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Determining the Limits of Microbial Life at Subzero Temperatures

  • Corien BakermansEmail author
Chapter

Abstract

Determining the low-temperature limit of life is a challenge complicated by the reduced availability of liquid water as water freezes and by the low rates of diffusion and reaction brought on by low temperatures. And yet, many microorganisms are able to grow at temperatures of −2 °C to 4 °C and many also survive much lower temperatures of −80 °C to −196 °C. A variety of approaches for determining the low-temperature limit of life are examined in this chapter and relevant data are reported. Theoretical approaches investigate the presence of liquid water at temperatures below 0 °C as well as universal laws of biology which may inform the low-temperature limits of life. Both reductionist and holistic experimental approaches reveal the known limits of cellular components, processes, and whole cells with multiple lines of evidence suggesting that cell reproduction occurs down to temperatures of −20 °C. Finally, observational studies of microorganisms in low-temperature environments of the polar regions expose how the low-temperature limit of life is entangled with other factors (perhaps inextricably) and that time at low temperatures may limit evolution and cold adaptation of terrestrial life.

References

  1. Amato P, Christner BC (2009) Energy metabolism response to low-temperature and frozen conditions in Psychrobacter cryohalolentis. Appl Environ Microbiol 75(3):711–718. doi: 10.1128/aem.02193-08 CrossRefPubMedGoogle Scholar
  2. Amato P, Doyle SM, Battista JR, Christner BC (2010) Implications of subzero metabolic activity on long-term microbial survival in terrestrial and extraterrestrial permafrost. Astrobiology 10(8):789–798. doi: 10.1089/ast.2010.0477 CrossRefPubMedGoogle Scholar
  3. Arcus VL, Prentice EJ, Hobbs JK, Mulholland AJ, Van der Kamp MW, Pudney CR, Parker EJ, Schipper LA (2016) On the temperature dependence of enzyme-catalyzed rates. Biochemistry (Moscow) 55(12):1681–1688. doi: 10.1021/acs.biochem.5b01094 CrossRefGoogle Scholar
  4. Bakermans C, Skidmore M (2011a) Microbial metabolism in ice and brine at -5°C. Environ Microbiol 13(8):2269–2278. doi: 10.1111/j.1462-2920.2011.02485.x CrossRefPubMedGoogle Scholar
  5. Bakermans C, Skidmore ML (2011b) Microbial respiration in ice at subzero temperatures (-4 to -33°C). Environ Microbiol Rep 3(6):774–782. doi: 10.1111/j.1758-2229.2011.00298.x CrossRefPubMedGoogle 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(4):321–326CrossRefPubMedGoogle Scholar
  7. Bakermans C, Ayala-del-Río HL, Ponder MA, Vishnivetskaya T, Gilichinsky D, Thomashow MF, Tiedje JM (2006) Psychrobacter cryohalolentis sp. nov. and Psychrobacter arcticus sp. nov. isolated from Siberian permafrost. Int J Syst Evol Microbiol 56(6):1285–1291CrossRefPubMedGoogle Scholar
  8. Barabasi AL, Oltvai ZN (2004) Network biology: understanding the cell’s functional organization. Nat Rev Genet 5(2):101–U115. doi: 10.1038/nrg1272 CrossRefPubMedGoogle Scholar
  9. Barrett P (2003) Palaeoclimatology – Cooling a continent. Nature 421(6920):221–223CrossRefPubMedGoogle Scholar
