursdottir S, Hjorleifsdottir S, Thorbjarnardottir SH, Kristjansson JK (2006) Rhodothermus marinus: physiology and molecular biology. Extremophiles 10:1–16

    Article  PubMed  CAS  Google Scholar 

  • Breitbart M, Wegley L, Leeds S, Schoenfeld T, Rohwer F (2004) Phage community dynamics in hot springs. Appl Environ Microbiol 70:1633–1640

    Article  PubMed  CAS  Google Scholar 

  • Brosius J, Palmer ML, Kennedy PJ, Noller HF (1978) Complete nucleotide sequence of a 16S ribosomal RNA gene from Escherichia coli. Proc Natl Acad Sci USA 75:4801–4805

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • D’Imperio S, Lehr CR, Oduro H, Druschel G, Kuhl M, McDermott TR (2008) The relative importance of H2 and H2S as energy sources for primary production in geothermal springs. Appl Environ Microbiol 74:5802–5808

    Article  PubMed  CAS  Google Scholar 

  • de la Torre JR, Walker CB, Ingallis AE, Konneke M, Stahl DA (2008) Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ Microbiol 10:810–818

    Article  CAS  Google Scholar 

  • Dojka MA, Hugenholtz P, Haack SK, Pace NR (1998) Microbial diversity in a hydrocarbon- and chlorinated-solvent-contaminated aquifer undergoing intrinsic bioremediation. Appl Environ Microbiol 64:3869–3877

    PubMed  CAS  Google Scholar 

  • Dunbar J, Takala S, Barns SM, Davis JA, Kuske CR (1999) Levels of bacterial community diversity in four arid soils compared by cultivation and 16S rRNA gene cloning. Appl Environ Microbiol 65:1662–1669

    PubMed  CAS  Google Scholar 

  • Eder W, Huber R (2002) New isolates and physiological properties of the Aquificales and description of Thermocrinis albus sp. nov. Extremophiles 6:309–318

    Article  PubMed  Google Scholar 

  • Eder W, Ludwig W, Huber R (1999) Novel 16S rRNA gene sequences retrieved from highly saline brine sediments of Kebrit Deep, Red Sea. Arch Microbiol 172:213–218

    Article  PubMed  CAS  Google Scholar 

  • Eder W, Jahnke LL, Schmidt M, Huber R (2001) Microbial diversity of the brine-seawater interface of the Kebrit Deep, Red Sea, studied via 16S rRNA gene sequences and cultivation methods. Appl Environ Microbiol 67:3077–3085

    Article  PubMed  CAS  Google Scholar 

  • Faulds JE, Coolbaugh MF, Vice GS, Edwards ML (2006) Characterizing structural controls on geothermal fields in the northwestern Great Basin: a progress report. GRC Trans 30:69–76

    Google Scholar 

  • Fournier RO (2005) Geochemistry and dynamics of the Yellowstone National Park Hydrothermal System. In: Inskeep WP, McDemott TR (eds) Geothermal biology and geochemistry in Yellowstone National Park. Montana State University Publications, Bozeman

    Google Scholar 

  • Hall JR, Mitchell KR, Jackson-Weaver O, Kooser AS, Cron BR, Crossey LJ, Takacs-Vesbach CD (2008) Molecular characterization of the diversity and distribution of a thermal spring microbial community using rRNA and metabolic genes. Appl Environ Microbiol 74:4910–4922

    Article  PubMed  CAS  Google Scholar 

  • Huang Z, Hedlund BP, Wiegel J, Zhou J, Zhang CL (2007) Molecular phylogeny of uncultivated Crenarchaeota in Great Basin hot springs of moderately elevated temperature. Geomicrobiol J 24:535–542

    CAS  Google Scholar 

  • Huber H, Stetter KO (2006) Desulfurococcales. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes. Springer, New York

    Google Scholar 

  • Huber R, Burggraf S, Mayer T, Barns SM, Rossnagel P, Stetter KO (1995) Isolation of a hyperthermophilic archaeum predicted by in situ RNA analysis. Nature 376:57–58

    Article  PubMed  CAS  Google Scholar 

  • Huber R, Eder W, Heldwein S, Wanner G, Huber H, Rachel R, Stetter KO (1998) Thermocrinis ruber gen. nov., sp. nov., a pink-filament-forming hyperthermophililc bacterium isolated from Yellowstone National Park. Appl Environ Microbiol 64:3576–3583

