Cellular and Molecular Life Sciences

, Volume 66, Issue 16, pp 2661–2676 | Cite as

Microbial thermosensors

  • Birgit Klinkert
  • Franz NarberhausEmail author


Temperature is among the most important of the parameters that free-living microbes monitor. Microbial physiology needs to be readjusted in response to sudden temperature changes. When the ambient temperature rises or drops to potentially harmful levels, cells mount protective stress responses—so-called heat or cold shock responses, respectively. Pathogenic microorganisms often respond to a temperature of around 37°C by inducing virulence gene expression. There are two main ways in which temperature can be measured. Often, the consequences of a sudden temperature shift are detected. Such indirect signals are known to be the accumulation of denatured proteins (heat shock) or stalled ribosomes (cold shock). However, this article focuses solely on direct thermosensors. Since the conformation of virtually every biomolecule is susceptible to temperature changes, primary sensors include DNA, RNA, proteins and lipids.


Heat shock Cold shock Temperature Sensor Thermometer Stress response Virulence Gene regulation 


  1. 1.
    Guisbert E, Yura T, Rhodius VA, Gross CA (2008) Convergence of molecular, modeling, and systems approaches for an understanding of the Escherichia coli heat shock response. Microbiol Mol Biol Rev 72:545–554PubMedCrossRefGoogle Scholar
  2. 2.
    Zhao K, Liu M, Burgess RR (2005) The global transcriptional response of Escherichia coli to induced σ32 protein involves σ32 regulon activation followed by inactivation and degradation of σ32 in vivo. J Biol Chem 280:17758–17768PubMedCrossRefGoogle Scholar
  3. 3.
    Nonaka G, Blankschien M, Herman C, Gross CA, Rhodius VA (2006) Regulon and promoter analysis of the E. coli heat-shock factor, σ32, reveals a multifaceted cellular response to heat stress. Genes Dev 20:1776–1789PubMedCrossRefGoogle Scholar
  4. 4.
    Wade JT, Roa DC, Grainger DC, Hurd D, Busby SJ, Struhl K, Nudler E (2006) Extensive functional overlap between sigma factors in Escherichia coli. Nat Struct Mol Biol 13:806–814PubMedCrossRefGoogle Scholar
  5. 5.
    Meibom KL, Dubail I, Dupuis M, Barel M, Lenco J, Stulik J, Golovliov I, Sjostedt A, Charbit A (2008) The heat-shock protein ClpB of Francisella tularensis is involved in stress tolerance and is required for multiplication in target organs of infected mice. Mol Microbiol 67:1384–1401PubMedCrossRefGoogle Scholar
  6. 6.
    Schumann W (2007) Thermosensors in eubacteria: role and evolution. J Biosci 32:549–557PubMedCrossRefGoogle Scholar
  7. 7.
    Huston WM, Theodoropoulos C, Mathews SA, Timms P (2008) Chlamydia trachomatis responds to heat shock, penicillin induced persistence, and IFN-gamma persistence by altering levels of the extracytoplasmic stress response protease HtrA. BMC Microbiol 8:190PubMedCrossRefGoogle Scholar
  8. 8.
    Konkel ME, Tilly K (2000) Temperature-regulated expression of bacterial virulence genes. Microbes Infect 2:157–166PubMedCrossRefGoogle Scholar
  9. 9.
    Jin S, Song YN, Deng WY, Gordon MP, Nester EW (1993) The regulatory VirA protein of Agrobacterium tumefaciens does not function at elevated temperatures. J Bacteriol 175:6830–6835PubMedGoogle Scholar
  10. 10.
    Banta LM, Bohne J, Lovejoy SD, Dostal K (1998) Stability of the Agrobacterium tumefaciens VirB10 protein is modulated by growth temperature and periplasmic osmoadaption. J Bacteriol 180:6597–6606PubMedGoogle Scholar
  11. 11.
    Lai EM, Kado CI (1998) Processed VirB2 is the major subunit of the promiscuous pilus of Agrobacterium tumefaciens. J Bacteriol 180:2711–2717PubMedGoogle Scholar
  12. 12.
    Wei ZM, Sneath BJ, Beer SV (1992) Expression of Erwinia amylovora hrp genes in response to environmental stimuli. J Bacteriol 174:1875–1882PubMedGoogle Scholar
  13. 13.
    van Dijk K, Fouts DE, Rehm AH, Hill AR, Collmer A, Alfano JR (1999) The Avr (effector) proteins HrmA (HopPsyA) and AvrPto are secreted in culture from Pseudomonas syringae pathovars via the Hrp (type III) protein secretion system in a temperature- and pH-sensitive manner. J Bacteriol 181:4790–4797PubMedGoogle Scholar
  14. 14.