  10. Beaty D, Buxbaum K, Meyer M, Barlow N, Boynton W, Clark B, Deming J, Doran PT, Edgett K, Hancock S, Head J, Hecht M, Hipkin V, Kieft T, Mancinelli R, McDonald E, McKay C, Mellon M, Newsom H, Ori G, Paige D, Schuerger AC, Sogin M, Spry JA, Steele A, Tanaka K, Voytek M (2006) Findings of the Mars special regions science analysis group. Astrobiology 6(5):677–732CrossRefGoogle Scholar
  11. Biddle JF, Lipp JS, Lever MA, Lloyd KG, Sorensen KB, Anderson R, Fredricks HF, Elvert M, Kelly TJ, Schrag DP, Sogin ML, Brenchley JE, Teske A, House CH, Hinrichs KU (2006) Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru. Proc Natl Acad Sci USA 103(10):3846–3851. doi: 10.1073/pnas.0600035103 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Bidle KD, Lee S, Marchant DR, Falkowski PG (2007) Fossil genes and microbes in the oldest ice on Earth. Proc Natl Acad Sci USA 104(33):13455–13460CrossRefPubMedPubMedCentralGoogle Scholar
  13. Bragger JM, Dunn RV, Daniel RM (2000) Enzyme activity down to −100°C. Biochim Biophys Acta – Protein Struct Mol Enzymol 1480(1–2):278–282. doi: 10.1016/S0167-4838(00)00081-9 CrossRefGoogle Scholar
  14. Breezee J, Cady N, Staley JT (2004) Subfreezing growth of the sea ice bacterium “Psychromonas ingrahamii”. Microb Ecol 47(3):300–304CrossRefPubMedGoogle Scholar
  15. Chong C-W, Pearce DA, Convey P (2015) Emerging spatial patterns in Antarctic prokaryotes. Front Microbiol 6(1058). doi: 10.3389/fmicb.2015.01058
  16. Chown SL, Clarke A, Fraser CI, Cary SC, Moon KL, McGeoch MA (2015) The changing form of Antarctic biodiversity. Nature 522(7557):427–434. doi: 10.1038/nature14505 CrossRefGoogle Scholar
  17. Cipolla A, Delbrassine F, Da Lage JL, Feller G (2012) Temperature adaptations in psychrophilic, mesophilic and thermophilic chloride-dependent alpha-amylases. Biochimie 94(9):1943–1950. doi: 10.1016/j.biochi.2012.05.013 CrossRefPubMedGoogle Scholar
  18. Clarke A, Morris GJ, Fonseca F, Murray BJ, Acton E, Price HC (2013) A low temperature limit for life on Earth. PLoS ONE 8(6):e66207. doi: 10.1371/journal.pone.0066207 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Collins MA, Buick RK (1989) Effect of temperature on the spoilage of stored peas by Rhodotorula glutinis. Food Microbiol (London) 6(3):135–142. doi: 10.1016/s0740-0020(89)80021-8 CrossRefGoogle Scholar
  20. Corkrey R, McMeekin TA, Bowman JP, Ratkowsky DA, Olley J, Ross T (2016) The biokinetic spectrum for temperature. PLoS ONE 11(4):e0153343. doi: 10.1371/journal.pone.0153343 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Davies PCW, Walker SI (2016) The hidden simplicity of biology. Rep Prog Phys 79(10):18. doi: 10.1088/0034-4885/79/10/102601 CrossRefGoogle Scholar
  22. Dieser M, Battista JR, Christner BC (2013) DNA double-strand break repair at -15 degrees C. Appl Environ Microbiol 79(24):7662–7668. doi: 10.1128/aem.02845-13 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Dolev MB, Braslavsky I, Davies PL (2016) Ice-binding proteins and their function. Annu Rev Biochem 85(1):515–542. doi: 10.1146/annurev-biochem-060815-014546 CrossRefPubMedGoogle Scholar
  24. England JL (2013) Statistical physics of self-replication. J Chem Phys 139(12):121923. doi: 10.1063/1.4818538 CrossRefPubMedGoogle Scholar
  25. Ewing SA, O’Donnell JA, Aiken GR, Butler K, Butman D, Windham-Myers L, Kanevskiy MZ (2015) Long-term anoxia and release of ancient, labile carbon upon thaw of Pleistocene permafrost. Geophys Res Lett 42(24):10730–10738. doi: 10.1002/2015gl066296 CrossRefGoogle Scholar
