Advertisement

Journal of Biosciences

, Volume 23, Issue 4, pp 423–435 | Cite as

Adaptation to low temperature and regulation of gene expression in antarctic psychrotrophic bacteria

  • Malay K RayEmail author
  • G Seshu Kumar
  • Kamala Janiyani
  • K Kannan
  • Pratik Jagtap
  • Malay K Basu
  • S Shivaji
Article

Abstract

Exposure to extremes of temperatures cause stresses which are sometimes lethal to living cells. Microorganisms in nature, however, are extremely diverse and some of them can live happily in the freezing cold of Antarctica. Among the cold adapted psychrotrophs and psychrophiles, the psychrotrophic bacteria are the predominant forms in the continental Antarctica. In spite of living in permanently cold area, the antarctic bacteria exhibit, similar to mesophiles, ‘cold-shock’ response albeit at a much lower temperatures, e.g., at 0–5°C. However, because of permanently cold condition and the long isolation of the continent, the microorganisms have acquired new adaptive features in the membranes, enzymes and macromolecular synthesis. Only recently these adaptive modifications are coming into light due to the efforts of various laboratories around the world. However, a lot more is known about adaptive response to low temperature in mesophilic bacteria than in antarctic bacteria. Combined knowledge from the two systems is providing useful clues to the understanding of basic biology of low temperature growing organisms. This article will provide an overview of this area of research with a special reference to sensing of temperature and regulation of gene expression at lower temperature.