    PubMed  CAS  Google Scholar 

  • Huber R, Huber H, Stetter KO (2000) Towards the ecology of hyperthermophiles: biotopes, new isolation strategies and novel metabolic properties. FEMS Microbiol Rev 24:615–623

    Article  PubMed  CAS  Google Scholar 

  • Huber T, Faulkner G, Hugenholtz P (2004) Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20:2317–2319

    Article  PubMed  CAS  Google Scholar 

  • Huber H, Huber R, Stetter KO (2006) Thermoproteales. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes. Springer, New York, pp 10–22

    Chapter  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

    PubMed  CAS  Google Scholar 

  • Inskeep WP, Ackerman GG, Taylor WP, Kozubal M, Korf S, Macur RE (2005) On the energetics of chemolithotrophy in nonequilibrium systems: case studies of geothermal springs in Yellowstone National Park. Geobiology 3:297–313

    Article  CAS  Google Scholar 

  • Jackson BE, McInerney MJ (2002) Anaerobic microbial metabolism can proceed close to thermodynamic limits. Nature 415:454–456

    Article  PubMed  CAS  Google Scholar 

  • Jeanthon C, L’Haridon S, Cueff V, Banta A, Reysenbach AL, Prieur D (2002) Thermodesulfobacterium hydrogeniphilum sp. nov., a thermophilic, chemolithoautotrophic, sulfate-reducing bacterium isolated from a deep-sea hydrothermal vent at Guaymas Basin, and emendation of the genus Thermodesulfobacterium. Int J Syst Evol Microbiol 52:765–772

    Article  PubMed  CAS  Google Scholar 

  • Johnson JW, Oelkers EH, Helgeson HC (1992) SUPCRT92: a software package for calculating the standard molal thermodynamic properties of minerals, gases, aqueous species, and reactions from 1 to 5,000 bar and 0 to 1,000° C. Comput Geosci 18:899–947

    Article  Google Scholar 

  • Kashefi K, Holmes DE, Reysenbach AL, Lovley DR (2002) Use of Fe(III) as an electron acceptor to recover previously uncultured hyperthermophiles: isolation and characterization of Geothermobacterium ferrireducens gen. nov., sp. nov. Appl Environ Microbiol 68:1735–1742

    Article  PubMed  CAS  Google Scholar 

  • Kashefi K, Shelobolina ES, Elliott WC, Lovley DR (2008) Growth of thermophilic and hyperthermophilic Fe(III)-reducing microorganisms on a ferruginous smectite as the sole electron acceptor. Appl Environ Microbiol 74:251–258

    Article  PubMed  CAS  Google Scholar 

  • Lee MH, Keams JL, Helzer DW, Leiser OP, Ochoa MA, Connon SA, Magnuson TS, Watwood ME (2007) Evaluation of viral and prokaryotic community dynamics in Alvord Desert hot springs, Oregon, USA. Aquatic Microb Ecol 48:19–26

    Article  Google Scholar 

  • Ley RE, Harris JK, Wilcox J, Spear JR, Miller SR, Bebout BM, Maresca JA, Bryant DA, Sogin ML, Pace NR (2006) Unexpected diversity and complexity of the Guerrero Negro hypersaline microbial mat. Appl Environ Microbiol 72:3685–3695

    Article  PubMed  CAS  Google Scholar 

  • Liao PC, Huang BH, Huang S (2007) Microbial community composition of the Danshui River estuary of Northern Taiwan and the practicality of the phylogenetic method in microbial barcoding. Microb Ecol 54:497–507

    Article  PubMed  Google Scholar 

  • Lozupone C, Hamady M, Knight R (2006) UniFrac—an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics 7:371

    Article  PubMed  CAS  Google Scholar 

  • Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar, Buchner A, Lai T, Steppi S, Jobb G, Forster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, Konig A, Liss T, Lussmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer KH (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371

    Article  PubMed  CAS  Google Scholar 

  • Morris DD, Gibbs MD, Chin CW, Koh MH, Wong KK, Allison RW, Nelson PJ, Bergquist PL (1998) Cloning of the xynB gene from Dictyoglomus thermophilum Rt46B.1 and action of the gene product on kraft pulp. Appl Environ Microbiol 64:1759–1765

