Skip to main content

Archaeal diversity from hydrothermal systems of Deception Island, Antarctica

Abstract

Antarctica is an extreme continent composed of cold environments but also of several geothermal sites, among them is Deception Island, an active stratovolcano located in the South Shetland archipelago. From this island, few microbiological studies have been performed, and the presence of archaea has not been reported. In order to investigate the archaeal diversity in hydrothermalism from Deception Island, different submarine samples were taken from the flooded caldera. Samples were analyzed by denaturing gradient gel electrophoresis (DGGE) of the 16S rRNA gene in conjunction with culture-dependent methods at hyperthermophilic temperatures. Analysis from DGGE band sequencing showed the presence of archaea belonging to the hyperthermophilic genus Thermococcus and different uncultured archaea closely related to environmental clones from hydrothermal vents. Archaea from the psychrotolerant genus Methanococcoides were also detected. Additionally, we have successfully isolated an anaerobic hyperthermophilic archaeon closely related to Thermococcus celericrescens. Cells were irregular cocci with a diameter between 0.6 and 2 μm and grew at 50–90 °C and at a NaCl concentration of 1–5 %. Here, we present, based on culture-dependent and culture-independent approaches, the first report on archaea from marine hydrothermal sites of Antarctica.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Allan RN, Lebbe L, Heyrman J, De Vos P, Buchanan J, Logan NA (2005) Brevibacillus levickii sp. nov. and Aneurinibacillus terranovensis sp. nov., two novel thermoacidophiles isolated from geothermal soils of northern Victoria Land, Antarctica. Int J Syst Evol Microbiol 55:1039–1050

    PubMed  Article  CAS  Google Scholar 

  2. Amann R, Ludwig IW, Schleifer K-H (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169

    PubMed  CAS  Google Scholar 

  3. Barns SM, Fundyga RE, Jeffries MW, Pace NR (1994) Remarkable archaeal diversity detected in a Yellowstone National Park hot spring environment. Proc Natl Acad Sci USA 91:1609–1613

    PubMed  Article  CAS  Google Scholar 

  4. Barry JP, Greene HG, Orange DL, Baxter CH, Robinson BH, Kochevar RE, Nybakken JW, Reed DL, Mchugh CM (1996) Biologic and geologic characteristics of cold seeps in Monterrey Bay, California. Deep Sea Res 43:1739–1762

    Article  CAS  Google Scholar 

  5. Bonch-Osmolovskaya EA, Stetter KO (1991) Interspecies hydrogen transfer in cocultures of thermophilic archaea. Syst Appl Microbiol 14:205–208

    Article  CAS  Google Scholar 

  6. Burggraf S, Fricke H, Neuner A, Kristjansson JK, Rouvier P, Mandelco L, Woese CR, Stetter KO (1990) Methanococcus igneus sp. nov., a novel hyperthermophilic methanogen from a shallow submarine hydrothermal system. Syst Appl Microbiol 13:263–269

    PubMed  Article  CAS  Google Scholar 

  7. Caldwell SL, Laidler JR, Brewer EA, Eberly JO, Sandborgh SC, Colwell FS (2008) Anaerobic oxidation of methane: mechanisms, bioenergetics, and the ecology of associated microorganisms. Environ Sci Technol 42:6791–6799

    PubMed  Article  CAS  Google Scholar 

  8. Casamayor EO, Schafer H, Bañeras L, Pedrós-Alió C, Muyzer G (2000) Identification of and spatio-temporal differences between microbial assemblages from two neighboring sulfurous lakes: comparison by microscopy and denaturing gradient gel electrophoresis. Appl Environ Microbiol 66:499–508

    PubMed  Article  CAS  Google Scholar 

  9. Casamayor EO, Muyzer G, Pedrós-Alió C (2001) Composition and temporal dynamics of planktonic archaeal assemblages from anaerobic sulfurous environments studied by 16S rDNA denaturating gradient gel electrophoresis and sequencing. Aquat Microb Ecol 25:237–246

    Article  Google Scholar 

  10. Caselli A, Dos Santos Afonso M, Agusto MR (2004) Gases fumarólicos de la Isla Decepción (Shetland del Sur, Antártida): variaciones químicas y depósitos vinculados a la crisis sísmica de 1999. Rev Asoc Geol Argent 59:291–302

    Google Scholar 

  11. Christner B, Mosley-Thompson E, Thompson L, Reeve JN (2001) Isolation of bacteria and 16SrDNA from Lake Vostok accretion ice. Environ Microbiol 3:570–577

    PubMed  Article  CAS  Google Scholar 

  12. Franzmann PD, Springer N, Ludwig W, De Macario EC, Rohde M (1992) A methanogenic archaeon from Ace Lake, Antarctica: Methanococcoides burtonii sp. nov. Syst Appl Microbiol 15:573–581

    Article  Google Scholar 

  13. Gray SC, Sturz A, Bruns MD, Marzan RL, Dougherty D, Law HB, Brackett JE, Marcou M (2003) Composition and distribution of sediments and benthic foraminifera in a submerged caldera after 30 years of volcanic quiescence. Deep Sea Res II 50:1727–1751

