Archives of Microbiology

, Volume 192, Issue 2, pp 85–95 | Cite as

How do bacteria sense and respond to low temperature?

Mini-Review

Abstract

Rigidification of the membrane appears to be the primary signal perceived by a bacterium when exposed to low temperature. The perception and transduction of the signal then occurs through a two-component signal transduction pathway consisting of a membrane-associated sensor and a cytoplasmic response regulator and as a consequence a set of cold-regulated genes are activated. In addition, changes in DNA topology due to change in temperature may also trigger cold-responsive mechanisms. Inducible proteins thus accumulated repair the damage caused by cold stress. For example, the fluidity of the rigidified membrane is restored by altering the levels of saturated and unsaturated fatty acids, by altering the fatty acid chain length, by changing the proportion of cis to trans fatty acids and by changing the proportion of anteiso to iso fatty acids. Bacteria could also achieve membrane fluidity changes by altering the protein content of the membrane and by altering the levels of the type of carotenoids synthesized. Changes in RNA secondary structure, changes in translation and alteration in protein conformation could also act as temperature sensors. This review highlights the various strategies by which bacteria senses low temperature signal and as to how it responds to the change.

Keywords

Cold adaptation Bacteria Desaturases Fatty acid synthesis Two-component signal transduction pathway DNA supercoiling 

Abbreviations

Carbon regulation

The preferred carbon source prevents the simultaneous utilization of alternative carbon sources

Core enzyme

Core enzyme of RNA polymerase (α2ββ′-subunits)

ECF

Extracytosolic function

General stress response

A stress response induced by a set of diverse environmental stimuli

GSP

General stress proteins

LPXTG motif

Amino acid motif for sortase anchoring

Partner switching

Formation of alternative protein complexes that is controlled by protein phosphorylation

RpoS

Sigma factor of general stress response of E. coli and other Gram-negative bacteria

