The Challenges of Low Temperature in the Evolution of Bacteria

  • Guido di Prisco
  • Daniela Giordano
  • Roberta Russo
  • Cinzia Verde
Part of the From Pole to Pole book series (POLE)


It is currently recognised that extreme environments, by virtue of their extension and often unique features, are the most important part of the Earth’s biosphere. Their study is still limited and is often hampered by logistic constraints; however, extreme environments are now becoming more and more accessible thanks to technological progress and research on adaptations to extreme conditions.


Extracellular Polymeric Substance High Oxygen Concentration Francisella Tularensis Anabaena Variabilis Psychrophilic Enzyme 
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.



This study is financially supported by the Italian National Programme for Antarctic Research (PNRA). It is in the framework of the SCAR programme Evolution and Biodiversity in the Antarctic (EBA), the project CAREX (Coordination Action for Research Activities on Life in Extreme Environments), European Commission FP7 call ENV.2007. DG and RR acknowledge CNR (for Short-Term Mobility fellowships) and CAREX (for Transfer of Knowledge grants).


  1. Ayala-Del-Río HL, Chain PS, Grzymski JJ, Ponder MA, Ivanova N, Bergholz PW, Di Bartolo G, Hauser L, Land M, Bakermans C, Rodrigues D, Klappenbach J, Zarka D, Larimer F, Richardson P, Murray A, Thomashow M, Tiedje JM (2010) The genome sequence of psychrobacter arcticus 273–4, a psychroactive siberian permafrost bacterium, reveals mechanisms for adaptation to low temperature growth. Appl Environ Microbiol 76:2304–2312CrossRefGoogle Scholar
  2. Carpenter JF, Crowe JH (1988) The mechanism of cryoprotection of proteins by solutes. Cryobiol 25:244–255CrossRefGoogle Scholar
  3. Casanueva A, Tuffin M, Craig C, Cowan DA (2010) Molecular adaptations to psychrophily: the impact of “omic” technologies. Trends Microbiol 18:374–381CrossRefGoogle Scholar
  4. Cavicchioli R, Siddiqui KS, Andrews D, Sowers KR (2002) Low-temperature extremophiles and their applications. Curr Opin Biotech 13:253–261CrossRefGoogle Scholar
  5. Cavicchioli R, Thomas T, Curmi PM (2000) Cold stress response in archaea. Extremophiles 4:321–331CrossRefGoogle Scholar
  6. Chauhan S, Shivaji S (1994) Growth and pigmentation in Sphingobacterium antarcticus, a psychrothrophic bacterium from Antarctica. Polar Biol 15:215–219Google Scholar
  7. Chintalapati S, Kiran MD, Shivaji S (2004) Role of membrane lipid fatty acids in cold adaptation. Cell Mol Biol (Noisy-le-grand) 50:631–642Google Scholar
  8. D’Amico S, Collins T, Marx JC, Feller G, Gerday C (2006) Psychrophilic microorganisms: challenges for life. EMBO Rep 7:385–389CrossRefGoogle Scholar
  9. Deming JW (2002) Psychrophiles and polar regions. Curr Opin Microbiol 5:301–309CrossRefGoogle Scholar
  10. Deming JW, Junge K (2005) Colwellia. In: Staley GT, Benner DJ, Krieg NR, Garrity GM (eds) The proteobacteria, part B, bergey’s manual of systematic bacteriology, vol 2, 2nd edn. Springer, New York, pp 447–454Google Scholar
  11. Duplantis BN, Osusky M, Schmerk CL, Ross DR, Bosio CM, Nano FE (2010) Essential genes from Arctic bacteria used to construct stable, temperature-sensitive bacterial vaccines. Proc Natl Acad Sci USA 107:3456–13460CrossRefGoogle Scholar
  12. Eriksson S, Hurme R, Rhen M (2002) Low temperature sensors in bacteria. Phil Trans R Soc Lond B 357:887–893CrossRefGoogle Scholar
