Abstract
Temperature is an important physical stress factor sensed by bacteria and used to regulate gene expression. Three different macromolecules have been identified being able to sense temperature: DNA, mRNA and proteins. Depending on the induction mechanism, two different pathways have to be distinguished, namely the heat shock response and the high temperature response. While the heat shock response is induced by temperature increments and is transient, the high temperature response needs a specific temperature to become induced and proceeds as long as cells are exposed to that temperature. The heat shock response is induced by denatured proteins and aimed to prevent formation of protein aggregates by refolding or degradation, and the high temperature response is mainly used by pathogenic bacteria to detect entry into a mammalian host followed by induction of their virulence genes. All known high temperature sensors are present in two alternative conformations depending on the temperature. Heat shock sensors are either molecular chaperones or proteases which keep either a positive transcriptional regulator inactive or a negative regulator active or do not attack the regulator, respectively, under physiological conditions. Denatured proteins either titrate the molecular chaperones or activate the protease. The evolution of the different temperature sensors is discussed.
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References
Ades S E 2004 Control of the alternative sigma factor σE in Escherichia coli; Curr. Opin. Microbiol. 7 157–162
Alba B M and Gross C A 2004 Regulation of the Escherichia coli σE-dependent envelope stress response; Mol. Microbiol. 52 613–619
Alba B M, Leeds J A, Onufryk C, Lu C Z and Gross C A 2002 DegS and YaeL participate sequentially in the cleavage of RseA to activate the σE-dependent extracytoplasmic stress response; Genes Dev. 16 2156–2168
Alba B M, Zhong H J, Pelayo J C, and Gross C A 2001 degS (hhoB) is an essential Escherichia coli gene whose indispensable function is to provide σE activity; Mol. Microbiol. 40 1323–1333
Altuvia S, Kornitzer D, Teff D, and Oppenheim A B 1989 Alternative mRNA structures of the cIII gene of bacteriophage λ determine the rate of its translation initiation; J. Mol. Biol. 210 265–280
Atlung T and Ingmer H 1997 H-NS: a modulator of environmentally regulated gene expression; Mol. Microbiol. 24 7–17
Bucca G, Brassington A M E, Schönfeld H-J and Smith C P 2000 The HspR regulon of Streptomyces coelicolor: a role for the DnaK chaperone as a transcriptional co-repressor; Mol. Microbiol. 38 1093–1103
Bucca G, Hindle Z and Smith C P 1997 Regulation of the dnaK operon of Streptomyces coelicolor A3(2) is governed by HspR, an autoregulatory repressor protein; J. Bacteriol. 179 5999–6004
Clausen T, Southan C and Ehrmann M 2004 The HtrA family of proteases: implications for protein composition and cell fate; Mol. Cell 10 443–455
Colonna B, Casalino M, Fradiani P A, Zagaglia C, Naitza S, Leoni L, Prosseda G, Coppo A, Ghelardini P and 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 4703–4712
Cornelis G R and Wolf-Watz H 1997 The Yersinia Yop virulon: a bacterial system for subverting eukaryotic cells; Mol. Microbiol. 23 861–867
Dame R T, Wyman C, Wurm R, Wagner R and Goosen N 2002 Structural basis for H-NS mediated trapping of RNA polymerase in the open initiation complex at the rrnB P1; J. Biol. Chem. 277 2146–2150
Grossman A D, Erickson J W and Gross C A 1984 The htpR gene product of E. coli is a sigma factor for heat-shock promoters; Cell 38 383–389
Herman C, Thévenet D, D’Ari R and Bouloc P 1997 The HflB protease of Escherichia coli degrades its inhibitor lambda cIII; J. Bacteriol. 179 358–363
Herman C, Thévenet D, D’Ari R and Bouloc P 1995 Degradation of σ32, the heat shock regulator in Escherichia coli, is governed by HflB; Proc. Natl. Acad. Sci. USA 92 3516–3520
Hurme R, Berndt K D, Namok E and Rhen M 1996 DNA binding exerted by a bacterial gene regulator with an extensive coiled-coil domain; J. Biol. Chem. 271 12626–12631