Rsb

Regulator of sigmaB

SigB-GSR

SigB-dependent general stress response

Specific stress/starvation response

Induced by only one stimulus, adaptation against this stimulus only

Vegetative dormancy

A quiescent metabolic state of vegetative cells

References

  1. Agafonov DE, Koib VA, Nazimov IV, Spirin AS (1999) A protein residing at the subunit interface of the bacterial ribosome. Proc Natl Acad Sci USA 96:12345–12349PubMedCrossRefGoogle Scholar
  2. Agafonov DE, Kolb VA, Spirin AS (2001) Ribosome-associated protein that inhibits translation at the aminoacyl-tRNA binding stage. EMBO Rep 2:399–402PubMedGoogle Scholar
  3. Aguilar PS, Lopez P, de Mendoza D (1999) Transcriptional control of the low temperature inducible des gene, encoding the delta 5 desaturase of Bacillus subtilis. J Bacteriol 181:7028–7033PubMedGoogle Scholar
  4. Aguilar PS, Hernandez-Arriaga AM, Cybulski LE, Erazo AC, de Mendoza D (2001) Molecular basis of thermosensing: a two-competent signal transduction thermometer in Bacillus subtilis. EMBO J 20:1681–1691PubMedCrossRefGoogle Scholar
  5. Albanesi D, Mansilla MC, de Mendoza D (2004) The membrane fluidity sensor DesK of Bacillus subtilis controls the signal decay of its cognate response regulator. J Bacteriol 186:2655–2663PubMedCrossRefGoogle Scholar
  6. Andersen J, Delihas N (1990) micF RNA binds to the 5′ end of ompF mRNA and to a protein from Escherichia coli. Biochemistry 29:9249–9256PubMedCrossRefGoogle Scholar
  7. Appleby JL, Parkinson JS, Bourret RB (1996) Signal transduction via the multi-step phosphorelay: not necessarily a road less traveled. Cell 86:845–848PubMedCrossRefGoogle Scholar
  8. Baldassare JJ, Rhinehart KB, Silbert DF (1976) Modifications of membrane lipid: physical properties in relation to fatty acid structure. Biochemistry 15:2986–2994PubMedCrossRefGoogle Scholar
  9. Bayles DO, Wilkinson BJ (2000) Osmoprotectants and cryoprotectants for Listeria monocytogenes. Lett Appl Microbiol 30:23–27PubMedCrossRefGoogle Scholar
  10. Becker LA, Evans SN, Hutkins RW, Benson AK (2000) Role of sigma(B) in adaptation of Listeria manocytogenes to growth at low temperature. J Bacteriol 182:7083–7087PubMedCrossRefGoogle Scholar
  11. Beckering CL, Steil L, Weber MHW, Volker U, Marahiel MA (2002) Genomewide transcriptional analysis of the cold shock response in Bacillus subtilis. J Bacteriol 184:6395–6402PubMedCrossRefGoogle Scholar
  12. Brandi A, Pon CL, Gualerzi CO (1994) Interaction of the main cold shock protein CS 7.4 (CspA) of Escherichia coli with the promoter region of HNS. Biochimie 76:1090–1098PubMedCrossRefGoogle Scholar
  13. Broeze RJ, Solomon CJ, Pope DH (1978) Effects of low temperature on in vivo and in vitro protein synthesis in Escherichia coli and Pseudomonas fluorescens. J Bacteriol 134:861–874PubMedGoogle Scholar
  14. Browse J, Xin Z (2001) Temperature sensing and cold acclimation. Curr Opin Plant Biol 4:241–246PubMedCrossRefGoogle Scholar
  15. Carty SM, Sreekumar KR, Raetz CR (1999) Effect of cold shock on lipid A biosynthesis in Escherichia coli. Induction at 12 degrees C of an acyltransferase specific for palmitoleoyl-acyl carrier protein. J Biol Chem 274:9677–9685PubMedCrossRefGoogle Scholar
  16. Chamot D, Owttrim GW (2000) Regulation of cold shock-induced RNA helicase gene expression in the Cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 182:1251–1256PubMedCrossRefGoogle Scholar
  17. Chamot D, Magee WC, Yu E, Owttrim GW (1999) A cold shock-induced cyanobacterial RNA helicase. J Bacteriol 181:1728–1732PubMedGoogle Scholar
  18. Chattopadhyay MK, Jagannadham MV, Vairamani M, Shivaji S (1997) Carotenoid pigments of an antarctic psychrotrophic bacterium Micrococcus roseus: temperature dependent biosynthesis, structure and interaction with synthetic membranes. Biochem Biophys Res Commun 239:85–90PubMedCrossRefGoogle Scholar
  19. Cronan JE Jr, Gelmann EP (1973) An estimate of the minimum amount of unsaturated fatty acid required for growth of Escherichia coli. J Biol Chem 248:1188–1195PubMedGoogle Scholar