    Lanham PG, Mcllravey KI, Perombelon MCM (1991) Production of cell wall dissolving enzymes by Erwinia carotovora subsp. atroseptica in vitro at 27°C and 30°C. J Appl Microbiol 70:20–24CrossRefGoogle Scholar
  15. 15.
    Smirnova A, Li H, Weingart H, Aufhammer S, Burse A, Finis K, Schenk A, Ullrich MS (2001) Thermoregulated expression of virulence factors in plant-associated bacteria. Arch Microbiol 176:393–399PubMedCrossRefGoogle Scholar
  16. 16.
    Ermolenko DN, Makhatadze GI (2002) Bacterial cold-shock proteins. Cell Mol Life Sci 59:1902–1913PubMedCrossRefGoogle Scholar
  17. 17.
    Horn G, Hofweber R, Kremer W, Kalbitzer HR (2007) Structure and function of bacterial cold shock proteins. Cell Mol Life Sci 64:1457–1470PubMedCrossRefGoogle Scholar
  18. 18.
    El-Sharoud WM, Graumann PL (2007) Cold shock proteins aid coupling of transcription and translation in bacteria. Sci Prog 90:15–27PubMedCrossRefGoogle Scholar
  19. 19.
    Narberhaus F (1999) Negative regulation of bacterial heat shock genes. Mol Microbiol 31:1–8PubMedCrossRefGoogle Scholar
  20. 20.
    Crick F (1970) Central dogma of molecular biology. Nature 227:561–563PubMedCrossRefGoogle Scholar
  21. 21.
    Lopez-Garcia P, Forterre P (2000) DNA topology and the thermal stress response, a tale from mesophiles and hyperthermophiles. Bioessays 22:738–746PubMedCrossRefGoogle Scholar
  22. 22.
    Kataoka K, Mizushima T, Ogata Y, Miki T, Sekimizu K (1996) Heat shock-induced DNA relaxation in vitro by DNA gyrase of Escherichia coli in the presence of ATP. J Biol Chem 271:24806–24810PubMedCrossRefGoogle Scholar
  23. 23.
    Mizushima T, Kataoka K, Ogata Y, Inoue R, Sekimizu K (1997) Increase in negative supercoiling of plasmid DNA in Escherichia coli exposed to cold shock. Mol Microbiol 23:381–386PubMedCrossRefGoogle Scholar
  24. 24.
    Lopez-Garcia P, Forterre P (1997) DNA topology in hyperthermophilic archaea: reference states and their variation with growth phase, growth temperature, and temperature stresses. Mol Microbiol 23:1267–1279PubMedCrossRefGoogle Scholar
  25. 25.
    Pruss GJ, Drlica K (1989) DNA supercoiling and prokaryotic transcription. Cell 56:521–523PubMedCrossRefGoogle Scholar
  26. 26.
    Dorman CJ (1996) Flexible response: DNA supercoiling, transcription and bacterial adaptation to environmental stress. Trends Microbiol 4:214–216PubMedCrossRefGoogle Scholar
  27. 27.
    Dorman CJ, Corcoran CP (2008) Bacterial DNA topology and infectious disease. Nucleic Acids Res 37:672–678PubMedCrossRefGoogle Scholar
  28. 28.
    Bell SD, Jaxel C, Nadal M, Kosa PF, Jackson SP (1998) Temperature, template topology, and factor requirements of archaeal transcription. Proc Natl Acad Sci USA 95:15218–15222PubMedCrossRefGoogle Scholar
  29. 29.
    Katayama S, Matsushita O, Tamai E, Miyata S, Okabe A (2001) Phased A-tracts bind to the alpha subunit of RNA polymerase with increased affinity at low temperature. FEBS Lett 509:235–238PubMedCrossRefGoogle Scholar
  30. 30.
    Mizuno T (1987) Random cloning of bent DNA segments from Escherichia coli chromosome and primary characterization of their structures. Nucleic Acids Res 15:6827–6841PubMedCrossRefGoogle Scholar
  31. 31.
    Nickerson CA, Achberger EC (1995) Role of curved DNA in binding of Escherichia coli RNA polymerase to promoters. J Bacteriol 177:5756–5761PubMedGoogle Scholar
  32. 32.