Hurme R, Berndt K D, Normark S J and Rhen M 1997 A proteinaceous gene regulatory thermometer in Salmonella; Cell 90 55–64
Johansson J, Mandin P, Renzoni A, Chiaruttini C, Springer M and Cossart P 2002 An RNA thermosensor controls expression of virulence genes in Listeria monocytogenes; Cell 110 551–561
Kaempfer R 2003 RNA sensors: novel regulators of gene expression; EMBO Rep. 4 1043–1047
Kanehara K, Ito K and Akiyama Y 2002 YaeL (EcfE) activates the σE pathway of stress response through a site-2 cleavage of anti-σE, RseA; Genes Dev. 16 2147–2155
Krojer T, Garrido-Franco M, Huber R, Ehrmann M and Clausen T 2002 Crystal structure of DegP (HtrA) reveals a new protease-chaperone machine; Nature (London) 416 455–459
Lambert de R C, Sluiters C, and Cornelis G R 1992 Role of the transcriptional activator, VirF, and temperature in the expression of the pYV plasmid genes of Yersinia enterocolitica; Mol. Microbiol. 6 395–409
Landick R, Vaughn V, Lau E T, VanBogelen R A, Erickson J W and Neidhardt F C 1984 Nucleotide sequence of the heat shock regulatory gene of E. coli suggests its protein product my be a transcription factor; Cell 38 175–182
Lemaux P G, Herendeen S L, Bloch P and Neidhardt F C 1978 Transient rates of synthesis of individual polypeptides in E. coli following temperature shifts; Cell 13 427–434
Mandal M and Breaker R R 2004 Gene regulation by riboswitches; Nat. Rev. Mol. Cell Biol. 5 451–463
Maurelli A T 1989 Temperature regulation of virulence genes in pathogenic bacteria: a general strategy for human pathogens?; Microb. Pathog. 7 1–10
Michiels T, Vanooteghem J C, Lambert de R C, China B, Gustin A, Boudry P, and Cornelis G R 1991 Analysis of virC, an operon involved in the secretion of Yop proteins by Yersinia enterocolitica; J. Bacteriol. 173 4994–5009
Mizuno T 1987 Random cloning of bent DNA segments from Escherichia coli chromosome and primary characterization of their structures; Nucleic Acids Res. 15 6827–6841
Mogk A, Homuth G, Scholz C, Kim L, Schmid F X, and Schumann W 1997 The GroE chaperonin machine is a major modulator of the CIRCE heat shock regulon of Bacillus subtilis; EMBO J. 16 4579–4590
Morimoto R I, Tissières A and Georgopoulos C 1990 Stress proteins in biology and medicine (New york; Cold Spring Harbor Laboratory Press)
Morita M, Kanemori M, Yanagi H and Yura T 1999a Heat-induced synthesis of σ32 in Escherichia coli: Structural and functional dissection of rpoH mRNA secondary structure; J. Bacteriol. 181 401–410
Morita M T, Tanaka Y, Kodama T S, Kyogoku Y, Yanagi H and Yura T 1999b Translational induction of heat shock transcription factor σ32: evidence for a built-in RNA thermosensor; Genes Dev. 13 655–665
Narberhaus F, Käser R, Nocker A and Hennecke H 1998 A novel DNA element that controls bacterial heat shock gene expression; Mol. Microbiol. 28 315–323
Narberhaus F, Waldminghaus T and Chowdhury S 2006 RNA thermometers; FEMS Microbiol. Rev. 30 3–16
Narberhaus F, Weiglhofer W, Fischer H M and Hennecke H 1996 The Bradyrhizobium japonicum rpoH1 gene encoding a σ32-like protein is part of a unique heat shock gene cluster together with groESL1 and three small heat shock genes; J. Bacteriol. 178 5337–5346
Nickerson C A and Achberger E C 1995 Role of curved DNA in binding of Escherichia coli RNA polymerase to promoters; J. Bacteriol. 177 5756–5761
Nocker A, Hausherr T, Balsiger S, Krstulovic N P, Hennecke H and Narberhaus F 2001 A mRNA-based thermosensor controls expression of rhizobial heat shock genes; Nucleic Acids Res. 29 4800–4807
Ohyama T 2001 Intrinsic DNA bends: an organizer of local chromatin structure for transcription; BioEssays 23 708–715
Prosseda G, Falconi M, Giangrossi M, Gualerzi C O, Micheli G and Colonna B 2004 The virF promoter in Shigella: more than just a curved DNA stretch; Mol. Microbiol. 51 523–537
Prosseda G, Falconi M, Nicoletti M, Casalino M, Micheli G and Colonna B 2002 Histone-like proteins and the Shigella invasivity regulon; Res. Microbiol. 153 461–468