  20. Cybulski LE, Albanesi D, Mansilla MC, Altabe S, Aguilar PS, de Mendoza D (2002) Mechanism of membrane fluidity optimization: isothermal control of the Bacillus subtilis acyl lipid desaturase. Mol Microbiol 45:1379–1388PubMedCrossRefGoogle Scholar
  21. Cybulski LE, del Solar G, Craig PO, Espinosa M, de Mendoza D (2004) Bacillus subtilis DesR functions as a phosphorylation-activated switch to control membrane lipid fluidity. J Biol Chem 279:39340–39347PubMedCrossRefGoogle Scholar
  22. Dammel CS, Noller HF (1995) Suppression of a cold-sensitive mutation in 16S rRNA by overexpression of a novel ribosome-binding factor, RbfA. Genes Dev 9:626–637PubMedCrossRefGoogle Scholar
  23. Das HK, Goldstein A (1968) Limited capacity for protein synthesis at zero degrees centigrade in Escherichia coli. J Mol Biol 31:209–226PubMedCrossRefGoogle Scholar
  24. de Wulf P, Akerley BJ, Lin EC (2000) Presence of the Cpx system in bacteria. Microbiology 146:247–248PubMedGoogle Scholar
  25. Denich TJ, Beaudette LA, Lee H, Trevors JT (2003) Effect of selected environmental and physico-chemical factors on bacterial cytoplasmic membranes. J Microbiol Meth 52:149–182CrossRefGoogle Scholar
  26. Dersch P, Kneip S, Bremer E (1994) The nucleoid-associated DNA-binding protein H-NS is required for the efficient adaptation of Escherichia coli K-12 to a cold environment. Mol Gen Genet 245:255–259PubMedCrossRefGoogle Scholar
  27. Diaz AR, Mansilla MC, Vila AJ, de Mendoza D (2002) Membrane topology of the acyl-lipid desaturase from Bacillus subtilis. J Biol Chem 277:48099–48106PubMedCrossRefGoogle Scholar
  28. Dorman CJ, Hinton JCD, Free A (1999) Domain organization and oligomerization among H-NS-like nucleoid-associated proteins in bacteria. Trends Microbiol 7:124–128PubMedCrossRefGoogle Scholar
  29. Drlica K (1992) Control of bacterial DNA supercoiling. Mol Microbiol 6:425–433PubMedCrossRefGoogle Scholar
  30. Epand RM (1998) Lipid polymorphism and protein–lipid interactions. Biochim Biophys Acta 1376:353–368PubMedGoogle Scholar
  31. Eriksson S, Hurme R, Rhen M (2002) Low temperature sensors in bacteria. Philos Trans R Soc Lond B 357:887–893CrossRefGoogle Scholar
  32. Ermolenko DN, Makhatadze GI (2002) Bacterial cold-shock proteins. Cell Mol Life Sci 59:1902–1913PubMedCrossRefGoogle Scholar
  33. Falconi M, Colonna B, Prosseda G, Micheli G, Gualerzi CO (1998) Thermoregulation of Shigella and Escherichia coli EIEC pathogenicity. A temperature-dependent structural transition of DNA modulates accessibility of virF promoter to transcriptional repressor H-NS. EMBO J 17:7033–7043PubMedCrossRefGoogle Scholar
  34. Farewell A, Neidhardt FC (1998) Effect of temperature on in vivo protein synthetic capacity in Escherichia coli. J Bacteriol 180:4704–4710PubMedGoogle Scholar
  35. Friedman H, Lu P, Rich A (1971) Temperature control of initiation of protein synthesis in Escherichia coli. J Mol Biol 61:105–121PubMedCrossRefGoogle Scholar
  36. Fujii DK, Fulco AJ (1977) Biosynthesis of unsaturated fatty acids by Bacilli. Hyperinduction and modulation of desaturase synthesis. J Biol Chem 252:3660–3670PubMedGoogle Scholar
  37. Fulco AJ (1969) The biosynthesis of unsaturated fatty acids by Bacilli. I. Temperature induction of the desaturation reaction. J Biol Chem 244:889–895PubMedGoogle Scholar
  38. Garwin JL, Cronan JE Jr (1980) Thermal modulation of fatty acid synthesis in Escherichia coli does not involve de novo enzyme synthesis. J Bacteriol 141:1457–1459PubMedGoogle Scholar
  39. Garwin JL, Klages AL, Cronan JE Jr (1980) Structural, enzymatic and genetic studies of beta-ketoacyl-acyl carrier protein synthases I and II of Escherichia coli. J Biol Chem 255:11949–11956PubMedGoogle Scholar
  40. Giangrossi M, Giuliodori AM, Gualerzi CO, Pon CL (2002) Selective expression of the beta-subunit of nucleoid-associated protein HU during cold shock in Escherichia coli. Mol Microbiol 44:205–216PubMedCrossRefGoogle Scholar
  41. Goldstein J, Pollitt NS, Inouye M (1990) Major cold-shock protein of Escherichia coli. Proc Natl Acad Sci USA 87:283–287PubMedCrossRefGoogle Scholar
  42. Goodchild A, Saunders NFW, Ertan H, Raftery M, Guilhaus M, Curmi PMG, Cavicchioli R (2004) A proteomic determination of cold adaptation in the Antarctic archaeon, Methanococcoides burtonii. Mol Microbiol 53:309–321PubMedCrossRefGoogle Scholar