  13. Feller G (2010) Protein stability and enzyme activity at extreme biological temperatures. J Phys Condens Matter 22:323101CrossRefGoogle Scholar
  14. Feller G, Gerday C (2003) Psychrophilic enzymes: hot topics in cold adaptation. Nat Rev Microbiol 1:200–208CrossRefGoogle Scholar
  15. Ferrer M, Chernikova TN, Yakimov M, Timmis KN, Golyshin PN (2003) Chaperonins govern growth of Escherichia coli at low temperatures. Nat Biotechnol 21:1266–1267CrossRefGoogle Scholar
  16. Finkel T (2003) Oxidant signals and oxidative stress. Curr Opin Cell Biol 15:247–254CrossRefGoogle Scholar
  17. Georlette D, Blaise V, Collins T, D’Amico S, Gratia E, Hoyoux A, Marx JC, Sonan G, Feller G, Gerday C (2004) Some like it cold: biocatalysis at low temperatures. FEMS Microbiol Rev 28:25–42CrossRefGoogle Scholar
  18. Giordano D, Parrilli E, Dettaï A, Russo R, Barbiero G, Marino G, Lecointre G, di Prisco G, Tutino ML, Verde C (2007) The truncated hemoglobins in the Antarctic psychrophilic bacterium Pseudoalteromonas haloplanktis TAC125. Gene 398:69–77CrossRefGoogle Scholar
  19. Giordano D, Russo R, Ciaccio C, Howes BD, di Prisco G, Smulevich G, Marden MC, Hui Bon Hoa G-H, Coletta M, Verde C (2011) Ligand- and proton-linked conformational changes of the ferrous 2/2 hemoglobin of Pseudoalteromonas haloplanktis TAC125. IUBMB Life 63:566–573CrossRefGoogle Scholar
  20. Howes BD, Giordano D, Boechi L, Russo R, Mucciacciaro S, Ciaccio C, Sinibaldi F, Fittipaldi M, Martì MA, Estrin DA, di Prisco G, Coletta M, Verde C, Smulevich G (2011) The peculiar heme pocket of the 2/2 hemoglobin of cold adapted Pseudoalteromonas haloplanktis TAC125. J Biol Inorg Chem 16:299–311CrossRefGoogle Scholar
  21. Jagannadham MV, Rao VJ, Shivaji S (1991) The major carotenoid pigment of a psychrotrophic Micrococcus roseus strain: purification, structure, and interaction with synthetic membranes. J Bacteriol 173:7911–7917Google Scholar
  22. Krembs C, Eicken H, Junge K, Deming JW (2002) High concentrations of exopolymeric substances in Arctic winter sea ice: implications for the polar ocean carbon cycle and cryoprotection of diatoms. Deep-Sea Res A 49:2163–2181CrossRefGoogle Scholar
  23. Kumar S, Nussinov R (2004) Different roles of electrostatic in heat and in cold: adaptation by citrate synthase. Chem-BioChem 5:280–290Google Scholar
  24. Lama A, Pawaria S, Bidon-Chanal A, Anand A, Gelpí JL, Arya S, Martí M, Estrin DA, Luque FJ, Dikshit KL (2009) Role of Pre-A motif in nitric oxide scavenging by truncated hemoglobin, HbN, of Mycobacterium tuberculosis. J Biol Chem 284:14457–14468CrossRefGoogle Scholar
  25. Marx JC, Blaise V, Collins T, D’Amico S, Delille D, Gratia E, Hoyoux A, Huston AL, Sonan G, Feller G, Gerday C (2004) A perspective on cold enzymes: current knowledge and frequently asked questions. Cell Mol Biol Noisy-le-grand 50:643–655Google Scholar
  26. Médigue C, Krin E, Pascal G, Barbe V, Bernsel A, Bertin PN, Cheung F, Cruveiller S, D’Amico S, Duilio A, Fang G, Feller G, Ho C, Mangenot S, Marino G, Nilsson J, Parrilli E, Rocha EP, Rouy Z, Sekowska A, Tutino ML, Vallenet D, von Heijne G, Danchin A (2005) Coping with cold: the genome of the versatile marine Antarctic bacterium Pseudoalteromonas haloplanktis TAC125. Genome Res 15:1325–1335CrossRefGoogle Scholar