    Katayama S, Matsushita O, Jung CM, Minami J, Okabe A (1999) Promoter upstream bent DNA activates the transcription of the Clostridium perfringens phospholipase C gene in a low temperature-dependent manner. EMBO J 18:3442–3450PubMedCrossRefGoogle Scholar
  33. 33.
    Los DA (2004) The effect of low-temperature-induced DNA supercoiling on the expression of the desaturase genes in Synechocystis. Cell Mol Biol (Noisy-le-Grand) 50:605–612Google Scholar
  34. 34.
    Prosseda G, Falconi M, Giangrossi M, Gualerzi CO, Micheli G, Colonna B (2004) The virF promoter in Shigella: more than just a curved DNA stretch. Mol Microbiol 51:523–537PubMedCrossRefGoogle Scholar
  35. 35.
    Tupper AE, Owen-Hughes TA, Ussery DW, Santos DS, Ferguson DJ, Sidebotham JM, Hinton JC, Higgins CF (1994) The chromatin-associated protein H-NS alters DNA topology in vitro. EMBO J 13:258–268PubMedGoogle Scholar
  36. 36.
    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
  37. 37.
    Ono S, Goldberg MD, Olsson T, Esposito D, Hinton JC, Ladbury JE (2005) H-NS is a part of a thermally controlled mechanism for bacterial gene regulation. Biochem J 391:203–213PubMedCrossRefGoogle Scholar
  38. 38.
    Atlung T, Ingmer H (1997) H-NS: a modulator of environmentally regulated gene expression. Mol Microbiol 24:7–17PubMedCrossRefGoogle Scholar
  39. 39.
    Colonna B, Casalino M, Fradiani PA, Zagaglia C, Naitza S, Leoni L, Prosseda G, Coppo A, Ghelardini P, Nicoletti M (1995) H-NS regulation of virulence gene expression in enteroinvasive Escherichia coli harboring the virulence plasmid integrated into the host chromosome. J Bacteriol 177:4703–4712PubMedGoogle Scholar
  40. 40.
    Rohde JR, Luan XS, Rohde H, Fox JM, Minnich SA (1999) The Yersinia enterocolitica pYV virulence plasmid contains multiple intrinsic DNA bends which melt at 37°C. J Bacteriol 181:4198–4204PubMedGoogle Scholar
  41. 41.
    Madrid C, Nieto JM, Paytubi S, Falconi M, Gualerzi CO, Juarez A (2002) Temperature- and H-NS-dependent regulation of a plasmid-encoded virulence operon expressing Escherichia coli hemolysin. J Bacteriol 184:5058–5066PubMedCrossRefGoogle Scholar
  42. 42.
    Dorman CJ, Porter ME (1998) The Shigella virulence gene regulatory cascade: a paradigm of bacterial gene control mechanisms. Mol Microbiol 29:677–684PubMedCrossRefGoogle Scholar
  43. 43.
    Tobe T, Yoshikawa M, Mizuno T, Sasakawa C (1993) Transcriptional control of the invasion regulatory gene virB of Shigella flexneri: activation by virF and repression by H-NS. J Bacteriol 175:6142–6149PubMedGoogle Scholar
  44. 44.
    White-Ziegler CA, Davis TR (2009) Genome-wide identification of H-NS-controlled, temperature-regulated genes in Escherichia coli K-12. J Bacteriol 191:1106–1110PubMedCrossRefGoogle Scholar
  45. 45.
    Goransson M, Sonden B, Nilsson P, Dagberg B, Forsman K, Emanuelsson K, Uhlin BE (1990) Transcriptional silencing and thermoregulation of gene expression in Escherichia coli. Nature 344:682–685PubMedCrossRefGoogle Scholar
  46. 46.
    White-Ziegler CA, Angus Hill ML, Braaten BA, van der Woude MW, Low DA (1998) Thermoregulation of Escherichia coli pap transcription: H-NS is a temperature-dependent DNA methylation blocking factor. Mol Microbiol 28:1121–1137PubMedCrossRefGoogle Scholar
  47. 47.
    Duong N, Osborne S, Bustamante VH, Tomljenovic AM, Puente JL, Coombes BK (2007) Thermosensing coordinates a cis-regulatory module for transcriptional activation of the intracellular virulence system in Salmonella enterica serovar Typhimurium. J Biol Chem 282:34077–34084PubMedCrossRefGoogle Scholar
  48. 48.
    Mitobe J, Morita-Ishihara T, Ishihama A, Watanabe H (2008) Involvement of RNA-binding protein Hfq in the post-transcriptional regulation of invE gene expression in Shigella sonnei. J Biol Chem 283:5738–5747PubMedCrossRefGoogle Scholar
  49. 49.
