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Extremophiles

, Volume 21, Issue 5, pp 891–901 | Cite as

Characterization of a cold-active bacterium isolated from the South Pole “Ice Tunnel”

  • Michael T. Madigan
  • Megan L. Kempher
  • Kelly S. Bender
  • Paul Sullivan
  • W. Matthew Sattley
  • Alice C. Dohnalkova
  • Samantha B. Joye
Original Paper

Abstract

Extremely cold microbial habitats on Earth (those below −30 °C) are rare and have not been surveyed for microbes as extensively as environments in the 0 to −20 °C range. Using cryoprotected growth media incubated at −5 °C, we enriched a cold-active Pseudomonas species from −50 °C ice collected from a utility tunnel for wastewater pipes under Amundsen–Scott South Pole Station, Antarctica. The isolate, strain UC-1, is related to other cold-active Pseudomonas species, most notably P. psychrophila, and grew at −5 °C to +34–37 °C; growth of UC-1 at +3 °C was significantly faster than at +34 °C. Strain UC-1 synthesized a surface exopolymer and high levels of unsaturated fatty acids under cold growth conditions. A 16S rRNA gene diversity screen of the ice sample that yielded strain UC-1 revealed over 1200 operational taxonomic units (OTUs) distributed across eight major classes of Bacteria. Many of the OTUs were Clostridia and Bacteriodia and some of these were probably of wastewater origin. However, a significant fraction of the OTUs were Proteobacteria and Actinobacteria of likely environmental origin. Our results shed light on the lower temperature limits to life and the possible existence of functional microbial communities in ultra-cold environments.

Keywords

Antarctic microbiology Amundsen–Scott South Pole Station Pseudomonas psychrophila 

Notes

Acknowledgements

This project was supported in part by NASA Exobiology/Astrobiology Program Award NNX11AG45G to SBJ. Electron microscopy was performed at the Environmental Molecular Sciences Laboratory (EMSL), a national scientific user facility sponsored by the Department of Energy’s Office of Biological and Environmental Research, located at the Pacific Northwest National Laboratory in Richland, WA. Special thanks are extended to Dr. Michael New (NASA) and Dr. Roberta Marinelli (NSF) for arranging the sample collection visit of MTM to Amundsen–Scott Station, and to the New York Air National Guard for round trip LC-130 transportation from McMurdo to the South Pole. MTM thanks Deborah Jung and Spencer Horn for technical assistance.

