Psychrophiles: Genetics, Genomics, Evolution

  • Federico M. Lauro
  • Michelle A. Allen
  • David Wilkins
  • Timothy J. Williams
  • Ricardo Cavicchioli


From the deepest depths of the ocean to the highest alpine peaks of the mountains, from the darkness of subterranean caves to the intense radiation of the upper atmosphere, and from the Northern to the Southern polar extremes, over two thirds of the Earth’s biosphere is dominated by cold habitats. In these cold zones, psychrophilic microorganisms thrive, actively metabolizing at temperatures as low as –20°C, surviving at –45°C (Margesin and Schinner 1999; Feller and Gerday 2003; Cavicchioli 2006) and in the process driving critical global biogeochemical cycles. Yet, despite the fundamental role that these organisms play within the cold biosphere, relatively little is known about their identity, their physiology, how they have evolved, and the biogeochemical processes they perform.

The classic definition of the term, psychrophile, which derives from the Greek words ψυχρος (psukhros, cold) and φιλειν (philein, to love), is for an organism with an optimal growth temperature (T


Protein Code Gene tRNA Gene Cold Shock Cold Adaptation rRNA Operon 


  1. Allen MA et al (2009) The genome sequence of the psychrophilic archaeon, Methanococcoides burtonii: the role of genome evolution in cold adaptation. ISME J 3(9):1012–1035PubMedCrossRefGoogle Scholar
  2. Bada JL, Lazcano A (2002) Some like it hot, but not the first biomolecules. Science 296:1983–1982CrossRefGoogle Scholar
  3. Bakermans C et al (2006) Psychrobacter cryohalolentis sp. nov. and Psychrobacter arcticus sp. nov., isolated from Siberian permafrost. Int J Syst Evol Microbiol 56(6):1285–1291PubMedCrossRefGoogle Scholar
  4. Bakermans C, Tollaksen SL, Giometti CS, Wilkerson C, Tiedje JM, Thomashow MF (2007) Proteomic analysis of Psychrobacter cryohalolentis K5 during growth at subzero temperatures. Extremophiles 11(2):343–354PubMedCrossRefGoogle Scholar
  5. Berger F, Morellet N, Menu F, Potier P (1996) Cold shock and cold acclimation proteins in the psychrotrophic bacterium Arthrobacter globiformis SI55. J Bacteriol 178(11):2999–3007PubMedGoogle Scholar
  6. Bergholz PW, Bakermans C, Tiedje JM (2009) Psychrobacter arcticus 273–4 uses resource efficiency and molecular motion adaptations for subzero temperature growth. J Bacteriol 191(7):2340PubMedCrossRefGoogle Scholar
  7. Burg D, Lauro FM, Williams T, Raftery M, Guilhaus M, Cavicchioli R (2010) Analyzing the hydrophobic proteome of the Antarctic archaeon Methanococcoides burtonii using differential solubility fractionation. J Proteome Res 9(2):664–676.PubMedCrossRefGoogle Scholar
  8. Campanaro S, Williams TJ, De Francisci D, Treu L, Lauro FM, Cavicchioli R (2010) Temperature-dependent global gene expression in the Antarctic archaeon, Methanococcoides burtonii. Environmental Microbiology (in press, accepted Sept 20)Google Scholar
  9. Cavicchioli R (2006) Cold adapted archaea. Nat Rev Microbiol 4:331–343PubMedCrossRefGoogle Scholar
  10. Cavicchioli R (2007) Antarctic metagenomics. Microbiol Austr 28:98–103Google Scholar
  11. Dalluge JJ, Hamamoto T, Horikoshi K, Morita RY, Stetter KO, McCloskey JA (1997) Posttranscriptional modification of tRNA in psychrophilic bacteria. J Bacteriol 179:1918–1923PubMedGoogle Scholar
  12. Duchaud E et al (2007) Complete genome sequence of the fish pathogen Flavobacterium psychrophilum. Nat Biotechnol 25(7):763–769PubMedCrossRefGoogle Scholar
  13. Feller G, Gerday C (2003) Psychrophilic enzymes: hot topics in cold adaptation. Nature Rev Microbiol 1:200–208CrossRefGoogle Scholar