    Storz G (1999) An RNA thermometer. Genes Dev 13:633–636PubMedCrossRefGoogle Scholar
  50. 50.
    Narberhaus F, Waldminghaus T, Chowdhury S (2006) RNA thermometers. FEMS Microbiol Rev 30:3–16PubMedCrossRefGoogle Scholar
  51. 51.
    Morita MT, Tanaka Y, Kodama TS, Kyogoku Y, Yanagi H, Yura T (1999) Translational induction of heat shock transcription factor σ32: evidence for a built-in RNA thermosensor. Genes Dev 13:655–665PubMedCrossRefGoogle Scholar
  52. 52.
    Narberhaus F, Käser R, Nocker A, Hennecke H (1998) A novel DNA element that controls bacterial heat shock gene expression. Mol Microbiol 28:315–323PubMedCrossRefGoogle Scholar
  53. 53.
    Nocker A, Krstulovic NP, Perret X, Narberhaus F (2001) ROSE elements occur in disparate rhizobia and are functionally interchangeable between species. Arch Microbiol 176:44–51PubMedCrossRefGoogle Scholar
  54. 54.
    Waldminghaus T, Fippinger A, Alfsmann J, Narberhaus F (2005) RNA thermometers are common in alpha- and gamma-proteobacteria. Biol Chem 386:1279–1286PubMedCrossRefGoogle Scholar
  55. 55.
    Nocker A, Hausherr T, Balsiger S, Krstulovic NP, Hennecke H, Narberhaus F (2001) A mRNA-based thermosensor controls expression of rhizobial heat shock genes. Nucleic Acids Res 29:4800–4807PubMedCrossRefGoogle Scholar
  56. 56.
    Chowdhury S, Ragaz C, Kreuger E, Narberhaus F (2003) Temperature-controlled structural alterations of an RNA thermometer. J Biol Chem 278:47915–47921PubMedCrossRefGoogle Scholar
  57. 57.
    Chowdhury S, Maris C, Allain FHT, Narberhaus F (2006) Molecular basis for temperature sensing by an RNA thermometer. EMBO J 25:2487–2497PubMedCrossRefGoogle Scholar
  58. 58.
    Waldminghaus T, Heidrich N, Brantl S, Narberhaus F (2007) FourU: a novel type of RNA thermometer in Salmonella. Mol Microbiol 65:413–424PubMedCrossRefGoogle Scholar
  59. 59.
    Hoe NP, Goguen JD (1993) Temperature sensing in Yersinia pestis: translation of the LcrF activator protein is thermally regulated. J Bacteriol 175:7901–7909PubMedGoogle Scholar
  60. 60.
    Johansson J, Mandin P, Renzoni A, Chiaruttini C, Springer M, Cossart P (2002) An RNA thermosensor controls expression of virulence genes in Listeria monocytogenes. Cell 110:551–561PubMedCrossRefGoogle Scholar
  61. 61.
    Waldminghaus T, Gaubig LC, Narberhaus F (2007) Genome-wide bioinformatic prediction and experimental evaluation of potential RNA thermometers. Mol Genet Genomics 278:555–564PubMedCrossRefGoogle Scholar
  62. 62.
    Waldminghaus T, Kortmann J, Gesing S, Narberhaus F (2008) Generation of synthetic RNA-based thermosensors. Biol Chem 389:1319–1326PubMedCrossRefGoogle Scholar
  63. 63.
    Wieland M, Hartig JS (2007) RNA quadruplex-based modulation of gene expression. Chem Biol 14:757–763PubMedCrossRefGoogle Scholar
  64. 64.
    Neupert J, Karcher D, Bock R (2008) Design of simple synthetic RNA thermometers for temperature-controlled gene expression in Escherichia coli. Nucleic Acids Res 36:e124PubMedCrossRefGoogle Scholar
  65. 65.
    Altuvia S, Kornitzer D, Teff D, Oppenheim AB (1989) Alternative mRNA structures of the cIII gene of bacteriophage lambda determine the rate of its translation initiation. J Mol Biol 210:265–280PubMedCrossRefGoogle Scholar
  66. 66.
    Yamanaka K, Mitta M, Inouye M (1999) Mutation analysis of the 5′ untranslated region of the cold shock cspA mRNA of Escherichia coli. J Bacteriol 181:6284–6291PubMedGoogle Scholar
  67. 67.
    Fang L, Jiang W, Bae W, Inouye M (1997) Promoter-independent cold-shock induction of cspA and its derepression at 37°C by mRNA stabilization. Mol Microbiol 23:355–364PubMedCrossRefGoogle Scholar
  68. 68.