Prosseda G, Fradiani PA, Di L M, Falconi M, Micheli G, Casalino M Nicoletti M, and Colonna B 1998 A role for H-NS in the regulation of the virF gene of Shigella and enteroinvasive Escherichia coli; Res. Microbiol. 149 15–25
Renzoni A, Klarsfeld A, Dramsi S and Cossart P 1997 Evidence that PrfA, the pleiotropic activator of virulence genes in Listeria monocytogenes, can be present but inactive; Infect. Immun. 65 1515–1518
Ritossa F 1962 A new puffing pattern induced by temperature shock and DNP in Drosophila; Experientia 18 571–573
Rohde J R, Luan X S, Rohde H, Fox J M and Minnich S A 1999 The Yersinia enterocolitica pYV virulence plasmid contains multiple intrinsic DNA bends which melt at 37°C; J. Bacteriol. 181 4198–4204
Saras J and Heldin C H 1996 PDZ domains bind carboxy-terminal sequences of target proteins; Trends Biochem. Sci. 21 455–458
Schröder O and Wagner R 2002 The bacterial regulatory protein H-NS—a versatile modulator of nucleic acid structures; Biol. Chem. 383 945–960
Schumann W 2003 The Bacillus subtilis heat shock stimulon; Cell Stress Chaperones 8 207–217
Servant P, Grandvalet C and Mazodier P 2000 The RheA repressor is the thermosensor of the HSP18 heat shock response in Streptomyces albus; Proc. Natl. Acad. Sci. USA 97 3538–3543
Servant P and Mazodier P 1995 Characterization of Streptomyces albus 18-kilodalton heat shock-responsive protein; J. Bacteriol. 177 2998–3003
Shotland Y, Koby S, Teff D, Mansur N, Oren D A, Tatematsu K, Tomoyasu T, Kessel M, Bukau B, Ogura T and Oppenheim A B 1997 Proteolysis of the phage lambda CII regulatory protein by FtsH (HflB) of Escherichia coli; Mol. Microbiol. 24 1303–1310
Spiess C, Beil A and Ehrmann M 1999 A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein; Cell 97 339–347
Storz G, Opdyke J A and Zhang A 2004 Controlling mRNA stability and translation with small, noncoding RNAs; Curr. Opin. Microbiol. 7 140–144
Strauch, K. L. and Beckwith J 1988 An Escherichia coli mutation preventing degradation of abnormal periplasmic proteins; Proc. Natl. Acad. Sci. USA 85 1576–1580
Sussman, R and Jacob F 1962 Sur un système de répression thermosensible chez le bactériophage d’Escherichia coli; C. R. Hebd. Seances Acad. Sci. 254 1517–1519
Tanaka K, Muramatsu S, Yamada H and Mizuno T 1991 Systematic characterization of curved DNA segments randomly cloned from Escherichia coli and their functional significance; Mol. Gen. Genet. 226 367–376
Tilly K, Spence J, and Georgopoulos C 1989 Modulation of stability of the Escherichia coli heat shock regulatory factor σ32; J. Bacteriol. 171 1585–1589
Tissières A, Mitchell H K, and Tracy V M 1974 Protein synthesis in salivary glands of Drosophila melanogaster: Relation to chromosome puffs; J. Mol. Biol. 84 389–398
Tomoyasu T, Gamer J, Bukau B, Kanemori M, Mori H, Rutman A J, Oppenheim A B, Yura T, Yamanaka K, Niki H, Hiraga S and Ogura T 1995 Escherichia coli FtsH is a membrane-bound, ATP-dependent protease which degrades the heat-shock transcription factor σ32; EMBO J. 14 2551–2560
Walsh N P, Alba B M, Bose B, Gross C A, and Sauer R T 2003 OMP peptide signals initiate the envelope-stress response by activating DegS protease via relief of inhibition mediated by its PDZ domain; Cell 113 61–71
Winkler W C and Breaker R R 2005 Regulation of bacterial gene expression by riboswitches; Annu. Rev. Microbiol. 59 487–517
Yamamori T and Yura T 1982 Genetic control of heat-shock protein synthesis and its bearing on growth and thermal regulation in Escherichia coli K12; Proc. Natl. Acad. Sci. USA 79 860–864
Yamanaka K 1999 Cold shock response in Escherichia coli; J. Mol. Microbiol. Biotechnol. 1 193–202
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Schumann, W. Thermosensors in eubacteria: role and evolution. J Biosci 32, 549–557 (2007). https://doi.org/10.1007/s12038-007-0054-8
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DOI: https://doi.org/10.1007/s12038-007-0054-8