References

  1. Abyzov SS (1995) Microorganisms in the Antarctic ice. In: Friedmann EI (ed) Antarctic microbiology. Wiley-Liss, New York, pp 265–295Google Scholar
  2. Achberger AM, Christner BC, Michaud AB, Priscu JC, Skidmore ML, Vick-Majors TJ, The WISSARD Science Team (2016) Microbial community structure of subglacial Lake Whillans, West Antarctica. Front Microbiol 7:1457. doi: 10.3389/fmicb.2016.01457 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Aislabie J, Broady P, Saul D (2006) Viable heterotrophic bacteria from high altitude, high latitude soil of La Gorce Mountains (86°30′S, 147°W), Antarctica. Antarct Sci 18:313–321CrossRefGoogle Scholar
  4. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefPubMedGoogle Scholar
  5. Bakermans C (2008) Limits for microbial life at subzero temperatures. In: Margesin R, Schinner F, Marx J-C, Gerday C (eds) Psychrophiles: from biodiversity to biotechnology. Springer, Berlin, pp 17–30CrossRefGoogle Scholar
  6. Bakermans C, Tsapin AI, Souza-Egipsy V, Gilichinsky DA, Nealson KH (2003) Reproduction and metabolism at −10 °C of bacteria isolated from Siberian permafrost. Environ Microbiol 5:321–326CrossRefPubMedGoogle Scholar
  7. Bodhaine BA, Deluisi JJ, Harris JM (1986) Aerosol measurements at the South Pole. Tellus 38B:223–235CrossRefGoogle Scholar
  8. Boetius A, Anesio AM, Deming JW, Mikucki JA, Rapp JZ (2015) Microbial ecology of the cryosphere: sea ice and glacial habitats. Nat Rev Microbiol 13:677–690CrossRefPubMedGoogle Scholar
  9. Bott TL, Brock TD (1969) Bacterial growth rates above 90 °C in Yellowstone hot springs. Science 164:1411–1412CrossRefPubMedGoogle Scholar
  10. Bottos EM, Scarrow JW, Archer SDJ, McDonald IR, Cary SC (2014) Bacterial community structures of Antarctic soils. In: Cowan DA (ed) Antarctic terrestrial microbiology. Springer, Berlin, pp 9–33CrossRefGoogle Scholar
  11. Brandt RE, Warren SG (1997) Temperature measurements and heat transfer in near-surface snow at the South Pole. J Glaciol 43:339–351CrossRefGoogle Scholar
  12. Breezee J, Cady N, Staley JT (2004) Subfreezing growth of the sea ice bacterium “Psychromonas ingrahamii”. Microb Ecol 47:300–304CrossRefPubMedGoogle Scholar
  13. Cameron RE (1971) Antarctic soil microbiological and ecological investigations. In: Quam LO, Porter HD (eds) Research in the Antarctic. American Association for the Advancement of Science, Washington, pp 137–189Google Scholar
  14. Cameron RE (1972) Farthest south algae and associated bacteria. Phycologia 11:133–139CrossRefGoogle Scholar
  15. Cameron RE, Morelli FA, Johnson RM (1972) Bacterial species in soil and air of the Antarctic continent. Antarc J US 7:187–189Google Scholar
  16. Carpenter EJ, Lin S, Capone DG (2000) Bacterial activity in South Pole snow. Appl Environ Microbiol 66:4514–4517CrossRefPubMedPubMedCentralGoogle Scholar
  17. Cary SC, McDonald IR, Barrett JE, Cowan DA (2010) On the rocks: the microbiology of Antarctic Dry Valley soils. Nat Rev Microbiol 8:129–138CrossRefPubMedGoogle Scholar
  18. Christner BC (2002) Incorporation of DNA and protein precursors into macromolecules by bacteria at −15 °C. Appl Environ Microbiol 68:6435–6438CrossRefPubMedPubMedCentralGoogle Scholar
  19. Christner BC, Mosley-Thompson E, Thompson LG, Zagorodnov V, Sandman K, Reeve JN (2000) Recovery and identification of viable bacteria immured in glacial ice. Icarus 144:479–485CrossRefGoogle Scholar