  14. Franzmann PD et al (1997) Methanogenium frigidum sp. nov., a psychrophilic, H2-using methanogen from Ace Lake, Antarctica. Int J Syst Bacteriol 47(4): 1068–1072PubMedCrossRefGoogle Scholar
  15. Gao H, Yang ZK, Wu L, Thompson DK, Zhou J (2006) Global transcriptome analysis of the cold shock response of Shewanella oneidensis MR-1 and mutational analysis of its classical cold shock proteins. J Bacteriol 188(12):4560PubMedCrossRefGoogle Scholar
  16. Giaquinto L, Curmi PMG, Siddiqui KS, Poljak A, DeLong E, DasSarma S, Cavicchioli R (2007) The structure and function of cold shock proteins in archaea. J Bacteriol 189:5738–5748PubMedCrossRefGoogle Scholar
  17. Gibson JAE, Miller MR, Davies NW, Neill GP, Nichols DS, Volkman JK (2005) Unsaturated diether lipids in the psychrotrophic archaeon Halorubrum lacusprofundi. Syst Appl Microbiol 28(1):19–26PubMedCrossRefGoogle Scholar
  18. Goodchild A, Saunders NFW, Ertan H, Raftery M, Guilhaus M, Curmi PMG, Cavicchioli R (2004a) A proteomic determination of cold adaptation in the Antarctic archaeon, Methanococcoides burtonii. Mol Microbiol 53(1):309–321PubMedCrossRefGoogle Scholar
  19. Goodchild A, Raftery M, Saunders NFW, Guilhaus M, Cavicchioli R (2004b) Biology of the cold adapted archaeon, Methanococcoides burtonii determined by proteomics using liquid chromatography-tandem mass spectrometry. J Proteome Res 3(6):1164–1176PubMedCrossRefGoogle Scholar
  20. Goodchild A, Raftery M, Saunders NFW, Guilhaus M, Cavicchioli R (2005) Cold adaptation of the Antarctic archaeon. Methanococcoides burtonii assessed by proteomics using ICAT. J Proteome Res 4(2):473–480PubMedCrossRefGoogle Scholar
  21. Hallam SJ et al (2006) Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proc Natl Acad Sci 103(48):18296–18301PubMedCrossRefGoogle Scholar
  22. Hjerde E et al (2008) The genome sequence of the fish pathogen Aliivibrio salmonicida strain LFI1238 shows extensive evidence of gene decay. BMC Genomics 9(1):616PubMedCrossRefGoogle Scholar
  23. Hou S et al (2004) Genome sequence of the deep-sea gamma-proteobacterium Idiomarina loihiensis reveals amino acid fermentation as a source of carbon and energy. Proc Natl Acad Sci USA 101(52):18036–18041PubMedCrossRefGoogle Scholar
  24. Jiang W, Hou Y, Inouye M (1997) CspA, the major cold-shock protein of Escherichia coli, is an RNA chaperone. J Biol Chem 272(1):196PubMedCrossRefGoogle Scholar
  25. Kawamoto J, Kurihara T, Kitagawa M, Kato I, Esaki N (2007) Proteomic studies of an Antarctic cold-adapted bacterium, Shewanella livingstonensis Ac10, for global identification of cold-inducible proteins. Extremophiles 11(6):819–826Google Scholar
  26. Kim JF et al (2008) Complete genome sequence of Leuconostoc citreum KM20. J Bacteriol 190(8):3093–3094PubMedCrossRefGoogle Scholar
  27. Kurihara T, Esaki N (2008) Proteomic studies of psychrophilic microorganisms. In: Margesin R, Schinner F, Marx J-C, Gerday C (eds) Psychrophiles: from Biodiversity to Biotechnology, Springer Verlag, Berlin Heidelberg. pp 333–344CrossRefGoogle Scholar
  28. Lim J, Thomas T, Cavicchioli R (2000) Low temperature regulated DEAD-box RNA helicase from the Antarctic archaeon Methanococcoides burtonii. J Mol Biol 297:553–567PubMedCrossRefGoogle Scholar
  29. Margesin R, Schinner F (1999) Cold-adapted organisms – ecology, physiology, enzymology and molecular biology. Springer, BerlinGoogle Scholar
  30. Medigue C et al (2005) Coping with cold: the genome of the versatile marine Antarctica bacterium Pseudoalteromonas haloplanktis TAC125. Genome Res 15(10):1325–1335PubMedCrossRefGoogle Scholar