    Uppal S, Akkipeddi VS, Jawali N (2008) Posttranscriptional regulation of cspE in Escherichia coli: involvement of the short 5′-untranslated region. FEMS Microbiol Lett 279:83–91PubMedCrossRefGoogle Scholar
  69. 69.
    Lybecker MC, Samuels DS (2007) Temperature-induced regulation of RpoS by a small RNA in Borrelia burgdorferi. Mol Microbiol 64:1075–1089PubMedCrossRefGoogle Scholar
  70. 70.
    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
  71. 71.
    Repoila F, Gottesman S (2003) Temperature sensing by the dsrA promoter. J Bacteriol 185:6609–6614PubMedCrossRefGoogle Scholar
  72. 72.
    Morimoto RI (1993) Cells in stress: transcriptional activation of heat shock genes. Science 259:1409–1410PubMedCrossRefGoogle Scholar
  73. 73.
    Servant P, Grandvalet C, Mazodier P (2000) The RheA repressor is the thermosensor of the HSP18 heat shock response in Streptomyces albus. Proc Natl Acad Sci USA 97:3538–3543PubMedCrossRefGoogle Scholar
  74. 74.
    Servant P, Mazodier P (2001) Negative regulation of the heat shock response in Streptomyces. Arch Microbiol 176:237–242PubMedCrossRefGoogle Scholar
  75. 75.
    Hurme R, Berndt KD, Normark SJ, Rhen M (1997) A proteinaceous gene regulatory thermometer in Salmonella. Cell 90:55–64PubMedCrossRefGoogle Scholar
  76. 76.
    Gal-Mor O, Valdez Y, Finlay BB (2006) The temperature-sensing protein TlpA is repressed by PhoP and dispensable for virulence of Salmonella enterica serovar Typhimurium in mice. Microbes Infect 8:2154–2162PubMedCrossRefGoogle Scholar
  77. 77.
    Naik RR, Kirkpatrick SM, Stone MO (2001) The thermostability of an alpha-helical coiled-coil protein and its potential use in sensor applications. Biosens Bioelectron 16:1051–1057PubMedCrossRefGoogle Scholar
  78. 78.
    Liu W, Vierke G, Wenke AK, Thomm M, Ladenstein R (2007) Crystal structure of the archaeal heat shock regulator from Pyrococcus furiosus: a molecular chimera representing eukaryal and bacterial features. J Mol Biol 369:474–488PubMedCrossRefGoogle Scholar
  79. 79.
    Maresca B, Kobayashi GS (1989) Dimorphism in Histoplasma capsulatum: a model for the study of cell differentiation in pathogenic fungi. Microbiol Rev 53:186–209PubMedGoogle Scholar
  80. 80.
    Nguyen VQ, Sil A (2008) Temperature-induced switch to the pathogenic yeast form of Histoplasma capsulatum requires Ryp1, a conserved transcriptional regulator. Proc Natl Acad Sci USA 105:4880–4885PubMedCrossRefGoogle Scholar
  81. 81.
    Nemecek JC, Wuthrich M, Klein BS (2006) Global control of dimorphism and virulence in fungi. Science 312:583–588PubMedCrossRefGoogle Scholar
  82. 82.
    Beier D, Gross R (2006) Regulation of bacterial virulence by two-component systems. Curr Opin Microbiol 9:143–152PubMedCrossRefGoogle Scholar
  83. 83.
    Calva E, Oropeza R (2006) Two-component signal transduction systems, environmental signals, and virulence. Microb Ecol 51:166–176PubMedCrossRefGoogle Scholar
  84. 84.
    Stock AM, Robinson VL, Goudreau PN (2000) Two-component signal transduction. Annu Rev Biochem 69:183–215PubMedCrossRefGoogle Scholar
  85. 85.
    Braun Y, Smirnova AV, Weingart H, Schenk A, Ullrich MS (2007) A temperature-sensing histidine kinase: function, genetics, and membrane topology. Methods Enzymol 423:222–249PubMedCrossRefGoogle Scholar
  86. 86.
    Hunger K, Beckering CL, Marahiel MA (2004) Genetic evidence for the temperature-sensing ability of the membrane domain of the Bacillus subtilis histidine kinase DesK. FEMS Microbiol Lett 230:41–46PubMedCrossRefGoogle Scholar
  87. 87.
    Suzuki I, Kanesaki Y, Mikami K, Kanehisa M, Murata N (2001) Cold-regulated genes under control of the cold sensor Hik33 in Synechocystis. Mol Microbiol 40:235–244PubMedCrossRefGoogle Scholar
  88. 88.