  20. Christner BC, Mosley-Thompson E, Thompson LG, Reeve JN (2001) Isolation of bacteria and 16SrDNAs from Lake Vostok accretion ice. Environ Microbiol 3:570–577CrossRefPubMedGoogle Scholar
  21. Christner BC, Mosley-Thompson E, Thompson LG, Reeve JN (2003) Bacterial recovery from ancient glacial ice. Environ Microbiol 5:433–436CrossRefPubMedGoogle Scholar
  22. Christner BC, Skidmore ML, Priscu JC, Tranter M, Foreman CM (2008) Bacteria in subglacial environments. In: Margesin R, Schinner F, Marx J-C, Gerday C (eds) Psychrophiles: from biodiversity to biotechnology. Springer, Berlin, pp 51–71CrossRefGoogle Scholar
  23. Christner BC, Priscu JC, Achberger AA, Barbante C, Carter SP, Christianson K, Michaud AB, Mikucki JA, Mitchell AC, Skidmore ML, Vick-Majors TJ, The WISSARD Science Team (2014) A microbial ecosystem beneath the West Antarctic ice sheet. Nature 512:310–313CrossRefPubMedGoogle Scholar
  24. Claridge GGC, Campbell IB, Stout JD, Dutch ME, Flint EA (1971) The occurrence of soil organisms in the Scott Glacier region, Queen Maud Range, Antarctica. N Z J Sci 14:306–312Google Scholar
  25. Clocksin KM, Jung DO, Madigan MT (2007) Cold-active chemoorganotrophic bacteria from the water column of the permanently ice-covered Lake Hoare, McMurdo Dry Valleys, Antarctica. Appl Environ Microbiol 73:3077–3083CrossRefPubMedPubMedCentralGoogle Scholar
  26. 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–D145CrossRefPubMedGoogle Scholar
  27. Cole JK, Hutchison JR, Renslow RS, Kim Y-M, Chrisler WB, Engelmann HE, Dohnalkova AC, Hu D, Metz TO, Frederickson JK, Lindemann SR (2014) Phototrophic biofilm assembly in microbial-mat-derived unicyanobacterial consortia: model systems for the study of autotroph–heterotroph interactions. Front Microbiol 5:109. doi: 10.3389/fmicb.2014.00109 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Collins MA, Buick RK (1989) Effect of temperature on the spoilage of stored peas by Rhodotorula glutinis. Food Microbiol 6:135–141CrossRefGoogle Scholar
  29. Cowan DA (ed) (2014) Antarctic terrestrial microbiology. Springer, HeidelbergGoogle Scholar
  30. Darling CA, Siple PA (1940) Bacteria of Antarctica. J Bacteriol 42:83–98Google Scholar
  31. de Vera J-P, Schulze-Makuch D, Khan A, Lorek A, Koncz A, Möhlmann D, Spohn T (2014) Adaptation of an Antarctic lichen to Martian niche conditions can occur within 34 days. Planet Space Sci 98:182–190CrossRefGoogle Scholar
  32. DeLeon-Rodriquez N, Lathem TL, Rodriquez-R LM, Barazesh JM, Anderson BE, Beyersdorf AJ, Ziemba LD, Bergin M, Nenes A, Konstantinidis KT (2013) Microbiome of the upper troposphere: species composition and prevalence, effects of tropical storms, and atmospheric implications. Proc Natl. Acad Sci USA 110:2575–2580CrossRefGoogle Scholar
  33. Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) (2006) The prokaryotes, vol 4, 3rd edn. Bacteria: firmicutes, cyanobacteria. Springer, BerlinGoogle Scholar
  34. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461CrossRefPubMedGoogle Scholar
  35. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200CrossRefPubMedPubMedCentralGoogle Scholar
  36. Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) (2006) The prokaryotes: vol 5: proteobacteria: alpha and beta subclasses. Springer, New YorkGoogle Scholar
  37. Felsenstein J (2005) PHYLIP (Phylogeny Inference Package) version 3.6. Department of Genome Sciences, University of Washington, SeattleGoogle Scholar