  31. Methe BA et al (2005) The psychrophilic lifestyle as revealed by the genome sequence of Colwellia psychrerythraea 34H through genomic and proteomic analyses. Proc Natl Acad Sci USA 102(31):10913–10918PubMedCrossRefGoogle Scholar
  32. Murray AE, Grzymski JJ (2007) Diversity and genomics of Antarctic marine micro-organisms. Philos Trans R Soc Lond B Biol Sci 362:2259–2271PubMedCrossRefGoogle Scholar
  33. Nichols DS, Miller MR, Davies NW, Goodchild A, Raftery M, Cavicchioli R (2004) Cold adaptation in the Antarctic archaeon Methanococcoides burtonii involves membrane lipid unsaturation. J Bacteriol 186(24):8508–8515PubMedCrossRefGoogle Scholar
  34. Noon KR, Guymon R, Crain PF, McCloskey JA, Thomm M, Lim J, Cavicchioli R (2003) Influence of temperature on tRNA modification in Archaea: Methanococcoides burtonii (Topt 23°C) and Stetteria hydrogenophila (Topt 90°C). J Bacteriol 185:5483–5490PubMedCrossRefGoogle Scholar
  35. Preston CM et al (1996) A psychrophilic crenarchaeon inhabits a marine sponge: Cenarchaeum symbiosum gen. nov., sp. nov. Proc Natl Acad Sci USA 93(13):6241–6246PubMedCrossRefGoogle Scholar
  36. Price B (2009) Microbial genesis, life and death in glacial ice. Can J Microbiol 55:1–11PubMedCrossRefGoogle Scholar
  37. Qiu Y, Kathariou S, Lubman DM (2006) Proteomic analysis of cold adaptation in a Siberian permafrost bacterium-Exiguobacterium sibiricum 255–15 by two-dimensional liquid separation coupled with mass spectrometry. Proteomics 6(19):5221–5233PubMedCrossRefGoogle Scholar
  38. Rabus R, Bruchert V, Amann J, Konneke M (2002) Physiological response to temperature changes of the marine, sulfate-reducing bacterium Desulfobacterium autotrophicum. FEMS Microbiol Ecol 42:409–417PubMedCrossRefGoogle Scholar
  39. Rabus R et al (2004) The genome of Desulfotalea psychrophila, a sulfate-reducing bacterium from permanently cold Arctic sediments. Environ Microbiol 6(9):887–902PubMedCrossRefGoogle Scholar
  40. Reith M et al (2008) The genome of Aeromonas salmonicida subsp. salmonicida A449: insights into the evolution of a fish pathogen. BMC Genomics 9(1):427PubMedCrossRefGoogle Scholar
  41. Riley M et al (2008) Genomics of an extreme psychrophile. Psychromonas ingrahamii. BMC Genomics 9(1):210PubMedCrossRefGoogle Scholar
  42. Risso C et al (2009) Genome-scale comparison and constraint-based metabolic reconstruction of the facultative anaerobic Fe(III)-reducer Rhodoferax ferrireducens. BMC Genomics 10(1):447PubMedCrossRefGoogle Scholar
  43. Rodrigues DF, Ivanova N, He Z, Huebner M, Zhou J, Tiedje JM (2008) Architecture of thermal adaptation in an Exiguobacterium sibiricum strain isolated from 3 million year old permafrost: a genome and transcriptome approach. BMC Genomics 9(1):547PubMedCrossRefGoogle Scholar
  44. Russell NJ (2008) Membrane components and cold sensing. psychrophiles: from biodiversity to biotechnology. Springer, Berlin, pp 177–190CrossRefGoogle Scholar
  45. Ting L, Williams TJ, Cowley MJ, Lauro FM, Guilhaus M, Raftery MJ, Cavicchioli R (2010) Cold adaptation in the marine bacterium, Sphingopyxis alaskensis assessed using quantitative proteomics. Environmental Microbiology doi:10.1111/j.1462-2920.2010.02235.xGoogle Scholar
  46. Saunders NFW, Ng C, Raftery M, Guilhaus M, Goodchild A, Cavicchioli R (2006) Proteomic and computational analysis of secreted proteins with type I signal peptides from the Antarctic archaeon Methanococcoides burtonii. J Proteome Res 5:2457–2464PubMedCrossRefGoogle Scholar
  47. Saunders NFW et al (2003) Mechanisms of thermal adaptation revealed from the genomes of the Antarctic archaea Methanogenium frigidum and Methanococcoides burtonii. Genome Res 13:1580–1588PubMedCrossRefGoogle Scholar