  26. Feller G (2013) Psychrophilic enzymes: from folding to function and biotechnology. Scientifica (Cairo). doi: 10.1155/2013/512840 Google Scholar
  27. Fonseca F, Marin M, Morris GJ (2006) Stabilization of frozen Lactobacillus delbrueckii subsp. bulgaricus in glycerol suspensions: freezing kinetics and storage temperature effects. Appl Environ Microbiol 72(10):6474–6482. doi: 10.1128/aem.00998-06 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Fonseca F, Meneghel J, Cenard S, Passot S, Morris GJ (2016) Determination of intracellular vitrification temperatures for unicellular microorganisms under conditions relevant for cryopreservation. PLoS ONE 11(4):e0152939. doi: 10.1371/journal.pone.0152939 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Froese DG, Westgate JA, Reyes AV, Enkin RJ, Preece SJ (2008) Ancient permafrost and a future, warmer Arctic. Science 321(5896):1648–1648. doi: 10.1126/science.1157525 CrossRefPubMedGoogle Scholar
  30. Gautier J, Passot S, Pénicaud C, Guillemin H, Cenard S, Lieben P, Fonseca F (2013) A low membrane lipid phase transition temperature is associated with a high cryotolerance of Lactobacillus delbrueckii subspecies bulgaricus CFL1. J Dairy Sci 96(9):5591–5602. doi: 10.3168/jds.2013-6802 CrossRefPubMedGoogle Scholar
  31. Gerday C (2011) Life at the extremes of temperature. In: Bacterial stress responses, 2nd edn. ASM Press, Washington, DCGoogle Scholar
  32. Gerday C (2013) Psychrophily and catalysis. Biology (Basel) 2(2):719–741. doi: 10.3390/biology2020719 Google Scholar
  33. Gilichinsky D, Wagener S (1995) Microbial life in permafrost: a historical review. Permafrost Periglac 6:243–250CrossRefGoogle Scholar
  34. Gilichinsky DA, Wilson GS, Friedmann EI, Mckay CP, Sletten RS, Rivkina EM, Vishnivetskaya TA, Erokhina LG, Ivanushkina NE, Kochkina GA, Shcherbakova VA, Soina VS, Spirina EV, Vorobyova EA, Fyodorov-Davydov DG, Hallet B, Ozerskaya SM, Sorokovikov VA, Laurinavichyus KS, Shatilovich AV, Chanton JP, Ostroumov VE, Tiedje JM (2007) Microbial populations in Antarctic permafrost: biodiversity, state, age, and implication for astrobiology. Astrobiology 7(2):275–311CrossRefPubMedGoogle Scholar
  35. Goldstein RA (2007) Amino-acid interactions in psychrophiles, mesophiles, thermophiles, and hyperthermophiles: insights from the quasi-chemical approximation. Protein Sci 16(9):1887–1895. doi: 10.1110/ps.072947007 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Goordial J, Davila A, Greer CW, Cannam R, DiRuggiero J, McKay CP, Whyte LG (2016a) Comparative activity and functional ecology of permafrost soils and lithic niches in a hyper-arid polar desert. Environ Microbiol. doi: 10.1111/1462-2920.13353 PubMedGoogle Scholar
  37. Goordial J, Davila A, Lacelle D, Pollard W, Marinova MM, Greer CW, DiRuggiero J, McKay CP, Whyte LG (2016b) Nearing the cold-arid limits of microbial life in permafrost of an upper dry valley, Antarctica. ISME J 10(7):1613–1624. doi: 10.1038/ismej.2015.239 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Gruebele M, Thirumalai D (2013) Perspective: reaches of chemical physics in biology. J Chem Phys 139(12):121701. doi: 10.1063/1.4820139 CrossRefPubMedGoogle Scholar
  39. Guendouzi A, Mekelleche SM (2012) Prediction of the melting points of fatty acids from computed molecular descriptors: a quantitative structure-property relationship study. Chem Phys Lipids 165(1):1–6. doi: 10.1016/j.chemphyslip.2011.10.001 CrossRefPubMedGoogle Scholar