  38. Gilichinsky D, Rivkina E, Shcherbakova V, Laurinavichuis K, Tiedje J (2003) Supercooled water brines within permafrost—an unknown ecological niche for microorganisms: a model for astrobiology. Astrobiology 3:331–341CrossRefPubMedGoogle Scholar
  39. Gilichinsky D, Rivkina E, Bakermans C, Shcherbakova V, Petrovskaya L, Ozerskaya S, Ivanushkina N, Kochkina G, Laurinavichuis K, Pecheritsina S, Fattakhova R, Tiedje JM (2005) Biodiversity of cryopegs in permafrost. FEMS Microbiol Ecol 53:117–128CrossRefPubMedGoogle Scholar
  40. Hauser E, Kämpfer P, Busse H-J (2004) Pseudomonas psychrotolerans sp. nov. Intl J Syst Evol Microbiol 54:1633–1637CrossRefGoogle Scholar
  41. Jakosky BM, Nealson KH, Bakermans C, Ley RE, Mellon MT (2003) Subfreezing activity of microorganisms and the potential habitability of Mars’ polar regions. Astrobiology 3:343–350CrossRefPubMedGoogle Scholar
  42. Jannson JK, Neslihan T (2014) The microbial ecology of permafrost. Nat Rev Microbiol 12:414–425CrossRefGoogle Scholar
  43. Jung DO, Achenbach LA, Karr EA, Takaichi S, Madigan MT (2004) A gas vesiculate planktonic strain of the purple non-sulfur bacterium Rhodoferax antarcticus isolated from Lake Fryxell, Dry Valleys, Antarctica. Arch Microbiol 182:236–243CrossRefPubMedGoogle Scholar
  44. Karl DM, Bird DF, Bjorkman K, Houlihan T, Shackelford R, Tupas L (1999) Microorganisms in the accreted ice of Lake Vostok, Antarctica. Science 286:2144–2147CrossRefPubMedGoogle Scholar
  45. Karr EA, Sattley WM, Rice MR, Jung DO, Madigan MT, Achenbach LA (2005) Diversity and distribution of sulfate-reducing bacteria in permanently frozen Lake Fryxell, McMurdo Dry Valleys, Antarctica. Appl Environ Microbiol 71:6353–6359CrossRefPubMedPubMedCentralGoogle Scholar
  46. Karr EA, Ng JM, Belchik SM, Sattley WM, Madigan MT, Achenbach LA (2006) Biodiversity of methanogenic and other Archaea in the permanently frozen Lake Fryxell, Antarctica. Appl Environ Microbiol 72:1663–1666CrossRefPubMedPubMedCentralGoogle Scholar
  47. Kong Y (2011) Btrim: a fast, lightweight adapter and quality trimming program for next-generation sequencing technologies. Genomics 98:152–153CrossRefPubMedGoogle Scholar
  48. Kwon M, Kim M, Takacs-Vesbach C, Lee J, Hong SG, Kim SJ, Priscu JC, Kim O-S (2017) Nich specialization in permanently ice-covered lakes of the McMurdo Dry Valleys. Environ Microbiol, Antarctica. doi: 10.1111/1462-2920.13721 Google Scholar
  49. Lamarche-Gagnon G, Comery R, Greer CW, Whyte LG (2015) Evidence of in situ microbial activity and sulphidogenesis in perennially sub-0 °C and hypersaline sediments of a high Arctic permafrost spring. Extremophiles 19:1–15CrossRefPubMedGoogle Scholar
  50. Lanoil B, Skidmore M, Priscu JC, Han S, Foo W, Vogel SW, Tulaczyk S, Engelhardt H (2009) Bacteria beneath the West Antarctic ice sheet. Environ Microbiol 11:609–615CrossRefPubMedGoogle Scholar
  51. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948CrossRefPubMedGoogle Scholar
  52. Madigan MT, Kempher ML, Bender KS, Sullivan P, Dohnalkova AC, Samarkin VA, Joye SB (2015) Characterization of a bacterium isolated from the South Pole “ice tunnel”. Abstracts Gen Meeting ASM, New OrleansGoogle Scholar
  53. Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963CrossRefPubMedPubMedCentralGoogle Scholar
  54. Marx JG, Carpenter SD, Deming JW (2009) Production of cyroprotectant extracellular polysaccharide substances (EPS) by the marine psychrophilic bacterium Colwellia psychrerythraea strain 34H under extreme conditions. Can J Microbiol 55:63–72CrossRefPubMedGoogle Scholar
