Microbial Diversity in Acidic High-Temperature Steam Vents

  • Richard L. Weiss Bizzoco
  • Scott T. Kelley
Part of the Cellular Origin, Life in Extreme Habitats and Astrobiology book series (COLE, volume 27)


Fumaroles represent one of the most abundant and understudied geothermal features on Earth. Recent discoveries of microorganisms transported in steam from the subsurface have increased interest in these extreme habitats. Isolation of environmental DNA from high-temperature low-pH steam deposits poses considerable challenges and has foiled many previous studies. We examined samples of steam deposits collected from steam caves/vents in three national parks, Hawaii Volcanoes National Park, Yellowstone National Park, and Lassen Volcanic National Park, and other more remote international sites for their chemical constituents and microbial populations. DNA culture-independent analysis of condensed steam generated from the subsurface showed that it carried halophilic organisms (Archaea), despite a paucity of dissolved ions. Several of these halophiles were also cultivated from the Hawaiian steam deposit samples. As found in previous studies, DNA isolation from deposits in direct contact with subsurface steam proved to be refractory to isolation in many of the cave/vent deposit samples. However, our modifications of existing DNA extraction methods yielded DNA in half of the samples, providing the first evidence of Archaea in steam deposit habitats. BLAST analysis of the resulting 16S rRNA gene sequences showed that sulfur steam caves and vents were inhabited by Sulfolobus and Acidianus. Nonsulfur cave inhabitants were represented by novel Crenarchaeota, and Hawaiian samples contained novel lineages related to ammonia-oxidizing Archaea in the newly proposed Thaumarchaeota. The 50 % of samples that proved to be refractory to DNA isolation eventually yielded cultures that were shown to be related to Sulfolobus or unknown Archaea. Recent culture-independent analysis of bacterial diversity in these habitats found them to be a complex and heterogeneous habitat composed of many extremophile lineages. These results show fumaroles to be a rich source of microorganisms that represent new and unknown microbes.


Thin Filament amoA Gene Condensed Steam Flowing Spring Cave Deposit 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The authors acknowledge the assistance of Dr. Steve Barlow and use of equipment at the San Diego State University Electron Microscopy Facility acquired by NSF Instrumentation grant DBI-0959908. We thank the National Park Service at Yellowstone National Park, Lassen Volcanic National Park, and Hawaii Volcanoes National Park for assistance and allowing our collections. We also thank Caryl McHarney, Benno Spingler, Xzayla Xibiti, and our graduate students who assisted or contributed ideas during the design of the steam collector. We thank Lisa Thurn for chemistry, and Courtney Benson, Wendy Gutierrez, Ann McAfee, and Harmony Saunders for the microbial culture. The generous contributions of Schering-Plough Biopharma are gratefully acknowledged.


