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The heat shock stimulon of Bacillus subtilis

Wolfgang Schumann

Institute of Genetics, University of Bayreuth, D-95440 Bayreuth Germany

ABSTRACT

The heat shock response is characterized by the transiently increased expression of a set of genes called heat shock genes. In Escherichia coli, the best studied eubacterial species, one major heat shock regulon with some 31 genes and two minor regulons are induced after heat stress; all three regulons are under the control of alternate sigma factors. In Bacillus subtilis, too, three classes of heat shock genes have been discovered, but two classes are most probably under negative control by two different repressors. Class I genes which form the CIRCE regulon are transcribed from s^A-dependent promoters and are characterized by a 9-bp inverted repeat called CIRCE element which is located between their transcriptional and translational start points and is recognized by the repressor protein HrcA. The CIRCE element is highly conserved among eubacteria. The majority of the heat-inducible genes belongs to class II, and they are under the control of the alternative factor s^B, whose activity is controlled by an anti-sigma factor. Class III genes encode predominantly ATP-dependent proteases or their regulatory ATPase subunits. They are transcribed from either one or two s^A-like promoters or from one s^A- and one s^B-dependent promoter. For two members of class III, it could be shown that they are under negative control of a repressor. Whereas class I heat shock genes are induced only by heat or puromycin, those of class II and class III recognize additional stress factors such as ethanol, salt, or oxygen limitation for induction. All heat shock genes of B. subtilis form one large heat shock stimulon. It remains to be clarified whether the three classes are interconnected.

Keywords: heat shock stimulon; Bacillus subtilis.

REFERENCES

Babst, M., Hennecke, H. and Fischer, H.-M. (1996). Two different mechanisms are involved in the heat-shock regulation of chaperonin gene expression in Bradyrhizobium japonicum. Mol. Microbiol. 19: 827-840.

Benson, A.K. and Haldenwang, W.G. (1992). Characterization of a regulatory network that controls s^B expression in Bacillus subtilis. J. Bacteriol. 174: 749-757.

Benson, A.K. and Haldenwang, W.G. (1993). Bacillus subtilis s^B is regulated by a binding protein (RsbW) that blocks its association with core RNA polymerase. Proc. Natl. Acad. Sci. USA 90: 2330-2334.

Bourgaize, D.B., Phillips, T.A., VanBogelen, R.A., Jones, P.G., Neidhardt, F.C. and Fournier, M.J. (1990). Loss of 4.5S RNA induces the heat shock response and lambda prophage in Escherichia coli. J. Bacteriol. 172: 1151-1154.

Boylan, S.A., Rutherford, A., Thomas, S.M. and Price, C.W. (1992). Activation of Bacillus subtilis transcription factor s^B by a regulatory pathway responsive to stationary-phase signals. J. Bacteriol. 174: 3695-3706.

Brissette, J.L., Weiner, L., Ripmaster, T.L. and Model, P. (1991). Characterization and sequence of the Escherichia coli stress-induced psp operon. J. Mol. Biol. 220: 35-48.

Bukau, B. (1993). Regulation of the heat-shock response. Mol. Microbiol. 9: 671-680.

Chang, B.-Y., Chen, K.-Y., Wen, Y.-D. and Liao, C.-T. (1994). The response of a Bacillus subtilis temperature-sensitive sigA mutant to heat stress. J. Bacteriol. 176: 3102-3110.

Craig, E.A. and Gross, C.A. (1991). Is hsp70 the cellular thermometer? Trends Biochem. Sci. 16: 135-140.

Deuerling, E., Paeslack, B. and Schumann, W. (1995). The ftsH gene of Bacillus subtilis is transiently induced after osmotic and temperature upshock. J. Bacteriol. 177: 4105-4112.

Dufour, A. and Haldenwang, W.G. (1994). Interactions between a Bacillus subtilis anti-s factor (RsbW) and its antagonist (RsbV). J. Bacteriol. 176: 1813-1820.

