Journal of Biosciences

, Volume 31, Issue 1, pp 157–165 | Cite as

Mechanism of bacterial adaptation to low temperature

  • M. K. Chattopadhyay
Review
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Accepted:

Abstract

Survival of bacteria at low temperatures provokes scientific interest because of several reasons. Investigations in this area promise insight into one of the mysteries of life science —namely, how the machinery of life operates at extreme environments. Knowledge obtained from these studies is likely to be useful in controlling pathogenic bacteria, which survive and thrive in cold-stored food materials. The outcome of these studies may also help us to explore the possibilities of existence of life in distant frozen planets and their satellites.

Key words

Antarctic cold adaptation low temperature psychrophiles 

Abbreviations used

AFPs

antifreeze proteins

CSPs

cold-shock proteins

HSPs

heat shock proteins

TH

thermal hysteresis

VBNC

viable but nonculturable

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References

  1. Alam S I, Singh L, Dube S, Reddy G S and Shivaji S2003 PsycrophilicPlanococcus maitriensis sp. nov. from Antarctica;Syst. Appl. Microbiol. 26 505–510PubMedCrossRefGoogle Scholar
  2. Annous B A, Becker L A, Bayles D O, Labeda D P and Wilkinson B J 1997 Critical role of anteiso-C15∶0 fatty acid in the growthof Listeria monocytogenes at low temperatures;Appl. Environ. Microbiol. 63 3887–3894PubMedGoogle Scholar
  3. Billi D, Friedmann E I, Hofer K G, Caiola M G and Ocampo-Friedmann R 2000 Ionizing-radiation resistance in the desiccation-tolerant cyanobacteriumChroococcidiopsis;Appl. Environ. Microbiol. 66 1489–1492PubMedCrossRefGoogle Scholar
  4. Bakermans C, Tsapin A I, Souza-Egipsy V, Gilichinsky D A and Nealson K H 2003 Reproduction and metabolism at —10°C of bacteria isolated from Siberian permafrost;Environ. Microbiol. 5 321–326PubMedCrossRefGoogle Scholar
  5. Breezee J, Cady N and Staley J.T 2004 Subfreezing growth of the sea ice bacterium “Psychromonas ingrahamii”;Micriobial Ecol. 47 300–304Google Scholar
  6. Caldas T, Demont-Caulet N, Ghazi A and Richarme G 1999 Thermoprotection by glycine betaine and choline;Microbiology 145 2543–2548PubMedGoogle Scholar
  7. Chattopadhyay M K2000 Cold adaptation of Antarctic microorganisms-possible involvement of viable but nonculturable cells;Polar Biol. 23 223–224CrossRefGoogle Scholar
  8. Chattopadhyay M K 2002a The cryoprotective effects of glycine betaine on bacteria;Trends Microbiol. 10 311CrossRefGoogle Scholar
  9. Chattopadhyay M K2002b The link between bacterial radiation resistance and cold adaptation;J. Biosci. 27 71–73PubMedCrossRefGoogle Scholar
  10. Chattopadhyay M K and Jagannadham M V 2001 Maintenance of membrane fluidity in Antarctic bacteria;Polar Biol. 24 386–388CrossRefGoogle Scholar
  11. Chattopadhyay M K, Kern R, Mistou M-Y, Dandekar A M, Uratsu S L and Richarme G 2004 The chemical chaperone proline relieves the thermosensitivity of adna K deletion mutant at 42°C;J. Bacteriol. 186 8149–8152PubMedCrossRefGoogle Scholar
  12. Chattopadhyay M K, Devi K U, Gopishankar Y and Shivaji S 1995 Thermolable alkaline phosphatase fromSphingobacterium antarcticus, a psychrotrophic bacterium from Antarctica;Polar Biol. 15 215–219CrossRefGoogle Scholar
  13. Chintalapati S, Kiran M D and Shivaji S2004 Role of membrane lipid fatty acids in cold adaptation;Cell. Mol. Biol. 50 631–642PubMedGoogle Scholar
  14. Chow K-C and Tung W L1998 Overexpression ofdna K/dna J andgro EL confers freeze tolerance toEscherichia coli;Biochem. Biophys. Res. Commun. 253 502–505PubMedCrossRefGoogle Scholar
  15. Coker J A, Sheridan P P, Loveland-Curtze J, Gutshall K R, Auman A J and Brenchley J E 2003 Biochemical characterization of a β-galactosidase with a low temperature optimum obtained from an AntarcticArthrobacter isolate;J. Bacteriol. 185 5473–5482PubMedCrossRefGoogle Scholar