  1. Ackerman CA, Anderson S, Anderson C (2007) Diversity of thermophilic microorganisms within Hawaiian fumaroles. Eos Trans Am Geophys Union 88:B33A–0854Google Scholar
  2. Arahal DR, Dewhirst FE, Paster BJ, Volcani BE, Ventosa A (1996) Phylogenetic analyses of some extremely halophilic archaea isolated from Dead Sea water, determined on the basis of their 16S rRNA sequences. Appl Environ Microbiol 62:3779–3786PubMedGoogle Scholar
  3. Benson CA (2010) Microbial diversity in steam vent sublimates. MS thesis, SDSU, San DiegoGoogle Scholar
  4. Benson CA, Bizzoco RW, Lipson DA, Kelley ST (2011) Microbial diversity in nonsulfur, sulfur and iron geothermal steam vents. FEMS Microbiol Ecol 76:74–88PubMedCrossRefGoogle Scholar
  5. Bonheyo GT, Frias-Lopez J, Fouke BW (2005) A test for airborne dispersal of thermophilic bacteria from hot springs. In: Inskeep WP, McDermott TR (eds) Geothermal biology and geochemistry in Yellowstone National Park. Montana State University Publications, Bozeman, pp 327–340Google Scholar
  6. Bowman JP, Rea SM, McCammon SA, McMeekin TA (2000) Diversity and community structure within anoxic sediment from marine salinity meromictic lakes and a costal meromictic marine basin, Vestfold Hills, Eastern Antarctica. Environ Microbiol 2:227–237PubMedCrossRefGoogle Scholar
  7. Boyd ES, Jackson RA, Encarnacion G, Zahn JA, Beard T, Leavitt WD et al (2007) Isolation, characterization, and ecology of sulfur-respiring Crenarchaea inhabiting acid-sulfate-chloride-containing geothermal springs in Yellowstone National Park. Appl Environ Microbiol 73:6669–6677PubMedCrossRefGoogle Scholar
  8. Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P (2008) Mesophilic crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 6:245–252PubMedCrossRefGoogle Scholar
  9. Brock TD, Mosser JL (1975) Rate of sulfuric-acid production in Yellowstone National Park. Geol Soc Am Bull 86:194–198CrossRefGoogle Scholar
  10. Costello EK, Halloy SRP, Reed SC, Sowell P, Schmidt SK (2009) Fumarole-supported islands of biodiversity within a hyperarid, high-elevation landscape on Socompa Volcano, Puna de Atacama, Andes. Appl Environ Microbiol 75:735–747PubMedCrossRefGoogle Scholar
  11. de la Torre JR, Walker CB, Ingalls AE, Könneke M, Stahl DA (2008) Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ Microbiol 10:810–818PubMedCrossRefGoogle Scholar
  12. Dunfield PF, Yuryev A, Senin P, Smirnova AV, Stott MB, Hou S et al (2007) Methane oxidation by an extremely acidophilic bacterium of the phylum Verrucomicrobia. Nature 450:879–882PubMedCrossRefGoogle Scholar
  13. Ellis DG, Bizzoco RW, Kelley ST (2008) Halophilic Archaea determined from geothermal steam vent aerosols. Environ Microbiol 10:1582–1590PubMedCrossRefGoogle Scholar
  14. Henneberger RM, Walter MR, Anitori RP (2006) Extraction of DNA from acidic, hydrothermally modified volcanic soils. Environ Chem 3:100–104CrossRefGoogle Scholar
  15. Herrera A, Cockell CS (2007) Exploring microbial diversity in volcanic environments: a review of methods in DNA extraction. J Microbiol Methods 70:1–12PubMedCrossRefGoogle Scholar
  16. Ihara K, Watanabe S, Tamura T (1997) Haloarcula argentinensis sp. nov. and Haloarcula mukohataei sp. nov., two new extremely halophilic archaea collected in Argentina. Int J Syst Bacteriol 47:73–77PubMedCrossRefGoogle Scholar
  17. Ikeda S, Tsurumaru H, Wakai S, Noritake C, Fujishiro K, Akasaka M, Ando K (2008) Evaluation of the effects of different additives in improving the DNA extraction yield and quality from andosol. Microbes Environ 23:159–166PubMedCrossRefGoogle Scholar
  18. Jones ME (1963) Ammonia equilibrium between vapor and liquid aqueous phases at elevated temperatures. J Phys Chem 67:1113–1115CrossRefGoogle Scholar
  19. Könneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546PubMedCrossRefGoogle Scholar
  20. Mayhew LE, Geist DJ, Childers SE, Pierson JD (2007) Microbial community comparisons as a function of the physical and geochemical conditions of Galápagos Island fumaroles. Geomicrobiol J 24:615–625CrossRefGoogle Scholar
  21. Nordstrom DK, Ball JW, McCleskey RB (2005) Ground water to surface water: chemistry of thermal outflows in Yellowstone National Park. In: Inskeep WP, McDermott TR (eds) Geothermal biology and geochemistry in Yellowstone National Park. Montana State University Publications, Bozeman, pp 73–94Google Scholar
  22. Oren A, Ventosa A, Gutiérrez MC, Kamekura M (1999) Haloarcula quadrata sp. nov., a square motile archaeon isolated from a brine pool in Sinai (Egypt). Int J Syst Bacteriol 49:1149–1155PubMedCrossRefGoogle Scholar
  23. Portillo MC, Gonzalez JM (2008) Microbial communities and immigration in volcanic environments of Canary Islands (Spain). Naturwissenschaften 95:307–315PubMedCrossRefGoogle Scholar
  24. Soo RM, Wood SA, Grzymski JJ, McDonald IR, Cary SC (2009) Microbial biodiversity of thermophilic communities in hot mineral soils of Tramway Ridge, Mount Erebus, Antarctica. Environ Microbiol 11:715–728PubMedCrossRefGoogle Scholar
  25. 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 10:2030–2041PubMedCrossRefGoogle Scholar
  26. Takada-Hoshino Y, Matsumoto N (2004) An improved DNA extraction method using skim milk from soils that strongly adsorb DNA. Microbes Environ 19:13–19CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Department of BiologySan Diego State UniversitySan DiegoUSA

Personalised recommendations