Keywords

Antarctic bacteria cold adaptation cold-shock proteins temperature sensing cold induced gene expression 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aghajari N, Feller G, Gerday C and Haser R 1996 Crystalization and preliminary X-ray diffraction studies of α-amylase from the antarctic psychrophileAlteromonas haloplanctis A23;Prot. Sci. 5 2128–2129CrossRefGoogle Scholar
  2. Adler E and Knowles J 1995 A thermolabile isomerase from the psychrophileVibrio sp. strain ANT-300;Arch. Biochem. Biophys. 321 137–139PubMedCrossRefGoogle Scholar
  3. Araki T 1991 Changes in rates of synthesis of individual proteins in a psychrotrophic bacterium after a shift in temperature;Can. J. Microbiol. 37 840–847PubMedCrossRefGoogle Scholar
  4. Bobier S R, Ferroni G D and Innis W E 1972 Protein synthesis by the psychrophilesBacillus psychrophilus andBacillus insolitus;Can. J. Microbiol. 18 1837–1843PubMedCrossRefGoogle Scholar
  5. Bowman J P, McCammon S A, Nichols D S, Skerrat J H, Rea S M, Nichols P D and McMeekin T A 1997Schewanella gelidimarina sp. nov. andSchewanella frigidimarina sp. nov., novel antarctic species with ability to produce eicosapentaenoic acid (20∶5 ε3) and grow anaerobically by dissimilatory Fe (III) reduction;Int. J. Syst. Bacteriol. 47 1040–1047PubMedCrossRefGoogle Scholar
  6. Brandi A, Pietroni P, Gualerzi C O and Pon C L 1996 Post transcriptional regulation ofcspA expression inEscherichia coli.;Mol. Microbiol. 19 231–240PubMedCrossRefGoogle Scholar
  7. Broeze R J, Solomon C J and Pope D H 1978 Effects of low temperature onin vivo andin vitro protein synthesis inEscherichia coli andPseudomonas fluorescence;J. Bacteriol. 134 861–874PubMedPubMedCentralGoogle Scholar
  8. Chattopadhyay, M K, Uma Devi K, Gopisankar Y and Shivaji S 1995 Thermolabile alkaline phosphatase fromSphingobacterium antarcticus, a psychrotrophic bacterium from Antarctica;Polar Biol. 15 215–219CrossRefGoogle Scholar
  9. Chauhan S and Shivaji S 1994 Growth and pigmentation inSphingobacterium antarcticus, a psychrotrophic bacterium from Antarctica;Polar Biol. 14 31–36CrossRefGoogle Scholar
  10. Chi E and Bartlett D H 1995 An rpoE-like locus controls outer membrane protein synthesis and growth at cold temperatures and high pressures in the deep sea bacteriumPhotobacterium sp strain SS9;Mol. Microbiol. 17 713–726PubMedCrossRefGoogle Scholar
  11. Cossins A N 1994 Homeoviscous adaptation of biological membranes and its functional significance; inTemperature adaptation of biological membrane (ed.) A R Cossin (London: Portland Press) pp 63–76Google Scholar
  12. Das H K and Goldstein A 1968 Limited capacity for protein synthesis at zero degree centigrade inEscherichia coli;J. Mol. Biol. 31 209–226PubMedCrossRefGoogle Scholar
  13. Davail S, Feller G, Narinx E and Gerday C 1995 Cold adaptation of proteins. Purification, characterization and sequence of the heat labile subtilisin from the antarctic psychrophileBacillus TA 47;J. Biol. Chem. 269 17448–17453Google Scholar
  14. Dersch P, Kneip S and Bremmer E 1994 The nucleoid-associated DNA-binding protein H-NS is required for the efficient adaptation ofEscherichia coli K-12 to a cold environment;Mol. Gen. Genet. 245 255–259PubMedCrossRefGoogle Scholar
  15. Donovan W P and Kusher S R 1986 Polynucleotide phosphorylase and ribonuclease II are required for cell viability and mRNA turn over inEscherichia coli K-12;Proc. Natl. Acad. Sci. USA 83 120–124PubMedCrossRefGoogle Scholar
  16. Fang L, Jiang W, Bae W and Inouye M 1997 Promoter-independent cold shock induction ofcspA and its derepression at 37°C by mRNA stabilization;Mol. Microbiol. 23 355–364PubMedCrossRefGoogle Scholar
  17. Feller G, Narinx E, Arpigny J L, Aittaleb M, Baise E, Genicot S and Gerday C 1996 Enzymes from psychrophilic organisms;FEMS Microbiol. Rev. 18 189–202CrossRefGoogle Scholar
  18. Feller G, Narinx E, Arpigny J L, Zekhnini Z, Swings J and Gerday C 1994a Temperature dependent of growth, enzyme secretion and activity of psychrophilic antarctic bacteria;Appl. Microbiol. Biotechnol. 41 477–479CrossRefGoogle Scholar
  19. Feller G, Payan F, Theys F, Qian M, Haser R and Gerday C 1994b Stability and structural analysis of α-amylase from the antarctic psychrophileAlternomonas haloplanctis A23;Eur. J. Biochem. 222 441–447PubMedCrossRefGoogle Scholar
  20. Fessenmaier M, Frank R, Retey J and Schubert C 1991 Cloning and sequencing of the urocanase gene (hutU) from thePseudomonas putida;FEBS Lett. 286 55–57PubMedCrossRefGoogle Scholar