  43. Grau R, Gardiol D, Glikin GC, de Mendoza D (1994) DNA supercoiling and thermal regulation of unsaturated fatty acid synthesis in Bacillus subtilis. Mol Microbiol 11:933–941PubMedCrossRefGoogle Scholar
  44. Graumann PL, Marahiel MA (1999) Cold shock response in Bacillus subtilis. J Mol Microbiol Biotechnol 1:203–209PubMedGoogle Scholar
  45. Graumann P, Wendrich TM, Weber MH, Schröder K, Marahiel MA (1997) A family of cold shock proteins in Bacillus subtilis is essential for cellular growth and for efficient protein synthesis at optimal and low temperatures. Mol Microbiol 25:741–756PubMedCrossRefGoogle Scholar
  46. Gulig PA, Danbara H, Guiney DG, Lax AJ, Norel F, Rhen M (1993) Molecular analysis of spv virulence genes of the Salmonella virulence plasmid. Mol Microbiol 7:825–830PubMedCrossRefGoogle Scholar
  47. Hasegawa Y, Kawada N, Nosho Y (1980) Change in chemical composition of membrane of Bacillus caldotenax after shifting the growth temperature. Arch Microbiol 126:103–108PubMedCrossRefGoogle Scholar
  48. Hebraud M, Potier P (1999) Cold shock response and low temperature adaption in psychrotrophic bacteria. J Mol Microbiol Biotechnol 1:211–219PubMedGoogle Scholar
  49. Hecker M, Pane-Faree J, Volker U (2007) SigB-dependent general stress response in Bacillus subtilis and related Gram-positive bacteria. Annu Rev Microbiol 61:215–236PubMedCrossRefGoogle Scholar
  50. Heipieper HJ, De Bont JAM (1994) Adaptation of Pseudomonas putida S12 to ethanol and toluene at the level of fatty acid composition of membranes. Appl Environ Microbiol 60:4440–4444PubMedGoogle Scholar
  51. Heipieper HJ, Meinhardt F, Segura A (2003) The cis-trans isomerase of unsaturated fatty acids in Pseudomonas and Vibrio: biochemistry, molecular biology and physiological function of a unique stress adaptive mechanism. FEMS Microbiol Lett 229:1–7PubMedCrossRefGoogle Scholar
  52. Hoch JA (2000) Two component and phosphorelay signal transduction. Curr Opin Microbiol 3:165–170PubMedCrossRefGoogle Scholar
  53. Hoe NP, Gougen JD (1993) Temperature sensing in Yersinia pestis: translation of the LerF activator protein is thermally regulated. J Bacteriol 175:7901–7909PubMedGoogle Scholar
  54. Hurme R, Rhen M (1998) Temperature sensing in bacterial gene regulation—what it all boils down to. Mol Microbiol 30:1–6PubMedCrossRefGoogle Scholar
  55. Hurme R, Berndt K, Namork D, Rhen M (1996) DNA binding exerted by a bacterial gene regulator with extensive coiled coil domains. J Biol Chem 272:12626–12631Google Scholar
  56. Hurme R, Berndt K, Normark SJ, Rhen M (1997) A proteinaceous gene regulatory thermometer in Salmonella. Cell 90:55–64PubMedCrossRefGoogle Scholar
  57. Inaba M, Suzuki I, Szalontai B, Kanesaki Y, Los DA, Hayashi H, Murata N (2003) Gene-engineered rigidification of membrane lipids enhances the cold inducibility of gene expression in Synechocystis. J Biol Chem 278:12191–12198PubMedCrossRefGoogle Scholar
  58. Jagannadham MV, Jayathirtha Rao V, Shivaji S (1991) The major carotenoid pigment of a psychrotrophic Micrococcus roseus: purification, structure and interaction of the pigment with synthetic membranes. J Bacteriol 173:7911–7917PubMedGoogle Scholar
  59. Jagannadham MV, Chattopadhyay MK, Shivaji S (1996a) The major carotenoid pigment of a psychrotrophic Micrococcus roseus strain: fluorescence properties of the pigment and its binding to membranes. Biochem Biophys Res Commun 220:724–728PubMedCrossRefGoogle Scholar
  60. Jagannadham MV, Narayanan K, MohanRao C, Shivaji S (1996b) In vivo characteristics and localisation of carotenoid pigments in psychrotrophic and mesophilic Micrococcus roseus using photoacoustic spectroscopy. Biochem Biophys Res Commun 227:221–226PubMedCrossRefGoogle Scholar
  61. Jagannadham MV, Chattopadhyay MK, Subbalakshmi C, Vairamani M, Narayanan K, MohanRao C, Shivaji S (2000) Carotenoids of an Antarctic psychrotolerant bacterium Sphingobacterium antarcticus and a mesophilic bacterium Sphingobacterium multivorum. Arch Microbiol 173:418–424PubMedCrossRefGoogle Scholar