    Mikami K, Kanesaki Y, Suzuki I, Murata N (2002) The histidine kinase Hik33 perceives osmotic stress and cold stress in Synechocystis sp PCC 6803. Mol Microbiol 46:905–915PubMedCrossRefGoogle Scholar
  89. 89.
    Budde IP, Ullrich MS (2000) Interactions of Pseudomonas syringae pv. glycinea with host and nonhost plants in relation to temperature and phytotoxin synthesis. Mol Plant Microbe Interact 13:951–961PubMedCrossRefGoogle Scholar
  90. 90.
    Mittal S, Davis KR (1995) Role of the phytotoxin coronatine in the infection of Arabidopsis thaliana by Pseudomonas syringae pv. tomato. Mol Plant Microbe Interact 8:165–171PubMedGoogle Scholar
  91. 91.
    Ullrich M, Penaloza-Vazquez A, Bailey AM, Bender CL (1995) A modified two-component regulatory system is involved in temperature-dependent biosynthesis of the Pseudomonas syringae phytotoxin coronatine. J Bacteriol 177:6160–6169PubMedGoogle Scholar
  92. 92.
    Smirnova AV, Braun Y, Ullrich MS (2008) Site-directed mutagenesis of the temperature-sensing histidine protein kinase CorS from Pseudomonas syringae. FEMS Microbiol Lett 283:231–238PubMedCrossRefGoogle Scholar
  93. 93.
    Rangaswamy V, Bender CL (2000) Phosphorylation of CorS and CorR, regulatory proteins that modulate production of the phytotoxin coronatine in Pseudomonas syringae. FEMS Microbiol Lett 193:13–18PubMedCrossRefGoogle Scholar
  94. 94.
    Guschina IA, Harwood JL (2006) Mechanisms of temperature adaptation in poikilotherms. FEBS Lett 580:5477–5483PubMedCrossRefGoogle Scholar
  95. 95.
    Mansilla MC, Cybulski LE, Albanesi D, de Mendoza D (2004) Control of membrane lipid fluidity by molecular thermosensors. J Bacteriol 186:6681–6688PubMedCrossRefGoogle Scholar
  96. 96.
    Aguilar PS, Hernandez-Arriaga AM, Cybulski LE, Erazo AC, de Mendoza D (2001) Molecular basis of thermosensing: a two-component signal transduction thermometer in Bacillus subtilis. EMBO J 20:1681–1691PubMedCrossRefGoogle Scholar
  97. 97.
    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
  98. 98.
    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
  99. 99.
    Mansilla MC, de Mendoza D (2005) The Bacillus subtilis desaturase: a model to understand phospholipid modification and temperature sensing. Arch Microbiol 183:229–235PubMedCrossRefGoogle Scholar
  100. 100.
    Los DA, Murata N (1999) Responses to cold shock in cyanobacteria. J Mol Microbiol Biotechnol 1:221–230PubMedGoogle Scholar
  101. 101.
    Suzuki I, Los DA, Kanesaki Y, Mikami K, Murata N (2000) The pathway for perception and transduction of low-temperature signals in Synechocystis. EMBO J 19:1327–1334PubMedCrossRefGoogle Scholar
  102. 102.
    Kanesaki Y, Yamamoto H, Paithoonrangsarid K, Shoumskaya M, Suzuki I, Hayashi H, Murata N (2007) Histidine kinases play important roles in the perception and signal transduction of hydrogen peroxide in the cyanobacterium, Synechocystis sp. PCC 6803. Plant J 49:313–324PubMedCrossRefGoogle Scholar
  103. 103.
    Mikami K, Murata N (2003) Membrane fluidity and the perception of environmental signals in cyanobacteria and plants. Prog Lipid Res 42:527–543PubMedCrossRefGoogle Scholar
  104. 104.
    Horvath I, Glatz A, Varvasovszki V, Torok Z, Pali T, Balogh G, Kovacs E, Nadasdi L, Benko S, Joo F, Vigh L (1998) Membrane physical state controls the signaling mechanism of the heat shock response in Synechocystis PCC 6803: identification of hsp17 as a “fluidity gene”. Proc Natl Acad Sci USA 95:3513–3518PubMedCrossRefGoogle Scholar
  105. 105.
    Horvath I, Multhoff G, Sonnleitner A, Vigh L (2008) Membrane-associated stress proteins: more than simply chaperones. Biochim Biophys Acta 1778:1653–1664PubMedCrossRefGoogle Scholar
  106. 106.