  40. Hamamoto T, Takata N, Kudo T, Horikoshi K (1995) Characteristic presence of polyunsaturated fatty acids in marine psychrophilic vibrios. FEMS Microbiol Lett 129(1):51–56CrossRefGoogle Scholar
  41. Hassan N, Rafiq M, Hayat M, Shah AA, Hasan F (2016) Psychrophilic and psychrotrophic fungi: a comprehensive review. Rev Environ Sci Bio/Technol 15(2):147–172. doi: 10.1007/s11157-016-9395-9 CrossRefGoogle Scholar
  42. Helland R, Larsen RL, Asgeirsson B (2009) The 1.4 angstrom crystal structure of the large and cold-active Vibrio sp. alkaline phosphatase. Biochim Biophys Acta – Proteins Proteom 1794(2):297–308. doi: 10.1016/j.bbapap.2008.09.020 CrossRefGoogle Scholar
  43. Hoehler TM, Jorgensen BB (2013) Microbial life under extreme energy limitation. Nat Rev Microbiol 11(2):83–94. doi: 10.1038/nrmicro2939 CrossRefPubMedGoogle Scholar
  44. Johnson S, Hebsgaard M, Christensen T, Mastepanov M, Nielsen R, Munch K, Brand T, Gilbert M, Zuber M, Bunce M, Ronn R, Gilichinsky D, Froese D, Willerslev E (2007) Ancient bacteria show evidence of DNA repair. Proc Natl Acad Sci 104(36):14401–14405CrossRefPubMedPubMedCentralGoogle Scholar
  45. Junge K, Eicken H, Swanson BD, Deming JW (2006) Bacterial incorporation of leucine into protein down to -20°C with evidence for potential activity in sub-eutectic saline ice formations. Cryobiology 52(3):417–429CrossRefPubMedGoogle Scholar
  46. Lamarche-Gagnon G, Comery R, Greer CW, Whyte LG (2015) Evidence of in situ microbial activity and sulphidogenesis in perennially sub-0 degrees C and hypersaline sediments of a high Arctic permafrost spring. Extremophiles 19(1):1–15. doi: 10.1007/s00792-014-0703-4 CrossRefPubMedGoogle Scholar
  47. Lever MA, Rogers KL, Lloyd KG, Overmann J, Schink B, Thauer RK, Hoehler TM, Jorgensen BB (2015) Life under extreme energy limitation: a synthesis of laboratory- and field-based investigations. FEMS Microbiol Rev 39(5):688–728. doi: 10.1093/femsre/fuv020 CrossRefPubMedGoogle Scholar
  48. Lomstein BA, Langerhuus AT, D’Hondt S, Jorgensen BB, Spivack AJ (2012) Endospore abundance, microbial growth and necromass turnover in deep sub-seafloor sediment. Nature 484(7392):101–104. doi: 10.1038/nature10905 CrossRefPubMedGoogle Scholar
  49. Mangelsdorf K, Finsel E, Liebner S, Wagner D (2009) Temperature adaptation of microbial communities in different horizons of Siberian permafrost-affected soils from the Lena Delta. Chemie Erde Geochem 69(2):169–182. doi: 10.1016/j.chemer.2009.02.001 CrossRefGoogle Scholar
  50. Marx JC, Collins T, D’Amico S, Feller G, Gerday C (2007) Cold-adapted enzymes from marine Antarctic microorganisms. Mar Biotechnol (NY) 9(3):293–304. doi: 10.1007/s10126-006-6103-8 CrossRefGoogle Scholar
  51. Mazur P (2004) Principles of cryobiology. In: Fuller BJ, Lane N, Benson EE (eds) Life in the frozen state. CRC Press, Boca Raton, FL, pp 3–65. doi: 10.1201/9780203647073.ch1 CrossRefGoogle Scholar
  52. Miao LL, Hou YJ, Fan HX, Qu J, Qi C, Liu Y, Li DF, Liu ZP (2016) Molecular structural basis for the cold adaptedness of the psychrophilic beta-glucosidase BglU in Micrococcus antarcticus. Appl Environ Microbiol 82(7):2021–2030. doi: 10.1128/aem.03158-15 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Miteva V, Sowers T, Brenchley J (2007) Production of N2O by ammonia oxidizing bacteria at subfreezing temperatures as a model for assessing the N2O anolmalies in the Vostok Ice Core. Geomicrobiol J 24:451–459CrossRefGoogle Scholar