  62. Jones PG, Inouye M (1994) The cold shock response: a hot topic. Mol Microbiol 11:811–818PubMedCrossRefGoogle Scholar
  63. Jones PG, Inouye M (1996) RbfA, a 305 ribosomal binding factor, is a cold-shock protein whose absence triggers the cold-shock response. Mol Microbiol 21:1207–1218PubMedCrossRefGoogle Scholar
  64. Jones PG, VanBogelan RA, Neidhardt FC (1987) Induction of proteins in response to low temperature in Escherichia coli. J Bacteriol 169:2092–2095PubMedGoogle Scholar
  65. Jones PG, Krah R, Tafuri SR, Wolffe AP (1992) DNA gyrase, CS7.4, and the cold shock response in Escherichia coli. J Bacteriol 174:5798–5802PubMedGoogle Scholar
  66. Jones PG, Mitta M, Kim Y, Jiang W, Inouye M (1996) Cold shock induces a major ribosomal-associated protein that unwinds double-stranded RNA in Escherichia coli. Proc Natl Acad Sci USA 93:76–80PubMedCrossRefGoogle Scholar
  67. Kaan T, Homuth G, Mäder U, Bandow J, Schweder T (2002) Genome-wide transcriptional profiling of the Bacillus subtilis cold-shock response. Microbiology 148:3441–3455PubMedGoogle Scholar
  68. Kandror O, DeLeon A, Goldberg AL (2002) Trehalose synthesis is induced upon exposure of Escherichia coli to cold and is essential for viability at low temperatures. Proc Natl Acad Sci USA 99:9727–9732PubMedCrossRefGoogle Scholar
  69. Kaneda T (1991) Iso- and anteiso- fatty acids in bacteria: biosynthesis, function and taxonomic significance. Microbiol Rev 55:288–302PubMedGoogle Scholar
  70. Kiran MD, Prakash JSS, Annapoorni S, Dube S, Kusano T, Okuyama H, Murata N, Shivaji S (2004) Psychrophilic Pseudomonas syringae required trans monounsaturated fatty acid for growth at higher temperature. Extremophiles 8:401–410PubMedCrossRefGoogle Scholar
  71. Kiran MD, Annapoorni S, Suzuki I, Murata N, Shivaji S (2005) Cis-trans isomerase gene in psychrophilic Pseudomonas syringae is constitutively expressed during growth and under conditions of temperature and solvent stress. Extremophiles 9:117–125PubMedCrossRefGoogle Scholar
  72. Ko R, Smith LT, Smith GM (1994) Glycine betaine confers enhanced osmotolerance and cryotolerance on Listeria monocytogenes. J Bacteriol 176:426–431PubMedGoogle Scholar
  73. Kunst F, Ogasawara N, Moszer I, Albertini AM, Alloni G, Azevedo V, Bertero MG, Bessieres P, Bolotin A, Borchert S, Borriss R, Boursier L, Brans A, Brauwn M, Brignell SC, Born S, Brouillet S, Bruschi SV, Caldwell B, Capuano V, Carter NM, Choi SK, Codani SJ, Connerton IF et al (1997) The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390:249–256PubMedCrossRefGoogle Scholar
  74. La Teana A, Brandi A, Falconi M, Spurio R, Pon CL, Gualerzi CO (1991) Identification of a cold shock transcriptional enhancer of the Escherichia coli gene encoding nucleoid protein H-NS. Proc Natl Acad Sci USA 88:10907–10911PubMedCrossRefGoogle Scholar
  75. Lai EC (2003) RNA sensors and riboswitches: self-regulating messages. Curr Biol 13:R285–R291PubMedCrossRefGoogle Scholar
  76. Lease RA, Belfort M (2000) A trans-acting RNA as a control switch in Escherichia coli: DsrA modulates function by forming alternative structures. Proc Natl Acad Sci USA 97:9919–9924PubMedCrossRefGoogle Scholar
  77. Los DA, Suzuki I, Zinchenko VV, Murata N (2008) Stress responses in Synechocystis: regulated genes and regulatory systems. In: Herrero A, Flores E (eds) The cyanobacteria: molecular biology, genetics and evolution. Horizon Scientific Press, Wymondham, pp 117–158Google Scholar
  78. Lost I, Dreyfus M (1994) mRNAs can be stabilized by DEAD-box proteins. Nature 372:193–196CrossRefGoogle Scholar
  79. Maeda K, Imae Y (1979) Thermosensory transduction in Escherichia coli: inhibition of the thermoresponse by l-serine. Proc Natl Acad Sci USA 76:91–95PubMedCrossRefGoogle Scholar
  80. Maeda K, Imae Y, Shioi JI, Oosawa F (1976) Effect of temperature on motility and chemotaxis of Escherichia coli. J Bacteriol 127:1039–1046PubMedGoogle Scholar
  81. Majdalani N, Cunning C, Sledjeski D, Elliot T, Gottesman S (1998) DsrA RNA regulates translation of RpoS message by an anti-antisense mechanism independent of its action as an antisilencer of transcription. Proc Natl Acad Sci USA 95:12462–12467PubMedCrossRefGoogle Scholar