    Tuominen I, Pollari M, Tyystjarvi E, Tyystjarvi T (2006) The SigB sigma factor mediates high-temperature responses in the cyanobacterium Synechocystis sp. PCC6803. FEBS Lett 580:319–323PubMedCrossRefGoogle Scholar
  107. 107.
    Nara T, Lee L, Imae Y (1991) Thermosensing ability of Trg and Tap chemoreceptors in Escherichia coli. J Bacteriol 173:1120–1124PubMedGoogle Scholar
  108. 108.
    Mizuno T, Imae Y (1984) Conditional inversion of the thermoresponse in Escherichia coli. J Bacteriol 159:360–367PubMedGoogle Scholar
  109. 109.
    Maeda K, Imae Y (1979) Thermosensory transduction in Escherichia coli: inhibition of the thermoresponse by L-serine. Proc Natl Acad Sci USA 76:91–95Google Scholar
  110. 110.
    Salman H, Libchaber A (2007) A concentration-dependent switch in the bacterial response to temperature. Nat Cell Biol 9:1098–1100PubMedCrossRefGoogle Scholar
  111. 111.
    Nishiyama S, Maruyama IN, Homma M, Kawagishi I (1999) Inversion of thermosensing property of the bacterial receptor Tar by mutations in the second transmembrane region. J Mol Biol 286:1275–1284PubMedCrossRefGoogle Scholar
  112. 112.
    Nishiyama SI, Umemura T, Nara T, Homma M, Kawagishi I (1999) Conversion of a bacterial warm sensor to a cold sensor by methylation of a single residue in the presence of an attractant. Mol Microbiol 32:357–365PubMedCrossRefGoogle Scholar
  113. 113.
    Nishiyama S, Nara T, Homma M, Imae Y, Kawagishi I (1997) Thermosensing properties of mutant aspartate chemoreceptors with methyl-accepting sites replaced singly or multiply by alanine. J Bacteriol 179:6573–6580PubMedGoogle Scholar
  114. 114.
    Fischetti VA, Jones KF, Hollingshead SK, Scott JR (1988) Structure, function, and genetics of streptococcal M protein. Rev Infect Dis 10(Suppl 2):S356–S359Google Scholar
  115. 115.
    Cedervall T, Johansson MU, Akerstrom B (1997) Coiled-coil structure of group A streptococcal M proteins. Different temperature stability of class A and C proteins by hydrophobic–nonhydrophobic amino acid substitutions at heptad positions a and d. Biochemistry 36:4987–4994PubMedCrossRefGoogle Scholar
  116. 116.
    Winter J, Jakob U (2004) Beyond transcription—new mechanisms for the regulation of molecular chaperones. Crit Rev Biochem Mol Biol 39:297–317PubMedCrossRefGoogle Scholar
  117. 117.
    McCarty JS, Walker GC (1991) DnaK as a thermometer: threonine-199 is site of autophosphorylation and is critical for ATPase activity. Proc Natl Acad Sci USA 88:9513–9517PubMedCrossRefGoogle Scholar
  118. 118.
    Grimshaw JP, Jelesarov I, Schönfeld HJ, Christen P (2001) Reversible thermal transition in GrpE, the nucleotide exchange factor of the DnaK heat-shock system. J Biol Chem 276:6098–6104PubMedCrossRefGoogle Scholar
  119. 119.
    Harrison C (2003) GrpE, a nucleotide exchange factor for DnaK. Cell Stress Chaperones 8:218–224PubMedCrossRefGoogle Scholar
  120. 120.
    Gelinas AD, Toth J, Bethoney KA, Langsetmo K, Stafford WF, Harrison CJ (2003) Thermodynamic linkage in the GrpE nucleotide exchange factor, a molecular thermosensor. Biochemistry 42:9050–9059PubMedCrossRefGoogle Scholar
  121. 121.
    Siegenthaler RK, Christen P (2006) Tuning of DnaK chaperone action by nonnative protein sensor DnaJ and thermosensor GrpE. J Biol Chem 281:34448–34456PubMedCrossRefGoogle Scholar
  122. 122.
    Groemping Y, Reinstein J (2001) Folding properties of the nucleotide exchange factor GrpE from Thermus thermophilus: GrpE is a thermosensor that mediates heat shock response. J Mol Biol 314:167–178PubMedCrossRefGoogle Scholar
  123. 123.