Eaton, T., Shearman, C. and Gasson, M. (1993). Cloning and sequence analysis of the dnaK gene region of Lactococcus lactis subsp. lactis. J. Gen. Microbiol. 139: 3253-3264.

Erickson, J.W. and Gross, C. (1989). Identification of the s^B subunit of Escherichia coli RNA polymerase: A second alternate a factor involved in high-temperature gene expression. Genes Dev. 3: 1462-1471.

Fernandez, R.C. and Weiss, A.A. (1995). Cloning and sequencing of the Bordetella pertusis cpn10/cpn60 (groESL) homolog. Gene 158: 151-152.

Fraser, C.M., Gocayne, J.D., White, O., Adams, M.D., Clayton, R.A., Fleischmann, R.D., Bult, C.J., Kerlavage, A.R., Sutton, G., Kelley, J.M., Fritchman, J.L., Weidman, J.F., Small, K.V., Sandusky, M., Fuhrmann, J., Nguyen, D., Utterback, T.R., Saudek, D.M., Phillips, C.A., Merrick, J.M., Tomb, J.F., Dougherty, B.A., Bott, K.F. and Hu, P.C. (1995). The minimal gene complement of Mycoplasma genitalium. Science 270: 397-403.

Gage, D.J. and Neidhardt, F.C. (1993). Modulation of the heat shock response by one-carbon metabolism in Escherichia coli. J. Bacteriol. 175: 1961-1970.

Gamer, J., Bujard, H. and Bukau, B. (1992). Physical interaction between heat shock proteins DnaK, DnaJ, and GrpE and the bacterial heat shock transcription factor s³². Cell 69: 833-842.

Gamer, J., Multhaup, G., Tomoyasu, T., McCarty, J.S., Rüdiger, S., Schönfeld, H.J., Schirra, C., Bujard, H. and Bukau, B. (1996). A cycle of binding and release of the DnaK, DnaJ and GrpE chaperones regulates activity of the Escherichia coli heat shock transcription factor 632. EMBO J. 15: 607-617.

Gatenby, A.A. and Ellis, R.J. (1990). Chaperone function: The assembly of ribulose bisphosphate carboxylaseoxygenase. Annu. Rev. Cell Biol. 6: 125-149. Georgopoulos, C. and Welch, W.J. (1993). Role of the major heat shock proteins as molecular chaperones. Annu. Rev. Cell Biol. 9: 601-634.

Haldenwang, W.G. (1995). The sigma factors of Bacillus subtilis. Microbiol. Rev. 59: 1-30.

Haldenwang, W.G. and Losick, R. (1979). A modified RNA polymerase transcribes a cloned gene under sporulation control in Bacillus subtilis. Nature 282: 256-260.

Hecker, M. and Völker, U. (1990). General stress proteins in Bacillus subtilis. FEMS Microbiol. Ecol. 74: 197-214.

Hecker, M., Schumann, W. and Völker, U. (1996). Heat-shock and general stress response in Bacillus subtilis. Mol. Microbiol. 19: 417-428.

Hendrick, J.P. and Hartl, F.U. (1995). The role of molecular chaperones in protein folding. FASEB j. 9: 1559-1569.

Herman, C., Ogura, T., Tomoyasu, T., Hiraga, S., Akiyama, Y., Ito, K., Thomas, R., D'Ari, R. and Bouloc, P. (1993). Cell growth and lambda phage development controlled by the same essential Escherichia coli gene ftsH/hflB. Proc. Natl. Acad. Sci. USA 90: 10861-10865.

Herman, C., Thévenet, D., D'Ari, R. and Bouloc, P. (1995). Degradation of s³², the heat shock regulator in Escherichia coli, is governed by HflB. Proc. Natl. Acad. Sci. USA 92: 3516-3520.

Jovanovic, G., Weiner, L. and Model, P. (1996). Identification, nucleotide sequence, and characterization of PspF, the transcriptional activator of the Escherichia coli stress-induced psp operon. j. Bacteriol. 178: 1936-1945.