  82. Majdalani N, Vanderpool CK, Gottesman S (2005) Bacterial small RNA regulators. Crit Rev Biochem Mol Biol 40:93–113PubMedCrossRefGoogle Scholar
  83. Mansilla MC, Aguilar PS, Albanesi D, Cybulski LE, Altabe S, de Mendoza D (2003) Regulation of fatty acid desaturation in Bacillus subtilis. Prostaglandins Leukot Essent Fatty Acids 68:187–190PubMedCrossRefGoogle Scholar
  84. Mansilla MC, Albanesi D, Cybulski LE, de Mendoza D (2005) Molecular mechanisms of low temperature sensing bacteria. Ann Hepatol 4:216–217PubMedGoogle Scholar
  85. Marr AG, Ingraham JJ (1962) Effect of temperature on the composition of fatty acids in Escherichia coli. J Bacteriol 84:1260–1267PubMedGoogle Scholar
  86. Medigue 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 Nilsson J, Parrilli E, Rocha EPC, Rouy Z, Sekowska S, Tutino ML, Vallenet D, Heijne SJ, Danchin A (2005) Coping with cold: the genome of the versatile marine Antarctica bacterium Pseudoalteromonas haloplanktis TAC125. Genome Res 15:1325–1335PubMedCrossRefGoogle Scholar
  87. Methe 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 102:10913–10918PubMedCrossRefGoogle Scholar
  88. Mikami K, Kanesaki Y, Suzuki I, Murata N (2002) The histidine kinase Hik33 perceives osmotic stress and low-temperature stress in Synechocystis sp. PCC 6803. Mol Microbiol 46:905–915PubMedCrossRefGoogle Scholar
  89. Mikami K, Suzuki I, Murata N (2003) 4 sensors of abiotic stress in Synechocystis. Top Curr Gen 4:103–119Google Scholar
  90. Mizuno T, Imae Y (1984) Conditional inversion of the thermoresponse in Escherichia coli. J Bacteriol 159:360–367PubMedGoogle Scholar
  91. Morita NA, Shibahara K, Yamamoto K, Shinkai G, Kajimoto G, Okuyama H (1993) Evidence for cis-trans isomerization of a double bond in the fatty acids of the psychrophilic bacterium Vibrio sp. strain ABE-1. J Bacteriol 175:916–918PubMedGoogle Scholar
  92. Murata N, Wada H (1995) Acyl lipid desaturases and their importance in the tolerance and acclimatization to cold of cyanobacteria. Biochem J 308:1–8PubMedGoogle Scholar
  93. Murata N, Wada H, Gombos Z (1992) Modes of fatty-acid desaturation in cyanobacteria. Plant Cell Physiol 33:933–941Google Scholar
  94. Nara T, Lee L, Imae Y (1991) Thermosensing ability of Trg and Tap chemoreceptors in Escherichia coli. J Bacteriol 173:1120–1124PubMedGoogle Scholar
  95. Nara T, Kawagishi I, Nishiyama S, Homma M, Imae Y (1996) Modulation of the thermosensing profile of the Escherichia coli aspartate receptor Tar by covalent modification of its methyl-accepting sites. J Biol Chem 271:17932–17936PubMedCrossRefGoogle Scholar
  96. Narberhaus F, Waldminghaus T, Chowdhury S (2005) RNA thermometers. FEMS Microbiol Rev 20:1–14Google Scholar
  97. Neuhaus K, Rapposch S, Francis KP, Scherer S (2000) Restart of exponential growth of cold-shocked Yersinia enterocolitica occurs after downregulation of cspAl/A2 mRNA. J Bacteriol 182:3285–3288PubMedCrossRefGoogle Scholar
  98. Nishida I, Murata N (1996) Chilling sensitivity in plants and cyanobacteria: the crucial contribution of membrane lipids. Annu Rev Plant Physiol Plant Mol Biol 47:541–568PubMedCrossRefGoogle Scholar
  99. Okuyama H, Sasaki S, Higashi S, Murata N (1990) A trans-unsaturated fatty acid in a psychrophilic bacterium, Vibrio sp. strain ABE-1. J Bacteriol 172:3515–3518PubMedGoogle Scholar
  100. Okuyama H, Okajima N, Sasaki S, Higashi S, Murata N (1991) The cis/trans isomerization of the double bond of a fatty acid as a strategy for adaptation to changes in ambient temperature in the psychrophilic bacterium, Vibrio sp. strain ABE-1. Biochim Biophys Acta 1084:13–20PubMedGoogle Scholar
  101. Oosawa K, Imae Y (1983) Glycerol and ethylene glycol: members of a new class of repellents of Escherichia coli chemotaxis. J Bacteriol 154:104–112PubMedGoogle Scholar
  102. Oosawa K, Imae Y (1984) Demethylation of methyl-accepting chemotaxis proteins in Escherichia coli induced by the repellents glycerol and ethylene glycol. J Bacteriol 157:576–581PubMedGoogle Scholar