  21. Friedman D I, Olson E R, Georgopoulos C, Tilly K, Herskowitz I and Banuett F 1984 Interactions of bacteriophage and host macromolecules in the growth of bacteriophage lambda;Microbiol. Rev. 48 299–325PubMedPubMedCentralGoogle Scholar
  22. Gerike U, Danson M J, Russell N J and Hough D W 1997 Sequencing and expression of the gene encoding a cold-active citrate synthase from an antarctic bacterium strain DS2-3R;Eur. J. Biochem. 248 49–57PubMedCrossRefGoogle Scholar
  23. Goldenberg D, Azar I and Oppenheim A B 1996 Differential mRNA stability of thecspA gene in the cold shock response ofEscherichia coli;Mol. Microbiol. 19 241–248PubMedCrossRefGoogle Scholar
  24. Goldstein E and Drilca K 1984 Regulation of bacterial DNA supercoiling: plasmid linking members vary with growth temperature;Proc. Natl. Acad. Sci. USA 81 4046–4050PubMedCrossRefGoogle Scholar
  25. Goldstein J, Pollitt N S and Inouye M I 1990 Major cold shock protein ofEschierchia coli;Proc. Natl. Acad. Sci. USA 87 283–287PubMedCrossRefGoogle Scholar
  26. Gounot A 1991 Bacterial life at low temperature: Physiological aspects and biotechnological implications;J. Appl. Bacteriol. 71 386–397PubMedCrossRefGoogle Scholar
  27. Graumann P and Marahiel M A 1996 Some like it cold: response of microorganisms to cold shock;Arch. Microbiol. 166 293–300PubMedCrossRefGoogle Scholar
  28. Graumann P, Schroder K, Schmid K and Marahiel M A 1996 Cold shock stress-induced proteins inBacillus subtilis;J. Bacteriol. 178 4611–4619PubMedPubMedCentralCrossRefGoogle Scholar
  29. Hamamoto T, Takata N, Kudo T and Horokoshi K 1995 Characteristic presence of polyunsaturated fatty acid in marine psychrophilicVibrios;FEMS Microbiol. Lett. 129 51–56CrossRefGoogle Scholar
  30. Hashimoto W, Suzuki H, Yamamoto K and Kumagai H 1997 Analysis of low temperature inducible mechanism of γ-glutamyl transpeptidase ofEscherichia coli K-12;Biosci. Biotech. Biochem. 61 34–39CrossRefGoogle Scholar
  31. Hebraud M, Dubois E, Potier P and Labadie J 1994 Effect of growth temperatures on the protein levels in a psychrotrophic bacterium,Pseudomonas fragi;J. Bacteriol. 176 4017–4024PubMedPubMedCentralCrossRefGoogle Scholar
  32. Hendrick J P and Hartl F U 1993 Molecular chaperone functions of heat-shock proteins;Annu. Rev. Biochem. 62 349–384PubMedCrossRefGoogle Scholar
  33. Herbert R A 1986 The ecology and physiology of psychrophilic microorganisms; inMicrobes in extreme environments (eds) R A Herbert and G A Cod (London: Academic Press) pp 1–23Google Scholar
  34. Hu L and Phillips A T 1988 Organization and multiple regulation of histidine utilization genes inPseudomonas putida;J. Bacteriol. 170 4272–4279PubMedPubMedCentralCrossRefGoogle Scholar
  35. Jaenicke R 1990 Protein structure and function at low temperatures;Philos. Trans. R. Soc. London B326 535–553CrossRefGoogle Scholar
  36. Jagannadham M V, Jayathirtha Rao V and Shivaji S 1991 The major carotenoid pigment of a psychrotrophicMicrococcus roseus: Purification, structure and interaction of the pigment with synthetic membranes;J. Bacteriol. 173 7911–7917PubMedPubMedCentralCrossRefGoogle Scholar
  37. Jiang W, Hou Y and Inouye M 1997 CspA, the major cold shock protein ofEscherichia coli is an RNA chaperone;J. Biol. Chem. 272 196–202PubMedCrossRefGoogle Scholar
  38. Jones P G and Inouye M 1994 The cold shock response a hot topic;Mol. Microbiol. 11 811–818PubMedCrossRefGoogle Scholar
  39. Jones P G and Inouye M 1996 RbfA, a 30S ribosomal binding factor is a cold shock protein whose absence triggers the cold shock response;Mol. Microbiol. 21 1207–1218PubMedCrossRefGoogle Scholar
  40. Jones P G, Cashel M, Glaser G and Neidhardt F C 1992a Function of a relaxed like state following temperature downshifts inEscherichia coli;J. Bacteriol. 174 3903–3914PubMedPubMedCentralCrossRefGoogle Scholar
  41. Jones P G, Krah R, Tafuri S R and Wolffe A P 1992b DNA gyrase, CS 7.4 and the cold shock response inEscherichia coli;J. Bacteriol. 174 5798–5802PubMedPubMedCentralCrossRefGoogle Scholar
  42. Jones P G, Mitta M, Kim Y, Jiang W and Inouye M 1996 Cold shock induces a major ribosomal associated protein that unwinds double stranded RNA inEschericia coli;Proc. Natl. Acad. Sci. USA 93 76–80PubMedCrossRefGoogle Scholar