    Article  Google Scholar 

  14. Hoehler TM, Alperin MJ, Albert DB, Martens CS (1994) Field and laboratory studies of methane oxidation in an anoxic marine sediment-evidence for a methanogen-sulfate reducer consortium. Global Biogeochem Cycles 8:451–463

    Article  CAS  Google Scholar 

  15. Huber JA, Butterfield DA, Baross JA (2002) Temporal changes in archaeal diversity and chemistry in a mid-ocean ridge subseafloor habitat. Appl Environ Microbiol 68:1585–1594

    PubMed  Article  CAS  Google Scholar 

  16. Hudson JA, Daniel RM (1988) Enumeration of thermophilic heterotrophs in geothermally heated soils from Mount Erebus, Ross Island, Antarctica. Appl Environ Microbiol 54:622–624

    PubMed  CAS  Google Scholar 

  17. Kuwabara T, Minaba M, Iwayama Y, Inouye I, Nakashima M, Marumo K et al (2005) Thermococcus coalescens sp. nov., a cell-fusing hyperthermophilic archaeon from Suiyo Seamount. Int J Syst Evol Microbiol 55:2507–2514

    PubMed  Article  CAS  Google Scholar 

  18. Kuwabara T, Minaba M, Ogi N, Kamekura M (2007) Thermococcus celericrescens sp. nov., a fast-growing and cell-fusing hyperthermophilic archaeon from a deep-sea hydrothermal vent. Int J Syst Evol Microbiol 57:437–443

    PubMed  Article  CAS  Google Scholar 

  19. Lavire C, Normand P, Alekhina I, Bulat S, Prieur D, Birrien J-L et al (2006) Presence of Hydrogenophilus thermoluteolus DNA in accretion ice in the subglacial Lake Vostok, Antarctica, assessed using rrs, cbb and hox. Environ Microbiol 8:2106–2114

    PubMed  Article  CAS  Google Scholar 

  20. LLarch A, Logan NA, Castellví J, Prieto MJ, Guinea J (1997) Isolation and characterization of thermophilic Bacillus spp. from geothermal environments on Deception Island, South Shetland Archipelago. Microb Ecol 34:58–65

    PubMed  Article  Google Scholar 

  21. Logan NA, Lebbe L, Hoste B, Goris J, Forsyth G, Heyndrickx M et al (2000) Aerobic endospore-forming bacteria from geothermal environments in northern Victoria Land, Antarctica, and Candlemas Island, South Sandwich archipelago, with the proposal of Bacillus fumarioli sp. nov. Int J Syst Evol Microbiol 50:1741–1753

    PubMed  CAS  Google Scholar 

  22. Martin W, Baross J, Kelley D, Russel M (2008) Hydrothermal vents and the origin of life. Nat Rev Microbiol 6:805–814

    PubMed  CAS  Google Scholar 

  23. Maugeri TL, Lentini V, Gugliandolo C, Italiano F, Cousin S, Stackebrandt E (2009) Bacterial and archaeal populations at two shallow hydrothermal vents off Panarea Island (Eolian Islands, Italy). Extremophiles 13:199–212

    PubMed  Article  CAS  Google Scholar 

  24. Miroshnichenko ML, Bonch-Osmolovskaya EA (2006) Recent developments in the thermophilic microbiology of deep-sea hydrothermal vents. Extremophiles 10:85–96

    PubMed  Article  Google Scholar 

  25. Moussard H, Moreira D, Cambon-Bonavita M, Lopez-Garcia P, Jeanthon C (2006) Uncultured Archaea in a hydrothermal microbial assemblage: phylogenetic diversity and characterization of a genome fragment from a euryarchaeote. FEMS Microbiol Ecol 57:452–469

    PubMed  Article  CAS  Google Scholar 

  26. Muñoz PA, Flores PA, Boehmwald FA, Blamey JM (2011) Thermophilic bacteria present in a sample from Fumarole Bay, Deception Island. Antarct Sci 23:549–555

    Article  Google Scholar 

  27. Muñoz-Martín A, Catalán M, Martín-Dávila J, Carbó A (2005) Upper crustal structure of Deception Island area (Bransfield Strait, Antarctica) from gravity and magnetic modeling. Antarct Sci 17:213–224

    Article  Google Scholar 

  28. Muyzer G, Brinkhoff T, Nübel U, Santegoeds C, Schäfer H, Wawer C (1998) Denaturing gradient gel electrophoresis (DGGE) in microbial ecology. In: Akkermans ADL, Van Elsas JD, De Bruijn FJ (eds) Molecular Microbial Ecology Manual. Kluwer, Dordrecht, pp 1–27

    Google Scholar 

  29. Nercessian O, Reysenbach AL, Prieur D, Jeanthon C (2003) Archaeal diversity associated with in situ samplers deployed on hydrothermal vents on the East Pacific Rise (13 degrees N). Environ Microbiol 5:492–502