  27. Methé BA, Nelson KE, Deming JW, Momen B, Melamud E, Zhang X, Moult J, Madupu R, Nelson WC, Dodson RJ, Brinkac LM, Daugherty SC, Durkin AS, DeBoy RT, Kolonay JF, Sullivan SA, Zhou L, Davidsen TM, Wu M, Huston AL, Lewis M, Weaver B, Weidman JF, Khouri H, Utterback TR, Feldblyum TV, Fraser CM (2005) The psychrophilic lifestyle as revealed by the genome sequence of Colwellia psychrerythraea 34H through genomic and proteomic analyses. Proc Natl Acad Sci USA 102:10913–10918CrossRefGoogle Scholar
  28. Moline MA, Karnovsky NJ, Brown Z, Divoky GJ, Frazer TK, Jacoby CA, Torres JJ, Fraser WR (2008) High latitude changes in ice dynamics and their impact on polar marine ecosystems. Annu NY Acad Sci 1134:267–319CrossRefGoogle Scholar
  29. Motohashi K, Watanabe Y, Yohda M, Yoshida M (1999) Heat-inactivated proteins are rescued by the DnaK.J-GrpE set and ClpB chaperones. Proc Natl Acad Sci USA 96:7184–7189CrossRefGoogle Scholar
  30. Murray AE, Grzymski JJ (2007) Diversity and genomics of Antarctic marine microorganisms. Phil Trans R Soc B 362:2259–2271CrossRefGoogle Scholar
  31. Nicoletti FP, Comandini A, Bonamore A, Boechi L, Boubeta F, Feis A, Smulevich G, Boffi A (2010) Sulfide binding properties of truncated hemoglobins. Biochemistry 49:2269–2278CrossRefGoogle Scholar
  32. Parrilli E, Giuliani M, Giordano D, Russo R, Marino G, Verde C, Tutino ML (2010) The role of a 2-on-2 haemoglobin in oxidative and nitrosative stress resistance of Antarctic Pseudoalteromonas haloplanktis TAC125. Biochimie 92:1003–1009CrossRefGoogle Scholar
  33. Pegg DE (2007) Principles of cryopreservation. Meth Mol Biol 368:39–57CrossRefGoogle Scholar
  34. Pesce A, Couture M, Dewilde S, Guertin M, Yamauchi K, Ascenzi P, Moens L, Bolognesi M (2000) A novel two-over-two alpha-helical sandwich fold is characteristic of the truncated hemoglobin family. EMBO J 19:2424–2434CrossRefGoogle Scholar
  35. Piette F, D’Amico S, Mazzuchelli G, Danchin A, Leprince P, Feller G (2011) Life in the cold: a proteomic study of cold-repressed proteins in the Antarctic bacterium Pseudoalteromonas haloplanktis TAC125. Appl Environ Microbiol 77:3881–3883CrossRefGoogle Scholar
  36. Piette F, D’Amico S, Struvay C, Mazzuchelli G, Renaut J, Tutino ML, Danchin A, Leprince P, Feller G (2010) Proteomics of life at low temperatures: trigger factor is the primary chaperone in the Antarctic bacterium Pseudoalteromonas haloplanktis TAC125. Mol Microbiol 76:120–132CrossRefGoogle Scholar
  37. Poole RK, Anjum MF, Membrillo-Hernàndez J, Kim SO, Hughes MN, Stewart V (1996) Nitric oxide, nitrite, and Fnr regulation of hmp (flavohemoglobin) gene expression in Escherichia coli K-12. J Bacteriol 178:5487–5492Google Scholar
  38. Rabus R, Ruepp A, Frickey T, Rattei T, Fartmann B, Stark M, Bauer M, Zibat A, Lombardot T, Becker I, Amann J, Gellner K, Teeling H, Leuschner WD, Glöckner FO, Lupas AN, Amann R, Klenk HP (2004) The genome of Desulfotalea psychrophila, a sulfate-reducing bacterium from permanently cold Arctic sediments. Environ Microbiol 6:887–902CrossRefGoogle Scholar
  39. Ray MK, Kumar GS, Janiyani K, Kannan K, Jagtap P, Basu MK, Shivaji S (1998) Adaptation to low temperature and regulation of gene expression in Antarctic psychrotrophic bacteria. J Biosci 23:423–435CrossRefGoogle Scholar
  40. Riley M, Staley JT, Danchin A, Wang TZ, Brettin TS, Hauser LJ, Land ML, Thompson LS (2008) Genomics of an extreme psychrophile, psychromonas ingrahamii. BMC Genomics 9:210CrossRefGoogle Scholar
  41. Rodrigues D, Tiedje M (2008) Coping with our cold planet. Appl Environ Microbiol 74:1677–1686CrossRefGoogle Scholar