  43. Jones P G, Van Bogelen R A and Neidhardt F C 1987 Induction of proteins in response to low temperature inEscherichia coli;J. Bacteriol. 169 2092–2095PubMedPubMedCentralCrossRefGoogle Scholar
  44. Kandror O and Goldberg A L 1997 Trigger factor is induced upon cold shock and enhances viability ofE. coli at low tempertures;Proc. Natl. Acad. Sci, USA 94 4978–4981PubMedCrossRefGoogle Scholar
  45. 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
  46. Kobori H, Sullivan C W and Shizuya H 1984 Heat labile alkaline phosphatase from Antarctic bacteria: rapid 5′ end-labelling of nucleic acids;Proc. Natl. Acad. Sci. USA 81 6691–6695PubMedCrossRefGoogle Scholar
  47. Le Teana A, Brandi A, Falconi M, Spurio R, Pon C L and Gualerzi C O 1991 Identification of a cold shock transcriptional enhancer of theE. coli gene encoding nucleoid protein H-NS;Proc. Natl. Acad. Sci. USA 88 10907–10911PubMedCrossRefGoogle Scholar
  48. Lee S J, Xie A, Jiang W, Etchegaray J P, Jones P G and Inouye M 1994 Family of the major cold shock protein cspA (CS 7·4) ofE. coli where members show a high sequence similarity with the eukaryotic Y-box binding protein;Mol. Microbiol. 11 833–839PubMedCrossRefGoogle Scholar
  49. 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 4900–4907PubMedPubMedCentralCrossRefGoogle Scholar
  50. Lottering E A and Streips U N 1995 Induction of cold shock proteins inBacillus subtilis;Curr. Microbiol. 30 193–199PubMedCrossRefGoogle Scholar
  51. Los D A, Ray M K and Murata N 1997 Differences in the control of the temperature dependent expression of four genes for desaturases inSynechocystis sp. PCC 6803;Mol. Microbiol. 25 1167–1175PubMedCrossRefGoogle Scholar
  52. Mangoli S H, Ramanathan Y, Sanzgiri V R and Mahajan S K 1997 Identification, mapping and characterization of two genes ofEscherichia coli K-12 regulating growth and resistance to streptomycin in cold;J. Genet. 76 73–87CrossRefGoogle Scholar
  53. Marshall C J 1997 Cold adapted enzyme;TIB TECH. 15 359–364Google Scholar
  54. Mayr B, Kaplan T, Lechner S and Scherer S 1996 Identification and purification of a family of dimeric major cold shock protein homologs from the psychrotrophicBacillus cereus WSBC 10201;J. Bacteriol. 178 2916–2925PubMedPubMedCentralCrossRefGoogle Scholar
  55. Merriman T R and Lamont I L 1993 Construction and use of a self-cloning promoter probe vector for Gram-negative bacteria;Gene 126 17–23PubMedCrossRefGoogle Scholar
  56. Mitta M, Fang L and Inouye M 1997 Deletion analysis ofcspA inEscherichia coli: requirement of the AT-rich UP element forcspA transcription and the downstream box in the coding region for its cold shock induction;Mol. Microbiol. 26 321–336PubMedCrossRefGoogle Scholar
  57. Monroy A F and Dhindsa R S 1995 Low temperature signal transduction: Induction of cold acclimation specific genes of alfalfa by calcium at 25°C;Plant Cell 7 321–331PubMedPubMedCentralGoogle Scholar
  58. Morita R Y 1975 Psychrophilic bacteria;Bacteriol. Rev. 39 144–167PubMedPubMedCentralGoogle Scholar
  59. Murata N and Wada H 1995 Acyl lipid desaturases and their importance in the tolerance and acclimatization to cold of cyanobacteria;Biochem. J. 308 1–8PubMedPubMedCentralCrossRefGoogle Scholar
  60. Newkirk K, Feng W, Jiang W, Tejero R, Emerson S D, Inouye M and Montelione G T 1994 Solution NMR structure of the major cold shock protein (CspA) fromEscherichia coli: identification of a binding epitope for DNA;Proc. Natl. Acad. Sci. USA 91 5114–5118PubMedCrossRefGoogle Scholar
  61. Nichols D S, Nichols P D and McMeekin T A 1993 Polyunsaturated fatty acid in Antarctic bacteria;Antarct. Sci. 5 149–160CrossRefGoogle Scholar
  62. Okuyama H, Okajima N, Sasaki S, Higashi S and Murata N 1991 Thecis/trans-isomerization of the double bond of a fattyacid as a strategy for adaptation to changes in ambient temperature in the psychrophilic bacterium,Vibrio sp. strain ABE-1;Biochim. Biophys. Acta 1084 13–20PubMedCrossRefGoogle Scholar
  63. Ray M K, Seshu Kumar G and Shivaji S 1994a Phosphorylation of lipopolysaccharides in the Antarctic psychrotrophPseudomonas syringae: A possible role in temperature adaptation;J. Bacteriol. 176 4243–4249PubMedPubMedCentralCrossRefGoogle Scholar
  64. Ray M K, Seshu Kumar G and Shivaji S 1994b Phosphorylation of membrane proteins in response to temperature in an AntarcticPseudomonas syringae;Microbiology 140 3217–3223PubMedCrossRefGoogle Scholar