    PubMed  CAS  Google Scholar 

  • Niederberger TD, Gotz DK, McDonald IR, Ronimus RS, Morgan HW (2006) Ignisphaera aggregans gen. nov., sp. nov., a novel hyperthermophilic crenarchaeote isolated from hot springs in Rotorua and Tokaanu, New Zealand. Int J Syst Evol Microbiol 56:965–971

    Article  PubMed  CAS  Google Scholar 

  • Pearson A, Huang Z, Ingalls AE, Romanek CS, Wiegel J, Freeman KH, Smittenberg RH, Zhang CL (2004) Nonmarine crenarchaeol in Nevada hot springs. Appl Environ Microbiol 70:5229–5237

    Article  PubMed  CAS  Google Scholar 

  • Pearson A, Pi Y, Zhao W, Li W, Li Y, Inskeep W, Perevalova A, Romanek C, Li S, Zhang CL (2008) Factors controlling the distribution of archaeal tetraethers in terrestrial hot springs. Appl Environ Microbiol 74:3523–3532

    Article  PubMed  CAS  Google Scholar 

  • Perry JJ (2006) The genus Thermomicrobium. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The prokaryotes. Springer, New York, pp 849–853

    Chapter  Google Scholar 

  • Ramirez-Arcos S, Fernandez-Herrero LA, Berenguer J (1998) A thermophilic nitrate reductase is responsible for the strain specific anaerobic growth of Thermus thermophilus HB8. Biochim Biophys Acta 1396:215–227

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Reysenbach A-L (2001) Class I. Thermoprotei class. nov. In: Boone DR, Castenholz RW (eds) Bergey’s manual of systematic bacteriology. Springer, New York

    Google Scholar 

  • Reysenbach AL, Giver LJ, Wickham GS, Pace NR (1992) Differential amplification of rRNA genes by polymerase chain reaction. Appl Environ Microbiol 58:3417–3418

    PubMed  CAS  Google Scholar 

  • Reysenbach AL, Wickham GS, Pace NR (1994) Phylogenetic analysis of the hyperthermophilic pink filament community in Octopus Spring, Yellowstone National Park. Appl Environ Microbiol 60:2113–2119

    PubMed  CAS  Google Scholar 

  • Reysenbach AL, Liu Y, Banta AB, Beveridge TJ, Kirshtein JD, Schouten S, Tivey MK, Von Damm KL, Voytek MA (2006) A ubiquitous thermoacidophilic archaeon from deep-sea hydrothermal vents. Nature 442:444–447

    Article  PubMed  CAS  Google Scholar 

  • Rice P, Longden I, Bleasby A (2000) EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16:276–277

    Article  PubMed  CAS  Google Scholar 

  • Schink B (1997) Energetics of syntrophic cooperation in methanogenic degradation. Microbiol Mol Biol Rev 61:262–280

    PubMed  CAS  Google Scholar 

  • Schink B (2002) Synergistic interactions in the microbial world. Antonie Van Leeuwenhoek 81:257–261

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Schouten S, Hopmans EC, Baas M, Boumann H, Standfest S, Konneke M, Stahl DA, Sinninghe Damste JS (2008) Intact membrane lipids of “Candidatus Nitrosopumilus maritimus”, a cultivated representative of the cosmopolitan mesophilic group I Crenarchaeota. Appl Environ Microbiol 74:2433–2440

    Article  PubMed  CAS  Google Scholar 

  • Shock E, Holland M, Meyer-Dombard DR, Amend JP (2005) Geochemical sources of energy for microbial metabolism in hydrothermal ecosystems: Obsidian Pool, Yellowstone National Park. In: Inskeep WP, McDermott TR (eds) Geothermal biology and geochemistry in Yellowstone National Park. Montana State University Publications, Bozeman, pp 95–109

    Google Scholar 

  • Singleton DR, Furlong MA, Rathburn SL, Whitman WB (2001) Quantitative comparisons of 16S rDNA sequence libraries from environmental samples. Appl Environ Microbiol 67:4373–4376

    Article  Google Scholar 

  • Skirnisdottir S, Hreggvidsson GO, Holst O, Kristjansson JK (2001) Isolation and characterization of a mixotrophic sulfur-oxidizing Thermus scotoductus. Extremophiles 5:45–51

    Article  PubMed  CAS  Google Scholar 

  • Sloan WT, Woodcock S, Lunn M, Head IM, Curtis TP (2007) Modeling taxa-abundance distributions in microbial communities using environmental sequence data. Microb Ecol 53:443–455

    Article  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  PubMed  CAS  Google Scholar 