  55. McKay CP (1995) Relevance of Antarctic microbial ecosystems to exobiology. In: Friedmann EI (ed) Antarctic microbiology. Wiley-Liss, New York, pp 593–601Google Scholar
  56. Mikucki JA, Pearson A, Johnston DT, Turchyn AV, Farquhar J, Schrag DP, Anbar AD, Priscu JC, Lee PA (2009) A contemporary microbially maintained subglacial ferrous “ocean”. Science 324:397–400CrossRefPubMedGoogle Scholar
  57. Mikucki JA, Auken E, Tulaczyk S, Virginia RA, Schamper C, Sørensen KI, Doran PT, Dugan H, Foley N (2015) Deep groundwater and potential subsurface habitats beneath an Antarctic dry valley. Nat Commun 6:6831. doi: 10.1038/ncomms7831. CrossRefPubMedPubMedCentralGoogle Scholar
  58. Mikucki JA, Lee PA, Ghosh D, Purcell AM, Mitchell AC, Mankoff KD, Fisher AT, Tulaczyk S, Carter S, Siegfried MR, Fricker HA, Hodson T, Coenen J, Prowll R, Scherer R, Vick-Majors T, Achberger AA, Christner BC, Tranter M, The WISSARD Science Team (2016) Subglacial Lake Whillans microbial biogeochemistry: a synthesis of current knowledge. Phil Trans R Soc A 374:20140290CrossRefPubMedGoogle Scholar
  59. Miteva V (2008) Bacteria in snow and glacier ice. In: Margesin R, Schinner F, Marx J-C, Gerday C (eds) Psychrophiles: from biodiversity to biotechnology. Springer, Berlin, pp 31–50CrossRefGoogle Scholar
  60. Miteva V, Sheridan PP, Brenchley JE (2004) Phylogenetic and physiological diversity of microorganisms isolated from a deep Greenland glacier ice core. Appl Environ Microbiol 70:202–213CrossRefPubMedPubMedCentralGoogle Scholar
  61. Molin G, Ternström A (1986) Phenotypically based taxonomy of psychrotrophic Pseudomonas isolated from spoiled meat, water, and soil. Int J Syst Bacteriol 36:257–274CrossRefGoogle Scholar
  62. Molin G, Ternström A, Ursing J (1986) Pseudomonas lundensis, a new bacterial species isolated from meat. Int J Syst Bacteriol 36:339–342CrossRefGoogle Scholar
  63. Mykytczuk NCS, Foote SJ, Omelon CR, Southan G, Greer CW, Whyte LG (2013) Bacterial growth at −15 °C; molecular insights from the permafrost bacterium Planococcus halocryophilus Or1. ISME J 7:1211–1226CrossRefPubMedPubMedCentralGoogle Scholar
  64. Palleroni NJ (1992) Introduction to the family Pseudomonadaceae. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer KH (eds) The prokaryotes, 2nd edn. Springer, New York, pp 3071–3085Google Scholar
  65. Panikov NS, Flanagan PW, Oechel WC, Mastepanov MA, Christensen TR (2006) Microbial activity in soils frozen to below −39 °C. Soil Biol Biochem 38:785–794CrossRefGoogle Scholar
  66. Price PB (1999) A habitat for psychrophiles in deep Antarctic ice. Proc Natl Acad Sci USA 97:1247–1251CrossRefGoogle Scholar
  67. Price PB, Sowers T (2004) Temperature dependence of metabolic rates for microbial growth, maintenance, and survival. Proc Natl Acad Sci USA 101:4631–4636CrossRefPubMedPubMedCentralGoogle Scholar
  68. Priscu JC, Fritsen CH, Adams EE, Giovannoni SJ, Paerl HW, McKay CP, Doran PT, Gordon DA, Lanoil BD, Pinckney JL (1998) Perennial Antarctic lake ice: an Oasis for life in a polar desert. Science 280:2095–2098CrossRefPubMedGoogle Scholar
  69. Priscu JC, Adams EE, Lyons WB, Voytek MA, Mogk DW, Brown RL, McKay CP, Takacs CD, Welch KA, Wolf CR, Kirshtein JD, Avci R (1999) Geomicrobiology of subglacial ice above Lake Vostok, Antarctica. Science 286:2141–2144CrossRefPubMedGoogle Scholar
  70. Rivkina EM, Friedmann EI, McKay CP, Gilichinsky DA (2000) Metabolic activity of permafrost bacteria below the freezing point. Appl Environ Microbiol 66:3230–3233CrossRefPubMedPubMedCentralGoogle Scholar