  65. Ray M K, Seshu Kumar G and Shivaji S 1994c Tyrosine phosphorylation of a cytosolic protein from the antarctic psychrotrophic bacteriumPseudomonas syringae;FEMS Microbiol. Lett. 122 49–54CrossRefGoogle Scholar
  66. Ray M K, Sitaramamma T, Ghandhi S and Shivaji S 1994d Occurrence and expression ofcspA a cold shock gene in Antarctic psychrotrophic bacteria;FEMS Microbiol. Lett. 116 55–60PubMedCrossRefGoogle Scholar
  67. Ray M K, Uma Devi K, Seshu Kumar G and Shivaji S 1992 Extracellular protease from the Antarctic yeastCandida humicola;Appl. Environ. Microbiol. 58 1918–1923PubMedPubMedCentralGoogle Scholar
  68. Reddy G S N, Rajagopalan G and 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
  69. Rhode J R, Fox J M and Minnich S A 1994 Thermoregulation inYersinia enterocolitica is coincident with changes in DNA supercoiling;Mol. Microbiol. 12 187–199CrossRefGoogle Scholar
  70. Russell N J 1984a Mechanism for thermal adaptation in bacteria: blueprint for survival;Trends Biochem. Sci. 9 108–112CrossRefGoogle Scholar
  71. Russell N J 1984b The regulation of membrane fluidity in bacteria by acyl chain length changes; inBiomembranes 12 membrane fluidity (eds) M Kates and L A Manson (New York: Plenum) pp 329–347CrossRefGoogle Scholar
  72. Russell N J 1990 Cold adaptation of microorganisms;Philos. Trans. R. Soc. London B326 595–611CrossRefGoogle Scholar
  73. Sato N 1995 A family of cold-regulated RNA-binding protein genes in the cyanobacteriumAnabaena variabilis M3;Nucleic Acids Res. 23 2161–2167PubMedPubMedCentralCrossRefGoogle Scholar
  74. Schindelin H, Jiang W, Inouye M and Heinemann U 1994 Crystal structures of CspA the major cold shock protein ofEscherichia coli;Proc. Natl. Acad. Sci. USA 91 5119–5123PubMedCrossRefGoogle Scholar
  75. Schindelin H, Marahiel M A and Heinemann U 1993 Universal nucleic acid binding domain revealed by crystal structure of theB. subtilis. major cold shock protein;Nature (London) 364 164–168CrossRefGoogle Scholar
  76. Schnuchel A, Wiltescheck R, Czisch M, Herrier M, Williamsky G, Grawmann P, Marahiel M A and Holak T A 1993 Structure in solution of the major cold shock protein fromBacillus subtilis;Nature (London) 364 164–171CrossRefGoogle Scholar
  77. Shivaji S and Ray M K 1995 Survival strategies of psychrotrophic bacteria and yeasts of Antarctica;Indian J. Microbiol. 35 263–281Google Scholar
  78. Shivaji S, Shyamala Rao N, Saisree L, Sheth V, Reddy G S N and Bhargava P M 1989 Isolation and identification ofPseudomonas species from Schirmacher Oasis, Antarctica;Appl. Environ. Microbiol. 55 767–770PubMedPubMedCentralGoogle Scholar
  79. Szer W 1970 Cell-free protein synthesis at 0°C. An activating factor from ribosomes of a psychrophilic microorganism;Biochem. Biophys. Acta 213 159–170PubMedGoogle Scholar
  80. van Bogelen R A and Neidhardt F C 1990 Ribosomes as senosrs of heat and cold shock inEscherichia coli;Proc. Natl. Acad. Sci. USA 87 5589–5593CrossRefGoogle Scholar
  81. Vigh L, Los D A, Horvath I and Murata N 1993 The primary signal in the biological perception of temperature: Pd catalyzed hydrogenation of membrane lipids stimulated the expression of thedesA gene inSynechocystis PCC 6803;Proc. Natl. Acad. Sci. USA 90 9090–9094PubMedCrossRefGoogle Scholar
  82. Wada H, Gombos Z and Murata N 1990 Enhancement of chilling tolerance of a Cyanobacterium by genetic manipulation of fatty acid desaturation;Nature (London) 347 200–203CrossRefGoogle Scholar
  83. Whyte L G and Innis W E 1992 Cold shock proteins and cold acclimation in a psychrotrophic bacterium;Can. J. Microbiol. 38 1281–1285CrossRefGoogle Scholar
  84. Williamsky G, Bang H, Fischer G and Marahiel M A 1992 Characterisation ofcspB, aBacillus subtilis inducible cold shock gene affecting cell viability at low temperatures;J. Bacteriol. 174 6326–6335CrossRefGoogle Scholar
  85. Wynn-Williams D D 1990 Ecological aspects of Antarctic microbiology;Adv. Microbiol. 11 71–146Google Scholar
  86. Zimmer S G and Millette R L 1975 DNA-dependent RNA polymerase fromPseudomonas BAL-31. I. Purification and properties of the enzyme;Biochemistry 14 290–299PubMedCrossRefGoogle Scholar

Copyright information

© Indian Academy of Sciences 1998

Authors and Affiliations

  • Malay K Ray
    • 1
    Email author
  • G Seshu Kumar
    • 1
  • Kamala Janiyani
    • 1
  • K Kannan
    • 1
  • Pratik Jagtap
    • 1
  • Malay K Basu
    • 1
  • S Shivaji
    • 1
  1. 1.Centre for Cellular and Molecular BiologyHyderabadIndia

Personalised recommendations