  • Stetter KO (1988) Archaeoglobus fulgidus gen. nov., sp. nov. a new taxon of extremely thermophilic Archaebacteria. Syst Appl Microbiol 10:172–173

    Google Scholar 

  • Stott MB, Crowe MA, Mountain BW, Smirnova AV, Hou S, Alam M, Dunfield PF (2008) Isolation of novel bacteria, including a candidate division, from geothermal soils in New Zealand. Environ Microbiol 10:2030–2041

    Article  PubMed  CAS  Google Scholar 

  • Takai K, Sako Y (1999) A molecular view of archaeal diversity in marine and terrestrial hot water environments. FEMS Microbiol Ecol 28:177–188

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Tarlera S, Muxi L, Soubes M, Stams AJ (1997) Caloramator proteoclasticus sp. nov., a new moderately thermophilic anaerobic proteolytic bacterium. Int J Syst Bacteriol 47:651–656

    Article  PubMed  CAS  Google Scholar 

  • Theisen AA, Harward ME (1962) A paste method for preparation of slides for clay mineral identification by X-ray diffraction. Soil Sci Soc Am Proc 26:90–91

    CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Vanfossen AL, Lewis DL, Nichols JD, Kelly RM (2008) Polysaccharide degradation and synthesis by extremely thermophilic anaerobes. Ann NY Acad Sci 1125:322–337

    Article  PubMed  CAS  Google Scholar 

  • von Wintzingerode F, Gobel UB, Stackebrandt E (1997) Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. FEMS Microbiol Rev 21:213–229

    Article  Google Scholar 

  • Wolery TJ (1992) EQ3/6: software package for geochemical modeling of aqueous systems: package overview and installation guide (version 7.0). Lawrence Livermore National Laboratory Report UCRL-MA-110662 PT I, Livermore, CA

  • Wu T, Chellemi DO, Graham JH, Martin KJ, Rosskopf EN (2008) Comparison of soil bacterial communities under diverse agricultural land management and crop production practices. Microb Ecol 55:293–310

    Article  PubMed  Google Scholar 

  • Zehner RE, Coolbaugh MF, Shevenell L (2006) Regional groundwater geochemical trends in the Great Basin: implications for geothermal exploration. Geotherm Resour Counc Trans 30:117–124

    CAS  Google Scholar 

  • Zhang CL, Pearson A, Li YL, Mills G, Wiegel J (2006a) Thermophilic temperature optimum for crenarchaeol synthesis and its implication for archaeal evolution. Appl Environ Microbiol 72:4419–4422

    Article  PubMed  CAS  Google Scholar 

  • Zhang R, Jiang J, Gu JD, Li S (2006b) Long term effect of methylparathion contamination on soil microbial community diversity estimated by 16S rRNA gene cloning. Ecotoxicology 15:523–530

    Article  PubMed  CAS  Google Scholar 

  • Zhang CL, Huang Z, Li Y-L, Romanek CS, Mills G, Wiegel J, Culp R, Noakes J, White DC (2007) Lipid biomarkers and carbon-isotope signatures of bacteria in Nevada hot springs. Geomicrobiol J 24:519–534

    Google Scholar 

Download references

Acknowledgments

We are grateful to David and Sandy Jamieson for access to the field site and Joy Hallmark and Nicole Fester for assistance in sample collection. We also thank Jeremy A. Dodsworth for assistance in the editorial process and Natasha Zolotova and Panjai Prapaipong at ASU for help with IC and ICP-MS. Harriet Brady and students from Pyramid Lake Junior and Senior High School were important participants in this research. This work was supported by NSF Grant Number MCB-054865 and start up funds from UNLV to BPH. KCC received fellowship support through NSF Grants 0447416 and 0724226. JBN received fellowship support through NIH grant P20 RR16464. CLZ was supported by NSF Grant Number MCB-0348180. Support to the Nevada Genomics Center also made this work possible through Grant Number P20 RR01646 from the National Center for Research Resources (NCRR), a component of the National Institutes of Health (NIH).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Brian P. Hedlund.

Additional information

Communicated by T. Matsunaga.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Costa, K.C., Navarro, J.B., Shock, E.L. et al. Microbiology and geochemistry of great boiling and mud hot springs in the United States Great Basin. Extremophiles 13, 447–459 (2009). https://doi.org/10.1007/s00792-009-0230-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00792-009-0230-x

Keywords

Navigation