  42. Rodrigues D, Ivanova N, He Z, Huebner M, Zhou J, Tiedje M (2008) Architecture of thermal adaptation in an Exiguobacterium sibiricum strain isolated from 3 million year old permafrost: a genome and transcriptome approach. BMC Genomics 9:547CrossRefGoogle Scholar
  43. Russell NJ (1998) Molecular adaptations in psychrophilic bacteria: potential for biotechnological applications. Adv Biochem Eng Biotechnol 61:1–21Google Scholar
  44. Russell NJ (2007) Psychrophiles: membrane adaptations. In physiology and biochemistry of extremophiles. In: Gerday C, Glansdorff N (eds) ASM Press, Washington, pp 155–164Google Scholar
  45. Russo R, Giordano D, Riccio A, di Prisco G, Verde C (2010) Cold-adapted bacteria and the globin case study in the Antarctic bacterium Pseudoalteromonas haloplanktis TAC125. Mar Gen 3:125–131CrossRefGoogle Scholar
  46. Sauer H, Wartenberg M, Hescheler J (2001) Reactive oxygen species as intracellular messengers during cell growth and differentiation. Cell Physiol Biochem 11:173–186CrossRefGoogle Scholar
  47. Saunders NF, Thomas T, Curmi PM, Mattick JS, Kuczek E, Slade R, Davis J, Franzmann PD, Boone D, Rusterholtz K, Feldman R, Gates C, Bench S, Sowers K, Kadner K, Aerts A, Dehal P, Detter C, Glavina T, Lucas S, Richardson P, Larimer F, Hauser L, Land M, Cavicchioli R (2003) Mechanisms of thermal adaptation revealed from the genomes of the Antarctic Archaea Methanogenium frigidum and Methanococcoides burtonii. Gen Res 13:1580–1588CrossRefGoogle Scholar
  48. Shivaji S, Prakash Jogadhenu SS (2010) How do bacteria sense and respond to low temperature? Arch Microbiol 192:85–95CrossRefGoogle Scholar
  49. Tehei M, Franzetti B, Madern D, Ginzburg m, Ginzburg BZ, Giudici-Orticoneìi MT, Bruschi M, Zaccai G (2004) Adaptation to extreme environments: macromolecular dynamics in bacteria compared in vivo by neutron scattering. EMBO Reports 5:66–70CrossRefGoogle Scholar
  50. Verde C, Giordano D, Russo R, Riccio A, Vergara A, Mazzarella L, di Prisco G (2009) Hemoproteins in the cold. Mar Gen 2:67–73CrossRefGoogle Scholar
  51. Vinogradov SN, Hoogewijs D, Bailly X, Arredondo-Peter R, Guertin M, Gough J, Dewilde S, Moens L, Vanfleteren JR (2005) Three globin lineages belonging to two structural classes in genomes from the three kingdoms of life. Proc Natl Acad Sci USA 102:11385–11389CrossRefGoogle Scholar
  52. Vinogradov S, Moens L (2008) Diversity of globin function: enzymatic, transport, storage, and sensing. J Biol Chem 283:8773–8777CrossRefGoogle Scholar
  53. Wada H, Murata N (1989) Synechocystis PCC6803 mutants defective in desaturation of fatty acids. Plant Cell Physiol 30:971–978Google Scholar
  54. Watanabe YH, Yoshida M (2004) Trigonal DnaK-DnaJ complex versus free DnaK and DnaJ; heat stress converts the former to the latter and only the latter can do disaggregation in cooperation with ClpB. J Biol Chem 279:15723–15727CrossRefGoogle Scholar
  55. Wittenberg JB, Bolognesi M, Wittenberg BA, Guertin M (2002) Truncated hemoglobins: a new family of hemoglobins widely distributed in bacteria, unicellular eukaryotes, and plants. J Biol Chem 227:871–874CrossRefGoogle Scholar
  56. Zheng S, Ponder MA, Shih JY, 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 28:467–488CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Guido di Prisco
    • 1
  • Daniela Giordano
    • 1
  • Roberta Russo
    • 1
  • Cinzia Verde
    • 1
  1. 1.Institute of Protein Biochemistry, National Research CouncilNaplesItaly

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