  71. Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) (2014) The prokaryotes—gammaproteobacteria, 4th edn. Springer, BerlinGoogle Scholar
  72. Russell NJ (1997) Psychrophilic bacteria—molecular adaptation of membrane lipids. Comp Biochem Physiol 118A:489–493CrossRefGoogle Scholar
  73. Sattley WM, Madigan MT (2006) Isolation, characterization and ecology of cold-active chemolithotrophic sulfur-oxidizing bacteria from perennially ice covered Lake Fryxell, Antarctica. Appl Environ Microbiol 72:5562–5568CrossRefPubMedPubMedCentralGoogle Scholar
  74. Sattley WM, Madigan MT (2007) Cold-active acetogenic bacteria from surficial sediments of perennially ice-covered Lake Fryxell, Antarctica. FEMS Microbiol Lett 272:48–54CrossRefPubMedGoogle Scholar
  75. Sattley WM, Madigan MT (2010) Temperature and nutrient induced responses of Lake Fryxell sulfate-reducing prokaryotes and description of Desulfovibrio lacusfryxellense, sp. nov., a pervasive, cold-active, sulfate-reducing bacterium from Lake Fryxell, Antarctica. Extremophiles 14:357–366CrossRefPubMedGoogle Scholar
  76. Shcherbakova VA, Chuvilskaya NA, Rivkina EM, Pecheritsyna SA, Laurinavichius KS, Suzina NE, Osipov GA, Lysenko AM, Gilichinsky DA, Akimenko VK (2005) Novel psychrophilic anaerobic spore-forming bacterium from the overcooled water brine in permafrost: description Clostridium algoriphilum sp. nov. Extremophiles 9:239–246CrossRefPubMedGoogle Scholar
  77. Shi T, Reever RH, Gilchinsky DA, Freidman EI (1997) Characterization of viable bacteria from Siberian permafrost by 16S rDNA sequencing. Microb Ecol 33:169–179CrossRefPubMedGoogle Scholar
  78. Shtarkman YM, Koçer ZA, Edgar R, Veerapaneni RS, D’Elia T, Morris PF, Rogers SO (2013) Subglacial Lake Vostok (Antarctica) accretion ice contains a diverse set of sequences from aquatic, marine, and sediment-inhabiting bacteria and Eukarya. PLoS One 8(7):e67221. doi: 10.1371/journal.pone.0067221 CrossRefPubMedPubMedCentralGoogle Scholar
  79. Smith JJ, Tow LH, Stafford W, Cary C, Cowan DA (2006) Bacterial diversity in three different Antarctic cold desert mineral soils. Microbial Ecol 51:413–421CrossRefGoogle Scholar
  80. Steven B, Léveillé R, Pollard WH, Whyte LG (2006) Microbial ecology and biodiversity in permafrost. Extremophiles 10:259–267CrossRefPubMedGoogle Scholar
  81. Stevenson A, Hallsworth JE (2014) Water and temperature relations of soil Actinobacteria. Environ Microbiol Rep 6:744–755CrossRefPubMedGoogle Scholar
  82. Straka RP, Stokes JL (1960) Psychrophilic bacteria from Antarctica. J Bacteriol 80:622–625PubMedPubMedCentralGoogle Scholar
  83. Takacs CD, Priscu JC (1998) Bacterioplankton dynamics in the McMurdo Dry Valley lakes, Antarctica: production and biomass loss over four seasons. Microb Ecol 36:239–250CrossRefPubMedGoogle Scholar
  84. Takacs-Vesbach C, Zeglin L, Barrett JE, Gooseff MN, Priscu JC (2010) Factors promoting microbial diversity in the McMurdo Dry Valleys, Antarctica. In: Doran PT, Lyons WB, McKnight DM (eds) Life in Antarctic deserts and other cold dry environments: astrobiological analogs. Cambridge University Press, Cambridge, pp 221–257CrossRefGoogle Scholar
  85. Takai K, Nakamura K, Toki T, Tsunogai U, Miyazaki M, Miyadaki J, Hirayama H, Nakagawa S, Nunoura T, Horikoshi K (2008) Cell proliferation at 122 °C and isotopically heavy CH4 production by a hyperthermophilic methanogen under high-pressure cultivation. Proc Natl Acad Sci USA 105:10949–10954CrossRefPubMedPubMedCentralGoogle Scholar