Kanemori, M., Mori, H. and Yura, T. (1994). Induction of heat shock proteins by abnormal proteins results from stabilization and not increased synthesis of s³² in Escherichia coli. j. Bacteriol. 176: 5648-5653.

Krüger, E., Völker, U. and Hecker, M. (1994). Stress induction of clpC in Bacillus subtilis and its involvement in stress tolerance. j. Bacteriol. 176: 3360-3367.

Krüger, E., Msadek, T. and Hecker, M. (1996). Alternate promoters direct stress-induced transcription of the Bacillus subtilis clpC operon. Mol. Microbiol. 20: 713-723.

Li, M. and Wong, S.-L. (1992). Cloning and characterization of the groESL operon from Bacillus subtilis. j. Bacteriol. 174: 3981-3992.

Liberek, K. and Georgopoulos, C. (1993). Autoregulation of the Escherichia coli heat shock response by the DnaK and DnaJ heat shock proteins. Proc. Natl. Acad. Sci. USA 90: 11019-11023.

Lipinska, B., Sharma, S. and Georgopoulos, C. (1988). Sequence analysis and regulation of the htrA gene of Escherichia coli: a s³²-independent mechanism of heat-inducible transcription. Nucleic Acids Res. 16: 10053-10067.

Matin, A., Auger, E.A., Blum, P.H. and Schulz, J.E. (1989). Genetic basis of starvation survival in nondifferentiating bacteria. Annu. Rev. Microbiol. 43: 293-316.

Maul, B., Völker, U., Riethdorf, S., Engelmann, S. and Hecker, M. (1995). s^B-dependent regulation of gsiB in response to multiple stimuli in Bacillus subtilis. Mol. Gen. Genet. 248: 114-120.

Mecsas, J., Rouviere, P.E., Erickson, J.W., Donohue, T.J. and Gross, C.A. (1993). The activity of s^E, an Escherichia coli heat-inducible s-factor, is modulated by expression of outer membrane proteins. Genes Dev. 7: 2618-2628.

Morimoto, R.I., Tissières, A. and Georgopoulos, C. (1990). Stress Proteins in Biology and Medicine. Cold Spring Harbor Laboratory Press, Cold Spring Harbor.

Msadek, T., Kunst, F. and Rapoport, G. (1994). MecB of Bacillus subtilis, a member of the C1pC ATPase family, is a pleiotropic regulator controlling competence gene expression and growth at high temperature. Proc. Natl. Acad. Sci. USA 91: 5788-5792.

Nagai, H., Yuzawa, H. and Yura, T. (1991). Interplay of two cis-acting mRNA regions in translational control of s³² synthesis during the heat shock response of Escherichia coli. Proc. Natl. Acad. Sci. USA 88: 10515-10519.

Narberhaus, F., Giebeler, K. and Bahl, H. (1992). Molecular characterization of the dnaK gene region of Clostridium acetobutylicum, includinggrpE, dnaj, and a new heat shock gene. j. Bacteriol. 174: 3290-3299.

Ohta, T., Saito, K., Kuroda, M., Honda, K., Hirata, H. and Hayashi, H. (1994). Molecular cloning of two new heat shock genes related to the hsp70 genes in Staphylococcus aureus. j. Bacteriol. 176: 4779-4783.

Parsell, D.A. and Sauer, R.T. (1989). Induction of a heat shock-like response by unfolded protein in Escherichia coli: dependence on protein level not protein

degradation. Genes Dev. 3: 1226-1232.

Riethdorf, S., Völker, U., Gerth, U., Winkler, A., Engelmann, S. and Hecker, M. (1994). Cloning, nucleotide sequence, and expression of the Bacillus subtilis lon gene. j. Bacteriol. 176: 6518-6527.

Rinke de Wit, T.F., Bekelie, S., Osland, A., Miko, T.L., Hermans, P.W.M., van Soolingen, D., Drijfhout, J., Schöningh, R., Janson, A.A. M. and Thole, J.E.R. (1992). Mycobacteria contain two groEL genes: the second Mycobacterium lepraegroEL gene is arranged in an operon with groES. Mol. Microbiol. 6: 1995-2007.