  48. Saunders NFW, Goodchild A, Raftery M, Guilhaus M, Curmi PMG, Cavicchioli R (2005) Predicted roles for hypothetical proteins in the low-temperature expressed proteome of the Antarctic archaeon Methanococcoides burtonii. J Proteome Res 4(2):464–472PubMedCrossRefGoogle Scholar
  49. Seo JB, Kim HS, Jung GY, Nam MH, Chung JH, Kim JY, Yoo JS, Kim CW, Kwon O (2004) Psychrophilicity of Bacillus psychrosaccharolyticus: a proteomic study. Proteomics 4(11):3654PubMedCrossRefGoogle Scholar
  50. Suzuki Y, Haruki M, Takano K, Morikawa M, Kanaya S (2004) Possible involvement of an FKBP family member protein from a psychrotrophic bacterium Shewanella sp. SIB1 in cold-adaptation. Eur J Biochem 271(7):1372PubMedCrossRefGoogle Scholar
  51. Tasara T, Stephan R (2006) Cold stress tolerance of Listeria monocytogenes: a review of molecular adaptive mechanisms and food safety implications. J Food Prot 69(6):1473–84PubMedGoogle Scholar
  52. Ting L, Cowley MJ, Hoon SL, Guilhaus M, Raftery MJ, Cavicchioli R (2009) Normalization and statistical analysis of quantitative proteomics data generated by metabolic labeling. Mol Cell Proteomics 8:2227–2242PubMedCrossRefGoogle Scholar
  53. Vezzi A et al (2005) Life at depth: photobacterium profundum genome sequence and expression analysis. Science 307(5714):1459–1461PubMedCrossRefGoogle Scholar
  54. Wang F et al (2007) A novel filamentous phage from the deep-sea bacterium Shewanella piezotolerans WP3 Is induced at low temperature. J Bacteriol 189(19):7151–7153PubMedCrossRefGoogle Scholar
  55. Wang F et al (2009) Role and regulation of fatty acid biosynthesis in the response of Shewanella piezotolerans WP3 to different temperatures and pressures. J Bacteriol 191(8):2574–2584PubMedCrossRefGoogle Scholar
  56. Wang F et al (2010) Environmental adaptation: genomic analysis of the piezotolerant and psychrotolerant deep-sea iron reducing bacterium Shewanella piezotolerans WP3. PLoS One 3(4):e1937, 9(2):640–652CrossRefGoogle Scholar
  57. Weiner RM et al (2010) Complete genome sequence of the complex carbohydrate-degrading marine bacterium, Saccharophagus degradans strain 2–40T. PLoS Genet 4(5):e1000087, 9(2):653–663CrossRefGoogle Scholar
  58. Williams T, Burg D, Raftery M, Poljak A, Guilhaus M, Pilak O, Cavicchioli R (2010a) A global proteomic analysis of the insoluble, soluble and supernatant fractions of the psychrophilic archaeon Methanococcoides burtonii Part I: the effect of growth temperature. J Proteome Res 9(2):640–652PubMedCrossRefGoogle Scholar
  59. Williams T, Burg D, Ertan H, Raftery M, Poljak A, Guilhaus M, Cavicchioli R (2010b) A global proteomic analysis of the insoluble, soluble and supernatant fractions of the psychrophilic archaeon Methanococcoides burtonii Part II: The effect of different methylated growth substrates. J Proteome Res 9(2):653–663PubMedCrossRefGoogle Scholar
  60. Yoshimune K, Galkin A, Kulakova L, Yoshimura T, Esaki N (2005) Cold-active DnaK of an Antarctic psychrotroph Shewanella sp. Ac10 supporting the growth of dnaK-null mutant of Escherichia coli at cold temperatures. Extremophiles 9(2):145–150Google Scholar
  61. Zheng S, Ponder MA, Shih JYJ, Tiedje JM, Thomashow MF, Lubman DM (2007) A proteomic analysis of Psychrobacter arcticus 273–4 adaptation to low temperature and salinity using a 2-D liquid mapping approach. Electrophoresis 28(3):467–488PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2011

Authors and Affiliations

  • Federico M. Lauro
    • 1
  • Michelle A. Allen
    • 1
  • David Wilkins
    • 1
  • Timothy J. Williams
    • 1
  • Ricardo Cavicchioli
    • 1
  1. 1.School of Biotechnology and Biomolecular SciencesUniversity of New South WalesSydneyAustralia

Personalised recommendations