  54. Morono Y, Terada T, Nishizawa M, Ito M, Hillion F, Takahata N, Sano Y, Inagaki F (2011) Carbon and nitrogen assimilation in deep subseafloor microbial cells. Proc Natl Acad Sci 108(45):18295–18300. doi: 10.1073/pnas.1107763108 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Murray AE, Kenig F, Fritsen CH, McKay CP, Cawley KM, Edwards R, Kuhn E, McKnight DM, Ostrom NE, Peng V, Ponce A, Priscu JC, Samarkin V, Townsend AT, Wagh P, Young SA, Yung PT, Doran PT (2012) Microbial life at −13 °C in the brine of an ice-sealed Antarctic lake. Proc Natl Acad Sci 109(50):20626–20631. doi: 10.1073/pnas.1208607109 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Mykytczuk NC, Trevors JT, Foote SJ, Leduc LG, Ferroni GD, Twine SM (2011) Proteomic insights into cold adaptation of psychrotrophic and mesophilic Acidithiobacillus ferrooxidans strains. Antonie Van Leeuwenhoek 100(2):259–277. doi: 10.1007/s10482-011-9584-z CrossRefPubMedGoogle Scholar
  57. Mykytczuk NCS, Wilhelm R, Whyte LG (2012) Planococcus halocryophilus sp. nov.; an extreme subzero species from high Arctic permafrost. Int J Syst Evol Microbiol 62(8):1937–1944. doi: 10.1099/ijs.0.035782-0 CrossRefPubMedGoogle Scholar
  58. Mykytczuk NCS, Foote SJ, Omelon CR, Southam G, Greer CW, Whyte LG (2013) Bacterial growth at -15C; molecular insights from the permafrost bacterium Planococcus halocryophilus Or1. ISME J 7(6):1211–1226. doi: 10.1038/ismej.2013.8 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Mykytczuk NCS, Lawrence JR, Omelon CR, Southam G, Whyte LG (2016) Microscopic characterization of the bacterial cell envelope of Planococcus halocryophilus Or1 during subzero growth at −15 °C. Pol Biol 39(4):701–712. doi: 10.1007/s00300-015-1826-5 CrossRefGoogle Scholar
  60. Nichols DS, Brown JL, Nichols PD, McMeekin TA (1997) Production of eicosapentaenoic and arachidonic acids by an Antarctic bacterium: response to growth temperature. FEMS Microbiol Lett 152(2):349–354. doi: 10.1016/s0378-1097(97)00224-3 CrossRefGoogle Scholar
  61. Niederberger TD, Sohm JA, Gunderson T, Tirindelli J, Capone DG, Carpenter EJ, Cary SC (2015) Carbon-fixation rates and associated microbial communities residing in arid and ephemerally wet Antarctic Dry Valley soils. Front Microbiol 6:9. doi: 10.3389/fmicb.2015.01347 PubMedPubMedCentralGoogle Scholar
  62. Nikrad MP, Kerkhof LJ, Haggblom MM (2016) The subzero microbiome: microbial activity in frozen and thawing soils. FEMS Microbiol Ecol 92(6). doi: 10.1093/femsec/fiw081
  63. Pearce DA (2012) Extremophiles in Antarctica: life at low temperatures. In: Stan-Lotter H, Fendrihan S (eds) Adaption of microbial life to environmental extremes: novel research results and application. Springer, Vienna, pp 87–118. doi: 10.1007/978-3-211-99691-1_5 CrossRefGoogle Scholar
  64. Peters B, Casciotti KL, Samarkin VA, Madigan MT, Schutte CA, Joye SB (2014) Stable isotope analyses of NO2−, NO3−, and N2O in the hypersaline ponds and soils of the McMurdo Dry Valleys, Antarctica. Geochim Cosmochim Acta 135:87–101. doi: 10.1016/j.gca.2014.03.024 CrossRefGoogle Scholar
  65. Price PB (2000) A habitat for psychrophiles in deep Antarctic ice. Proc Natl Acad Sci 97(3):1247–1251CrossRefPubMedPubMedCentralGoogle Scholar