  103. Park H, Saha SK, Inouye M (1998) Two-domain reconstitution of a functional protein histidine kinase. Proc Natl Acad Sci USA 95:6728–6732PubMedCrossRefGoogle Scholar
  104. Prakash JSS, Zorina A, Kupriyanova E, Sinetova M, Suzuki I, Murata N, Los DA (2009) DNA supercoiling regulates the stress-inducible expression of genes in Synechocystis sp. PCC 6803. Mol Biosyst 5:1904–1912CrossRefPubMedGoogle Scholar
  105. Ray MK, Seshu Kumar G, Shivaji S (1994a) Phosphorylation of membrane proteins in response to temperature in an Antarctic Pseudomonas syringae. Microbiology 140:3217–3223PubMedCrossRefGoogle Scholar
  106. Ray MK, Seshu Kumar G, Shivaji S (1994b) Tyrosine phosphorylation of a cytosolic protein from the antarctic psychrotrophic bacterium Pseudomonas syringae. FEMS Microbiol Lett 122:49–54CrossRefGoogle Scholar
  107. Ray MK, Seshu Kumar G, Shivaji S (1994c) Phosphorylation of lipopolysaccharides in the Antarctic psychrotroph Pseudomonas syringae: a possible role in temperature adaptation. J Bacteriol 176:4243–4249PubMedGoogle Scholar
  108. Repoila F, Gottesman S (2003) Temperature sensing by the dsrA promoter. J Bacteriol 185:6609–6614PubMedCrossRefGoogle Scholar
  109. Rodrigues DF, Tiedje M (2008) Coping with our cold planet. Appl Environ Microbiol 74:1677–1686PubMedCrossRefGoogle Scholar
  110. Romby P, Ehresmann C (2003) At the flick of a switch: a Listeria mRNA turns on and off its own expression in response to temperature. The ELSO Gazette http://www.the-elso-gazette.org/magazines/issue14/mreviews/mreviews1.asp (Issue 14 Apr 2003)
  111. Rowbury RJ (2003) Temperature effects on biological systems: introduction. Sci Prog 86:1–8PubMedCrossRefGoogle Scholar
  112. Sakamoto T, Murata N (2002) Regulation of the desaturation of fatty acids and its role in tolerance to cold and salt stress. Curr Opin Microbiol 5:206–210CrossRefGoogle Scholar
  113. Sato N, Murata N (1980) Temperature shift-induced responses in lipids in the blue-green alga, Anabaena variabilis. The central role of diacylmonogalactosylglycerol in thermo-adaptation. Biochim Biophys Acta 619:353–366PubMedGoogle Scholar
  114. Sato N, Murata N, Miura Y, Ueta N (1979) Effect of growth temperature on lipid and fatty acid compositions in the blue-green algae, Anabaena variabilis and Anacystis nidulans. Biochim Biophys Acta 572:19–28PubMedGoogle Scholar
  115. Shivaji S, Kiran MD, Chintalapati S (2007) Perception and transduction of low temperature in bacteria. In: Gerday C, Glansdorff N (eds) Physiology and biochemistry of extremophiles. ASM Press, Washington, pp 194–207Google Scholar
  116. Singh AK, Pindi PK, Dube S, Sundareswaran VR, Shivaji S (2009) Importance of trmE for growth of the psychrophile Pseudomonas syringae at low temperatures. Appl Environ Microbiol 75(13):4419−4426 (Epub 8 May 2009)Google Scholar
  117. Sledjeski DD, Gupta A, Gottesman S (1996) The small RNA, DsrA, is essential for the low temperature expression of RpoS during exponential growth in Escherichia coli. EMBO J 15:3993–4000PubMedGoogle Scholar
  118. Sonnenfield JM, Burns CM, Higgins CF, Hinton J (2001) The nucleoid-associated protein StpA binds curved DNA, has a greater DNA-binding affinity than H-NS and is present in significant levels in hns mutants. Biochimie 83:243–249PubMedCrossRefGoogle Scholar
  119. Straley S, Perry RD (1995) Environmental modulation of gene expression and pathogenesis in Yersinia. Trends Microbiol 3:310–317PubMedCrossRefGoogle Scholar
  120. Suutari M, Laakso S (1994) Microbial fatty acids and thermal adaptation. Crit Rev Microbiol 20:285–328PubMedCrossRefGoogle Scholar
  121. Suzuki I, Los DA, Kanesaki Y, Mikami Y, Murata N (2000a) The pathway for perception and transduction of low-temperature signals in Synechocystis. EMBO J 19:1327–1334PubMedCrossRefGoogle Scholar
  122. Suzuki I, Los DA, Murata N (2000b) Perception and transduction of low temperature signals to induce desaturation of fatty acids. Biochem Soc Trans 28:626–630CrossRefGoogle Scholar
  123. Suzuki I, Kanasaki Y, Mikami K, Kanehisa M, Murata N (2001) Cold regulated genes under the control of cold sensor hik33 in Synechocystis. Mol Microbiol 40:235–245PubMedCrossRefGoogle Scholar