  16. D'Amico S, Claverie P, Collins T, Georlette D, Gratia E, Hoyoux A, Meuwis M-A, Feller G and Gerday C 2002 Molecular basis of cold adaptation;Philos. Trans. R. Soc. London B Biol. Sci. 357 917–925PubMedCrossRefGoogle Scholar
  17. Duman J G and Olsen T M1993 Thermal hysteresis protein activity in bacteria, fungi, and phylogenetically diverse plants;Cryobiology 30 322–328CrossRefGoogle Scholar
  18. Ferrer M, Chernikova T N, Yakimov M M, Golyshin P N and Timmis K N 2003 Chaperonins govern growth ofEscherichia coli at low temperatures;Nat. Biotechnol. 21 1266–1267PubMedCrossRefGoogle Scholar
  19. Gerday C, Aittaleb M, Bentahir M, Chessa J-P, Claverie P, Collins T, D'Amico S, Dumont J, Garsoux G, Georlette D, Hoyoux A, Lonhienne T, Meuwis M-A and Feller G2000 Cold-adapted enzymes:from fundamentals to biotechnology;Trends Biotechnol. 18 103–107PubMedCrossRefGoogle Scholar
  20. Gilbert J A, Hill P J, Dodd C E R and Laybourn-Parry J2004 Demonstration of antifreeze protein activity in Antarctic lake bacteria;Microbiology 150 171–180PubMedCrossRefGoogle Scholar
  21. Gilbert J A, Davies P L and Laybourn-Parry J2005 A hyperactive Ca2+ -dependent antifreeze protein in an Antarctic bacterium;FEMS Microbiol. Lett. 245 67–72PubMedCrossRefGoogle Scholar
  22. Groudieva T, Kambourova M, Yusef H, Royter M, Grote R, Trinks H and Antranikian G2004 Diversity and cold-active hydrolytic enzymes of culturable bacteria associated with Arctic sea ice, Spitzbergen;Extremophiles 8 475–488PubMedCrossRefGoogle Scholar
  23. Hirsch P, Gallikowski C A, Siebert J, Peissl K, Kroppenstedt R, Schumann P, Stackebrandt E and Anderson R 2004Deinococcus frigens sp. nov.,Deinococcus saxicola sp.nov., andDeinococcus marmoris sp.nov., low temperature and draughttolerating, UV-resistant bacteria from continental Antarctica;Syst. Appl. Microbiol. 27 636–645PubMedCrossRefGoogle Scholar
  24. Hossain M M and Nakamoto H 2002 Htp G plays a role in cold acclimation in Cyanobacteria;Curr. Microbiol. 44 291–296PubMedCrossRefGoogle Scholar
  25. Hossain M M and Nakamoto H 2003 Role for the cyanobacterial Htp G in protection from oxidative stress;Curr. Microbiol. 46 70–76PubMedCrossRefGoogle Scholar
  26. Huston A L, Methe B and Deming J W 2004 Purification, characterization, and sequencing of an extracellular coldactive aminopeptidase produced by marine psychrophileColwellia psychrerythraea strain 34H;Appl. Environ. Microbiol. 70 3321–3328PubMedCrossRefGoogle Scholar
  27. Jagtap P and Ray M K1999 Studies on the cytoplasmic protein tyrosine kinase activity of the Antarctic psychrotrophic bacteriumPseudomonas syringae;FEMS Microbiol. Lett. 173 379–388PubMedCrossRefGoogle Scholar
  28. Junge K, Eicken H and Deming J W2004 Bacterial activity at −2 to −20°C in Arctic wintertime sea ice;Appl. Environ. Microbiol. 70 550–557PubMedCrossRefGoogle Scholar
  29. Kaan T, Homuth G, Mader U, Bandow J and Schweder T2002 Genome-wide transcriptional profiling of theBacillus subtilis cold-shock response;Microbiology 148 3441–3455PubMedGoogle Scholar
  30. Kannan K, Janiyani K L, Shivaji S and Ray M K 1998 Histidine utilisation operon (hut) is upregulated at low temperature in the Antarctic psychrotrophic bacteriumPseudomonas syringae;FEMS Microbiol. Lett. 161 7–14PubMedCrossRefGoogle Scholar
  31. Kawahara H, Koda N, Oshio M and Obata H 2000 A cold acclimation protein with refolding activity on frozen denatured enzymes;Biosci. Biotechnol. Biochem. 64 2668–2674PubMedCrossRefGoogle Scholar
  32. Kiran M D, Annapoorni S, Suzuki I, Murata N and Shivaji S2005Cis-trans isomerase gene in psychrophilicPseudomonas syringae is constitutively expressed during growth and under conditions of temperature and solvent stress;Extremophiles 9 117–125PubMedCrossRefGoogle Scholar