  66. Radde NE, Hutt MT (2016) The physics behind systems biology. EPJ Nonlinear Biomed Phys 4:19. doi: 10.1140/epjnbp/s40366-016-0034-8 CrossRefGoogle Scholar
  67. Rivkina EM, Friedmann EI, McKay CP, Gilichinsky DA (2000) Metabolic activity of permafrost bacteria below the freezing point. Appl Environ Microbiol 66(8):3230–3233CrossRefPubMedPubMedCentralGoogle Scholar
  68. Rivkina E, Shcherbakova V, Laurinavichius K, Petrovskaya L, Krivushin K, Kraev G, Pecheritsina S, Gilichinsky D (2007) Biogeochemistry of methane and methanogenic archaea in permafrost. FEMS Microbiol Ecol 61(1):1–15CrossRefPubMedGoogle Scholar
  69. Rummel JD, Beaty DW, Jones MA, Bakermans C, Barlow NG, Boston PJ, Chevrier VF, Clark BC, de Vera J-PP, Gough RV, Hallsworth JE, Head JW, Hipkin VJ, Kieft TL, McEwen AS, Mellon MT, Mikucki JA, Nicholson WL, Omelon CR, Peterson R, Roden EE, Sherwood Lollar B, Tanaka KL, Viola D, Wray JJ (2014) A new analysis of Mars “special regions”: findings of the second MEPAG special regions science analysis group (SR-SAG2). Astrobiology 14(11):887–968. doi: 10.1089/ast.2014.1227 CrossRefPubMedGoogle Scholar
  70. Russell NJ (2007) Psychrophiles: membrane adaptations. In: Physiology and biochemistry of extremophiles, p 155–164Google Scholar
  71. Russell N (2008) Membrane components and cold sensing. In: Margesin R, Schinner F, Marx J-C, Gerday C (eds) Psychrophiles: from biodiversity to biotechnology. Springer, Berlin, pp 177–190CrossRefGoogle Scholar
  72. Samarkin VA, Madigan MT, Bowles MW, Casciotti KL, Priscu JC, McKay CP, Joye SB (2010) Abiotic nitrous oxide emission from the hypersaline Don Juan Pond in Antarctica. Nat Geosci 3(5):341–344. http://www.nature.com/ngeo/journal/v3/n5/suppinfo/ngeo847_S1.html CrossRefGoogle Scholar
  73. Schaefer K, Jafarov E (2016) A parameterization of respiration in frozen soils based on substrate availability. Biogeosciences 13(7):1991–2001. doi: 10.5194/bg-13-1991-2016 CrossRefGoogle Scholar
  74. Schuur EAG, Bockheim J, Canadell JG, Euskirchen E, Field CB, Goryachkin SV, Hagemann S, Kuhry P, Lafleur PM, Lee H, Mazhitova G, Nelson FE, Rinke A, Romanovsky VE, Shiklomanov N, Tarnocai C, Venevsky S, Vogel JG, Zimov SA (2008) Vulnerability of permafrost carbon to climate change: implications for the global carbon cycle. Bioscience 58(8):701–714. doi: 10.1641/b580807 CrossRefGoogle Scholar
  75. Seki S, Kleinhans FW, Mazur P (2009) Intracellular ice formation in yeast cells vs. cooling rate: predictions from modeling vs. experimental observations by differential scanning calorimetry. Cryobiology 58(2):157–165. doi: 10.1016/j.cryobiol.2008.11.011 CrossRefPubMedGoogle Scholar
  76. Sonan GK, Receveur-Brechot V, Duez C, Aghajari N, Czjzek M, Haser R, Gerday C (2007) The linker region plays a key role in the adaptation to cold of the cellulase from an Antarctic bacterium. Biochem J 407:293–302. doi: 10.1042/bj20070640 CrossRefPubMedPubMedCentralGoogle Scholar
  77. Stevenson A, Burkhardt J, Cockell CS, Cray JA, Dijksterhuis J, Fox-Powell M, Kee TP, Kminek G, McGenity TJ, Timmis KN, Timson DJ, Voytek MA, Westall F, Yakimov MM, Hallsworth JE (2015) Multiplication of microbes below 0.690 water activity: implications for terrestrial and extraterrestrial life. Environ Microbiol 17(2):257–277. doi: 10.1111/1462-2920.12598 CrossRefPubMedGoogle Scholar