  86. Tang C, Madigan MT, Lanoil B (2013) Bacterial and archaeal diversity in sediments of West Lake Bonney, McMurdo Dry Valleys, Antarctica. Appl Environ Microbiol 79:1034–1038CrossRefPubMedPubMedCentralGoogle Scholar
  87. Tregoning GS, Kempher ML, Jung DO, Samarkin VA, Joye SB, Madigan MT (2015) A halophilic bacterium inhabiting the warm, CaCl2-rich brine of the perennially ice-covered Lake Vanda, McMurdo Dry Valleys, Antarctica. Appl Environ Microbiol 81:1988–1995CrossRefPubMedPubMedCentralGoogle Scholar
  88. Tuorto SJ, Darias P, McGuinness LR, Panikov N, Zhang T, Häggblom MM, Kerkhof LJ (2014) Bacterial genome replication at subzero temperatures in permafrost. ISME J 8:139–149CrossRefPubMedGoogle Scholar
  89. United States Department of Commerce–NOAA (2017) Earth System Research Laboratory–Meteorology South Pole, Antarctica. https://www.esrl.noaa.gov/gmd/obop/spo/. Accessed 15 Mar 2017
  90. Vick-Majors TJ, Mitchell AC, Achberger AM, Christner BC, Dore JE, Alexander BM, Mikucki JA, Purcell AM, Skidmore ML, Priscu JC (2016) Physiological ecology of microorganisms in subglacial Lake Whillans. Front Microbiol. doi: 10.3389/fmicb.2016.01705 Google Scholar
  91. Vorobyova E, Soina V, Gorlenko M, Minkovskaya N, Zalinova N, Mamukelashvili A, Gilichinsky DA, Rivkina E, Vishnivetskaya T (1997) The deep cold biosphere: facts and hypothesis. FEMS Microbiol Rev 20:277–290CrossRefGoogle Scholar
  92. Wahlund TM, Woese CR, Castenholz RW, Madigan MT (1991) A thermophilic green sulfur bacterium from New Zealand hot springs, Chlorobium tepidum, nov. sp. Arch Microbiol 156:81–90CrossRefGoogle Scholar
  93. Williams KP, Gillespie JJ, Bruno WSS, Nordberg EK, Snyder EE, Shallom JM, Dickerman AW (2010) Phylogeny of Gammaproteobacteria. J Bacteriol 192:2305–2314CrossRefPubMedPubMedCentralGoogle Scholar
  94. Wu L, Wen C, Qin Y, Yin H, Tu Q, Van Nostrand JD, Yuan T, Yuan M, Deng Y, Zhou J (2015) Phasing amplicon sequencing on Illumina Miseq for robust environmental microbial community analysis. BMC Microbiol 15:125. doi: 10.1186/s12866-015-0450-4 CrossRefPubMedPubMedCentralGoogle Scholar
  95. Yang B, Wang Y, Qian P-Y (2016) Sensitivity and correlation of hypervariable regions in 16S rRNA genes in phylogenetic analysis. BMC Bioinform 17:135. doi: 10.1186/s12859-016-0992-y CrossRefGoogle Scholar
  96. Yumoto I, Kusano T, Shingyo T, Nodasaka Y, Matsuyama H, Okuyama H (2001) Assignment of Pseudomonas sp. strain E-3 to Pseudomonas psychrophila sp. nov., a new facultatively psychrophilic bacterium. Extremophiles 5:343–349CrossRefPubMedGoogle Scholar
  97. Zhou J, Bruns MA, Tiedje JM (1996) DNA recovery from soils of diverse composition. Appl Environ Microbiol 62:316–322PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Japan KK 2017

Authors and Affiliations

  • Michael T. Madigan
    • 1
  • Megan L. Kempher
    • 1
    • 2
  • Kelly S. Bender
    • 1
  • Paul Sullivan
    • 3
  • W. Matthew Sattley
    • 4
  • Alice C. Dohnalkova
    • 5
  • Samantha B. Joye
    • 6
  1. 1.Department of MicrobiologySouthern Illinois UniversityCarbondaleUSA
  2. 2.Department of Microbiology and Plant BiologyUniversity of OklahomaNormanUSA
  3. 3.United States Antarctic ProgramAmundsen-Scott StationAntarctica
  4. 4.Division of Natural SciencesIndiana Wesleyan UniversityMarionUSA
  5. 5.Pacific Northwest National LaboratoryRichlandUSA
  6. 6.Department of Marine SciencesUniversity of GeorgiaAthensUSA

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