    Groemping Y, Klostermeier D, Herrmann C, Veit T, Seidel R, Reinstein J (2001) Regulation of ATPase and chaperone cycle of DnaK from Thermus thermophilus by the nucleotide exchange factor GrpE. J Mol Biol 305:1173–1183PubMedCrossRefGoogle Scholar
  124. 124.
    Schroda M, Vallon O, Whitelegge JP, Beck CF, Wollman FA (2001) The chloroplastic GrpE homolog of Chlamydomonas: two isoforms generated by differential splicing. Plant Cell 13:2823–2839PubMedCrossRefGoogle Scholar
  125. 125.
    Willmund F, Muhlhaus T, Wojciechowska M, Schroda M (2007) The NH2-terminal domain of the chloroplast GrpE homolog CGE1 is required for dimerization and cochaperone function in vivo. J Biol Chem 282:11317–11328Google Scholar
  126. 126.
    Narberhaus F (2002) Alpha-crystallin-type heat shock proteins: socializing minichaperones in the context of a multichaperone network. Microbiol Mol Biol Rev 66:64–93PubMedCrossRefGoogle Scholar
  127. 127.
    Haslbeck M, Franzmann T, Weinfurtner D, Buchner J (2005) Some like it hot: the structure and function of small heat-shock proteins. Nat Struct Mol Biol 12:842–846PubMedCrossRefGoogle Scholar
  128. 128.
    Franzmann TM, Menhorn P, Walter S, Buchner J (2008) Activation of the chaperone Hsp26 is controlled by the rearrangement of its thermosensor domain. Mol Cell 29:207–216PubMedCrossRefGoogle Scholar
  129. 129.
    Clausen T, Southan C, Ehrmann M (2002) The HtrA family of proteases: implications for protein composition and cell fate. Mol Cell 10:443–455PubMedCrossRefGoogle Scholar
  130. 130.
    Spiess C, Beil A, Ehrmann M (1999) A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell 97:339–347PubMedCrossRefGoogle Scholar
  131. 131.
    Krojer T, Garrido-Franco M, Huber R, Ehrmann M, Clausen T (2002) Crystal structure of DegP (HtrA) reveals a new protease-chaperone machine. Nature 416:455–459PubMedCrossRefGoogle Scholar
  132. 132.
    Krojer T, Sawa J, Schafer E, Saibil HR, Ehrmann M, Clausen T (2008) Structural basis for the regulated protease and chaperone function of DegP. Nature 453:885–890PubMedCrossRefGoogle Scholar
  133. 133.
    Kim DY, Kwon E, Shin YK, Kweon DH, Kim KK (2008) The mechanism of temperature-induced bacterial HtrA activation. J Mol Biol 377:410–420PubMedCrossRefGoogle Scholar
  134. 134.
    Kamath-Loeb AS, Gross CA (1991) Translational regulation of σ32 synthesis: requirement for an internal control element. J Bacteriol 173:3904–3906PubMedGoogle Scholar
  135. 135.
    Nagai H, Yuzawa H, Yura T (1991) Interplay of two cis-acting mRNA regions in translational control of σ32 synthesis during the heat shock response of Escherichia coli. Proc Natl Acad Sci USA 88:10515–10519PubMedCrossRefGoogle Scholar
  136. 136.
    Yuzawa H, Nagai H, Mori H, Yura T (1993) Heat induction of σ32 synthesis mediated by mRNA secondary structure: a primary step of the heat shock response in Escherichia coli. Nucleic Acids Res 21:5449–5455PubMedCrossRefGoogle Scholar
  137. 137.
    Balsiger S, Ragaz C, Baron C, Narberhaus F (2004) Replicon-specific regulation of small heat shock genes in Agrobacterium tumefaciens. J Bacteriol 186:6824–6829PubMedCrossRefGoogle Scholar
  138. 138.
    White-Ziegler CA, Um S, Perez NM, Berns AL, Malhowski AJ, Young S (2008) Low temperature (23°C) increases expression of biofilm-, cold-shock- and RpoS-dependent genes in Escherichia coli K-12. Microbiology 154:148–166PubMedCrossRefGoogle Scholar
  139. 139.
    Moll I, Afonyushkin T, Vytvytska O, Kaberdin VR, Bläsi U (2003) Coincident Hfq binding and RNase E cleavage sites on mRNA and small regulatory RNAs. RNA 9:1308–1314PubMedCrossRefGoogle Scholar

Copyright information

© Birkhäuser Verlag, Basel/Switzerland 2009

Authors and Affiliations

  1. 1.Lehrstuhl für Biologie der MikroorganismenRuhr-Universität BochumBochumGermany

Personalised recommendations