  33. Ko R, Smith L T and Smith G M 1994 Glycine betaine confers enhanced osmotolerance and cryotolerance onListeria monocytogenes;J. Bacteriol. 176 426–431PubMedGoogle Scholar
  34. Kumar G S, Jagannadham M V and Ray M K 2002 Low-temperature induced changes in composition and fluidity of lipopolysaccharides in the Antarctic psychrotrophic bacteriumPseudomonas syringae;J. Bacteriol. 184 6746–6749PubMedCrossRefGoogle Scholar
  35. Lelivelt M J and Kawula, T H 1995 Hsc 66, an Hsp 70 homolog inEscherichia coli, is induced by cold shock but not by heat shock;J. Bacteriol. 177 4900–4907PubMedGoogle Scholar
  36. Liu S, Graham J E, Bigelow L, Morse P D 2nd and Wilkinson B J 2002 Identificationof Listeria monocytogenes genes expressed in response to growth at low temperature;Appl. Environ. Microbiol. 68 1697–1705PubMedCrossRefGoogle Scholar
  37. Panasik N, Brenchley J E and Farber G K 2000 Distributions of structural features contributing to thermostability in mesophilic and thermophilic alpha/beta barrel glycosyl hydrolases;Biochim. Biophys. Acta 1543 189–201PubMedGoogle Scholar
  38. Pfennig P L and Flower A M2001 Bip A is required for growth ofEscherichia coli K 12 at low temperature;Mol. Genet. Genomics 266 313–317PubMedCrossRefGoogle Scholar
  39. Porankiewicz, J and Clarke A K 1997 Induction of the heat shock protein Clp B affects cold acclimation in the cyanobacteriumSynechococcus sp. strain PCC 7942;J. Bacteriol. 179 5111–5117PubMedGoogle Scholar
  40. Prabahar V, Dube S, Reddy G S and Shivaji S2004Pseudonocardia antarctica sp. nov. an Actinomycetes from McMurdo Dry Valleys, Antarctica;Syst. Appl. Microbiol. 27 66–71PubMedCrossRefGoogle Scholar
  41. Purusharth R I, Klein F, Sulthana S, Jager S, Jagannadham M V, Evguenieva-Hackenberg E, Ray M K and Klug G2005 Exoribonuclease R interacts with endoribonuclease E and an RNA-helicase in the psychrotrophic bacteriumPseudomonas syringae LZ 4W;J. Biol. Chem. 280 14572–14578PubMedCrossRefGoogle Scholar
  42. Ray M K, Devi K U, Kumar G S and Shivaji S 1992 Extracellular protease from the Antarctic yeastCandida humicola;Appl. Environ. Microbiol. 58 1918–1923PubMedGoogle Scholar
  43. Ray M K, Kumar G S, Janiyani K, Kannan K, Jagtap P, Basu M K and Shivaji S 1998 Adaptation to low temperature and regulation of gene expression in Antarctic psychrotrophic bacteria;J. Biosci. 23 423–435CrossRefGoogle Scholar
  44. Ray M K, Kumar G S and Shivaji S1994a Phosphorylation of membrane proteins in response to temperature in an AntarcticPseudomonas syringae;Microbiology 140 3217–3223PubMedCrossRefGoogle Scholar
  45. Ray M K, Kumar G S and Shivaji S1994b Phosphorylation of lipopolysaccharides in the Antarctic psychrotrophPseudomonas syringae: a possible role in temperature adaptation;J. Bacteriol. 176 4243–4249PubMedGoogle Scholar
  46. Ray M K, Sitaramamma T, Gandhi S and Shivaji S 1994c Occurrence and expression ofcsp A a cold shock gene in Antarctic psychrotrophic bacteria;FEMS Microbiol. Lett. 116 55–60PubMedCrossRefGoogle Scholar
  47. Reddy G S, Rajagopalan Gand Shivaji S 1994 Thermolabile ribonucleases from Antarctic psychrotrophic bacteria: Detection of the enzyme in various bacteria and purification fromPseudomonas fluorescens;FEMS Microbiol. Lett. 122 211–216CrossRefGoogle Scholar
  48. Reddy G S, Raghavan P U, Sarita N B, Prakash J S, Nagesh N, Delille D and Shivaji S 2003aHalomonas glaciei sp. nov. isolated from fast ice of Adelie land Antarctica;Extremophiles 7 55–61PubMedGoogle Scholar
  49. Reddy G S, Matsumoto G I and Shivaji S 2003bSporosarcina macmurdoensis sp. nov., from a cyanobacterial mat sample from a pond in the McMurdo Dry Valleys, Antarctica;Int. J. Syst. Evol. Microbiol. 53 1363–1367PubMedCrossRefGoogle Scholar