  78. Stomeo F, Makhalanyane TP, Valverde A, Pointing SB, Stevens MI, Cary CS, Tuffin MI, Cowan DA (2012) Abiotic factors influence microbial diversity in permanently cold soil horizons of a maritime-associated Antarctic Dry Valley. FEMS Microbiol Ecol 82(2):326–340. doi: 10.1111/j.1574-6941.2012.01360.x CrossRefPubMedGoogle Scholar
  79. Strauss J, Schirrmeister L, Mangelsdorf K, Eichhorn L, Wetterich S, Herzschuh U (2015) Organic-matter quality of deep permafrost carbon – a study from Arctic Siberia. Biogeosciences 12(7):2227–2245. doi: 10.5194/bg-12-2227-2015 CrossRefGoogle Scholar
  80. Taha A, Ahmed RZ, Motoigi T, Watanabe K, Kurosawa N, Okuyama H (2013) Lipids in cold-adapted microorganisms. In: Yumoto I (ed) Cold-adapted microorganisms. Caister Academic Press, WymondhamGoogle Scholar
  81. Tiao G, Lee CK, McDonald IR, Cowan DA, Cary SC (2012) Rapid microbial response to the presence of an ancient relic in the Antarctic Dry Valleys. Nat Commun 3:8. doi: 10.1038/ncomms1645 CrossRefGoogle Scholar
  82. Tuorto SJ, Darias P, McGuinness LR, Panikov N, Zhang T, Haggblom MM, Kerkhof LJ (2014) Bacterial genome replication at subzero temperatures in permafrost. ISME J 8(1):139–149. doi: 10.1038/ismej.2013.140 CrossRefPubMedGoogle Scholar
  83. Vishnivetskaya T, Kathariou S, McGrath J, Gilichinsky D, Tiedje JM (2000) Low-temperature recovery strategies for the isolation of bacteria from ancient permafrost sediments. Extremophiles 4:165–173CrossRefPubMedGoogle Scholar
  84. Vishnivetskaya TA, Petrova MA, Urbance J, Ponder M, Moyer CL, Gilichinsky DA, Tiedje JM (2006) Bacterial community in ancient siberian permafrost as characterized by culture and culture-independent methods. Astrobiology 6(3):400–414CrossRefPubMedGoogle Scholar
  85. Vrielink ASO, Aloi A, Olijve LLC, Voets IK (2016) Interaction of ice binding proteins with ice, water and ions. Biointerphases 11(1):17. doi: 10.1116/1.4939462 Google Scholar
  86. Waldrop MP, Wickland KP, White R, Berhe AA, Harden JW, Romanovsky VE (2010) Molecular investigations into a globally important carbon pool: permafrost-protected carbon in Alaskan soils. Glob Change Biol 16(9):2543–2554. doi: 10.1111/j.1365-2486.2009.02141.x Google Scholar
  87. Wells LE, Deming JW (2006) Modelled and measured dynamics of viruses in Arctic winter sea-ice brines. Environ Microbiol 8(6):1115–1121CrossRefPubMedGoogle Scholar
  88. Williams R, Frausto da Silva J (1996) The natural selection of the chemical elements: the environment and life’s chemistry. Oxford University Press, New York, NYGoogle Scholar
  89. Yoshida K, Hashimoto M, Hori R, Adachi T, Okuyama H, Orikasa Y, Nagamine T, Shimizu S, Ueno A, Morita N (2016) Bacterial long-chain polyunsaturated fatty acids: their biosynthetic genes, functions, and practical use. Mar Drugs 14(5):23. doi: 10.3390/md14050094 CrossRefGoogle Scholar
  90. Yusof NY, Abu Bakar FD, Mahadi NM, Raih MF, Murad AMA (2015) Structure prediction of Fe(II) 2-oxoglutarate dioxygenase from a psychrophilic yeast Glaciozyma antarctica PI12. In: Ahmad A, AbdKarim NH, Hassan NI et al. (eds) 2015 The UKM FST Postgraduate Colloquium. AIP Conference Proceedings, vol 1678. doi: 10.1063/1.4931235

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© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Penn State Altoona, The Pennsylvania State UniversityAltoonaUSA

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