    PubMed  Article  Google Scholar 

  30. Nercessian O, Prokofeva M, Lebedinski A, L’haridon S, Cary C, Prieur D, Jeanthon C (2004) Design of 16S rRNA-targeted oligonucleotide probes for detecting cultured and uncultured archaeal lineages in high-temperature environments. Environ Microbiol 6:170–182

    PubMed  Article  CAS  Google Scholar 

  31. Nercessian O, Fouquet Y, Pierre C, Prieur D, Jeanthon C (2005) Diversity of bacteria and archaea associated with a carbonate-rich metalliferous sediment sample from the rainbow vent field on the Mid-Atlantic Ridge. Environ Microbiol 7:698–714

    PubMed  Article  CAS  Google Scholar 

  32. Nicolaus B, Improta R, Manca M, Lama L, Esposito E, Gambacorta A (1998) Alicyclobacilli from an unexplored geothermal soil in Antarctica, Mount Rittmann. Polar Biol 19:133–141

    Article  Google Scholar 

  33. Nicolaus B, Lama L, Esposito E, Belliti MR, Improta R, Panico A, Gambacorta A (2000) Extremophiles in Antarctica. Ital J Zool 1:169–174

    Article  Google Scholar 

  34. Nunoura T, Oida H, Nakaseama M, Kosaka A, Ohkubo SB, Kikuchi T et al (2010) Archaeal diversity and distribution along thermal and geochemical gradients in hydrothermal sediments at the Yonaguni Knoll IV hydrothermal field in the Southern Okinawa Trough. Appl Environ Microbiol 76:1198–1211

    PubMed  Article  CAS  Google Scholar 

  35. Osburn MR, Amend JP (2011) Thermogladius shockii gen. nov., sp. nov., a hyperthermophilic crenarchaeote from Yellowstone National Park, USA. Arch Microbiol 193:45–52

    PubMed  Article  CAS  Google Scholar 

  36. Pernthaler A, Dekas AE, Brown CT, Goffredi SK, Embaye T, Orphan VJ (2008) Diverse syntrophic partnerships from deep-sea methane vents revealed by direct cell capture and metagenomics. Proc Natl Acad Sci USA 105:7052–7057

    PubMed  Article  CAS  Google Scholar 

  37. Poli A, Esposito E, Lama L, Orlando P, Nicolaus G, De Appolonia F et al (2006) Anoxybacillus amylolyticus sp. nov., a thermophilic amylase producing bacterium isolated from Mount Rittmann (Antarctica). Syst Appl Microbiol 29:300–307

    PubMed  Article  CAS  Google Scholar 

  38. Raskin L, Stromley JM, Rittmann BE, Stahl DA (1994) Group-specific 16S rRNA hybridization probes to describe natural communities of methanogens. Appl Environ Microbiol 60:1232–1240

    PubMed  CAS  Google Scholar 

  39. Reysenbach AL, Cady S (2001) Microbiology of ancient and modern hydrothermal systems. Trends Microbiol 9:79–86

    PubMed  Article  CAS  Google Scholar 

  40. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  41. Sako Y, Nomura N, Uchida A, Ishida Y, Morii H, Koga Y, Hoaki T, Maruyama T (1996) Aeropyrum pernix gen. nov., sp nov., a novel aerobic hyperthermofilic archeon growing al temperatures up to 100 °C. Int J Syst Evol Microbiol 46:1070–1077

    CAS  Google Scholar 

  42. Stahl DA, Amann RI (1991) Development and application of nucleic acid probes. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 205–248

    Google Scholar 

  43. Takai K, Nealson KH, Horikoshi K (2004) Methanotorris formicicus sp. nov., a novel extremely thermophilic, methane-producing archaeon isolated from a black smoker chimney in the Central Indian Ridge. Int J Syst Evol Microbiol 54:1095–1100

    PubMed  Article  CAS  Google Scholar 

  44. Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci USA 101:11030–11035

    PubMed  Article  CAS  Google Scholar 

  45. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    PubMed  Article  CAS  Google Scholar 

  46. Zillig W, Reysenbach A-L (2001) Class IV. Thermococci class. nov. In: Boone DR, Castenholz RW (eds) Bergey’s manual of systematic bacteriology. Springer, New York, pp 342–346

    Google Scholar 

Download references

Acknowledgments

We would like to thank Dr. Jorge Rey from the Spanish Institute of Oceanography for his help on collecting the samples used in this work. We also thank to Alissa Cook from the Writing Center of Montana State University for its help improving the language of our manuscript, to Alejandro Munizaga for its help in TEM analysis and to the Instituto Antártico Chileno for its support. This work was funded by the project Innova-Corfo grant #07CN13PXT264, 2008–2012.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Maximiliano J. Amenábar.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Amenábar, M.J., Flores, P.A., Pugin, B. et al. Archaeal diversity from hydrothermal systems of Deception Island, Antarctica. Polar Biol 36, 373–380 (2013). https://doi.org/10.1007/s00300-012-1267-3

Download citation

Keywords

  • Hyperthermophilic archaea
  • Thermococcales
  • DGGE
  • Submarine hydrothermalism