  50. Reddy G S, Prakash J S, Srinivas R, Matsumoto G I and Shivaji S 2003cLeifsonia rubra sp. nov. andLeifsonia aurea sp. nov., psychrophiles from a pond in Antarctica;Int. J. Syst. Evol. Microbiol. 53 977–984PubMedCrossRefGoogle Scholar
  51. Reddy G S, Matsumoto G I, Schumann P, Stackebrandt Eand Shivaji S 2004 Psychrophilic pseudomonads from Antarctica:Pseudomonas antarctica sp nov.,Pseudomonas meridiana sp. nov. andPseudomonas proteolytica sp. nov;Int. J. Syst. Evol. Microbiol. 54 713–719PubMedCrossRefGoogle Scholar
  52. Regha K, Satapathy A K and Ray M K 2005 Rec D plays an essential function during growth at low temperature in the Antarctic bacteriumPseudomonas syringae Lz 4W;Genetics 170 1473–1484PubMedCrossRefGoogle Scholar
  53. Rivkina E M, Friedmann E I, McKay C P and Gilichinsky D A 2000 Metabolic activity of permafrost bacteria below the freezing point;Appl. Environ. Microbiol. 66 3230–3233PubMedCrossRefGoogle Scholar
  54. Shivaji S, Chaturvedi P, Reddy G S and Suresh K 2005aPedobacter himalayensis sp. nov. from the Hamta glacier located in the Himalayan mountain ranges of India;Int. J. Syst. Evol. Mocrobiol. 55 1083–1088CrossRefGoogle Scholar
  55. Shivaji S, Reddy G S, Suresh K, Gupta P, Chintalapati S, Schumann P, Stackebrandt E and Matsumoto GI2005bPsychrobacter vallis sp.nov. andPsychrobacter aquaticus sp.nov., from Antarctica;Int. J. Syst. Evol. Microbiol. 55 757–762PubMedCrossRefGoogle Scholar
  56. Shivaji S, Reddy G S, Aduri R P, Kutty R and Ravenschlag K 2004 Bacterial diversity of a soil sample from Schirmacher Oasis, Antarctica;Cell. Mol. Biol. 50 525–536PubMedGoogle Scholar
  57. Smirnova G V, Zakirova O N and Oktiabr'skii O N2001 Role of the antioxidant system in responseof Escherichia coli bacteria to cold stress;Mikrobiologiia 70 55–60PubMedGoogle Scholar
  58. Subczynski W K, Markowska E, Gruszecki W I and Sielewiesiuk J1992 Effect of polar carotenoids on dimyristoylphosphatidylcholine membranes: a spin-label study;Biochim. Biophys. Acta 1105 97–108PubMedCrossRefGoogle Scholar
  59. Suutari M and Laakso S1994 Microbial fatty acids and thermal adaptation;Crit. Rev. Microbiol. 20 285–328PubMedGoogle Scholar
  60. Suzuki L, Kanesaki Y, Mikami K, Kanehisa M and Murata N 2001 Cold-regulated genes under control of the cold sensor Hik 33 inSynechocystis;Mol. Microbiol. 40 235–244PubMedCrossRefGoogle Scholar
  61. Tsuruta H, Tamura J, Yamagata H and Aizono Y 2004 Specification of amino acid residues essential for the catalytic reaction of cold-active protein-tyrosine phosphatase of a psychrophile,Shewanella sp.;Biosci. Biotechnol. Biochem. 68 440–443PubMedCrossRefGoogle Scholar
  62. Uma S, Jadhav R S, Kumar G S, Shivaji S and Ray M K 1999 A RNA polymerase with transcriptional activity at 0°C from the Ant-arctic bacteriumPseudomonas syringae;FEBS Lett. 453 313–317PubMedCrossRefGoogle Scholar
  63. Wintrode P L, Miyazaki K and Arnold F H2000 Cold-adaptation of a mesophilic subtilisin-like protease by laboratory evolution;J. Biol. Chem. 275 31635–31640PubMedCrossRefGoogle Scholar
  64. Yamanaka K1999 Cold shock response inEscherichia coli;J. Mol. Microbiol. Biotechnol. 1 193–202PubMedGoogle Scholar
  65. Yamashita Y, Nakamura N, Omiya K, Nishikawa J, Kawahara H and Obata H 2002 Identification of an antifreeze lipoprotein fromMoraxella sp. of Antarctic origin;Biosci. Biotechnol. Biochem. 66 239–247PubMedCrossRefGoogle Scholar
  66. Zartler E R, Jenney F E Jr, Terrell M, Eidsness M K, Adams M W, and Prestegard J H 2001 Structural basis for thermostability in aporubredoxins fromPyrococcus furiosus andClostridium pasteurianum;Biochemistry 40 7279–7290PubMedCrossRefGoogle Scholar

Copyright information

© Indian Academy of Sciences 2006

Authors and Affiliations

  • M. K. Chattopadhyay
    • 1
  1. 1.Centre for Cellular and Molecular BiologyHyderabadIndia

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