  124. Szalontai B, Nishiyaina Y, Gombos Z, Murata N (2000) Membrane dynamics as seen by Fourier transform infrared spectroscopy in a cyanobacterium, Synechocystis PCC 6803—the effects of lipid unsaturation and the protein-to-lipid ratio. Biochim Biophys Acta Biomembr 1509:409–410CrossRefGoogle Scholar
  125. Takeuchi Y, Ohnishi SI, Ishinaga M, Kito M (1978) Spin-labeling of Escherichia coli membrane by enzymatic synthesis of phosphatidylglycerol and divalent cation-induced interaction of phosphatidylglycerol with membrane proteins. Biochim Biophys Acta 506:54–63PubMedCrossRefGoogle Scholar
  126. Takeuchi Y, Ohnishi SI, Ishinaga M, Kito M (1981) Dynamic states of phospholipids in Escherichia coli B membrane. Electron spin resonance studies with biosynthetically generated phospholipid spin labels. Biochim Biophys Acta 646:119–125PubMedCrossRefGoogle Scholar
  127. Taylor BL, Zhulin IB (1999) PAS domains: internal sensors of oxygen, redox potential and light. Microbiol Mol Biol Rev 63:479–506PubMedGoogle Scholar
  128. Tobe T, Yoshokawa M, Mizuno T, Sasakawa C (1993) Transcriptional control of the invasion regulatory gene virB of Shigella exneri: activation by VirF and repression by H-NS. J Bacteriol 175:6142–6149PubMedGoogle Scholar
  129. Tse-Dinh YC, Qi H, Menzel H (1997) DNA supercoiling and bacterial adaptation: thermotolerance and thermoresistance. Trends Microbiol 5:323–326PubMedCrossRefGoogle Scholar
  130. Vigh L, Los DA, Horvath I, Murata N (1993) The primary signal in the biological perception of temperature: Pd-catalyzed hydrogenation of membrane lipids stimulated the expression of the desA gene in Synechocystis PCC6803. Proc Natl Acad Sci USA 90:9090–9094PubMedCrossRefGoogle Scholar
  131. Wada H, Murata N (1989) Synechocystis PCC6803 mutants defective in desaturation of fatty acids. Plant Cell Physiol 30:971–978Google Scholar
  132. Wada H, Murata N (1990) Temperature-induced changes in the fatty acid composition of the cyanobacterium, Synechocystis PCC6803. Plant Physiol 92:1062–1069PubMedCrossRefGoogle Scholar
  133. Wada M, Kano Y, Ogawa T, Okazaki T, Imamoto F (1988) Construction and characterization of the deletion mutant of hupA and hupB genes in Escherichia coli. J Mol Biol 204:581–591PubMedCrossRefGoogle Scholar
  134. Weber MHW, Marahiel MA (2003) Bacterial cold shock responses. Sci Prog 86:9–75PubMedCrossRefGoogle Scholar
  135. Weber MH, Klein W, Müller L, Niess UM, Marahiel MA (2001) Role of the Bacillus subtilis fatty acid desaturase in membrane adaptation during cold shock. Mol Microbiol 39(5):1321–1329PubMedCrossRefGoogle Scholar
  136. Williams RM, Rimsky S (1997) Escherichia coli nucleoid associated protein H-NS: a central controller of gene regulatory networks. FEMS Microbiol Lett 156:175–185PubMedCrossRefGoogle Scholar
  137. Woldringh CL, Jensen PR, Westerhoff HV (1995) Structure and partitioning of bacterial DNA: determined by a balance of compaction and expansion forces? FEMS Microbiol Lett 131:235–242PubMedCrossRefGoogle Scholar
  138. Wollenweber HW, Schlecht S, Luderitz O, Rietschel ET (1983) Fatty acid in lipopolysaccharides of Salmonella species grown at low temperature. Identification and position. Eur J Biochem 130:167–171PubMedCrossRefGoogle Scholar
  139. Xia B, Ke H, Shinde U, Inouye M (2003) The role of RbfA in 16S rRNA processing and cell growth at low temperature in Escherichia coli. J Mol Biol 332:575–584PubMedCrossRefGoogle Scholar
  140. Yu E, Owttrim GW (2000) Characterization of the cold stress-induced cyanobacterial DEAD-box protein CrhC as an RNA helicase. Nucl Acids Res 28:3926–3934PubMedCrossRefGoogle Scholar
  141. Zhang W, Shi L (2005) Distribution and evolution of multiple-step phosphorelay in prokaryotes: lateral domain recruitment involved in the formation of hybrid-type histidine kinases. Microbiology 151:2159–2173PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Centre for Cellular and Molecular BiologyHyderabadIndia
  2. 2.Department of Plant Sciences, School of Life SciencesUniversity of HyderabadHyderabadIndia

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