Roberts, R.C., Toochinda, C., Avedissian, M., Baldini, R.L., Gomes, S.L. and Shapiro, L. (1996). Identification of a Caulobacter crescentus operon encoding hrcA, involved in negatively regulating heat-inducible transcription, and the chaperone gene grpE. J. Bacteriol. 178: 1829-1841.

Schmidt, A., Schiesswohl, M., Völker, U., Hecker, M. and Schumann, W. (1992). Cloning, sequencing, mapping, and transcriptional analysis of the groESL operon from Bacillus subtilis. j. Bacteriol. 174: 3993-3999.

Schmidt, R., Decatur, A.L., Rather, P.N., Moran Jr., C.P. and Losick, R. (1994). Bacillus subtilis ion protease prevents inappropriate transcription of genes under the control of the sporulation transcription factor s^G. j. Bacteriol. 176: 6528-6537.

Schmiel, D.H. and Wyrick, P.B. (1994). Another putative heat-shock gene and aminoacyl-tRNA synthetase gene are located upstream from the grpE-like and dnaK-like genes in Chlamydia trachomatis. Gene 145: 57-63.

Schulz, A. and Schumann, W. (1996). hrcA, the first gene of the Bacillus subtilis dnaK operon encode a negative regulator of class I heat-shock genes. j. Bacteriol. 178: 1088-1093.

Schulz, A., Tzschaschel, B. and Schumann, W. (1995). Isolation and analysis of mutants of the dnaK operon of Bacillus subtilis. Mol. Microbiol. 15: 421-429.

Schumann, W. and Zuber, U. (1992). Regulation of the heat shock response in prokaryotes. Ciênc. Cult. 44: 287-291.

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.

Straus, D.B., Walter, W.A. and Gross, C.A. (1989). The activity of s³² is reduced under conditions of excess heat shock protein production in Escherichia coli. Genes Dev. 3: 2003-2010.

Tomoyasu, T., Yamanaka, K., Murata, K., Suzaki, T., Bouloc, P., Kato, A., Niki, H., Hiraga, S. and Ogura, T. (1993). Topology and subcellular localization of FtsH protein in Escherichia coli. j. Bacteriol. 175: 1352-1357.

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 s³². EMBO j. 14: 2551-2560.

Tozawa, Y., Yoshikawa, H., Kawamura, F., Itaya, M. and Takahashi, H. (1992). Isolation and characterization of the groES and groEL gene of Bacillus subtilis Marburg. Biosci. Biotech. Biochem. 56: 1995-2002.

Van Asseldonk, M., Simons, A., Visser, H., De Vos, W.M. and Simons, G. (1993). Cloning, nucleotide sequence, and regulatory analysis of the Lactococcus lactis dnaj gene. j. Bacteriol. 175: 1637-1644.

VanBogelen, R.A. and Neidhardt, F.C. (1990). Ribosomes as sensors of heat and cold shock in Escherichia coli. Proc. Natl. Acad. Sci. USA 87: 5589-5593.

Vanet, A., Plumbridge, J.A., Guérin, M. and Alix, J. (1994). Ribosomal protein methylation in Escherichia coli: the gene prmA, encoding the ribosomal protein L11 methyltransferase, is dispensable. Mol. Microbiol. 14: 947-958.

Völker, U., Mach, H., Schmid, R. and Hecker, M. (1992). Stress proteins and cross-protection by heat shock and salt stress in Bacillus subtilis. j. Gen. Microbiol. 138: 21252135.

Völker, U., Engelmann, S., Maul, B., Riethdorf, S., Völker, A., Schmid, R., Mach, H. and Hecker, M. (1994). Analysis of the induction of general stress proteins of Bacillus subtilis. Microbiol. 140: 741-752.

Voelker, U., Dufour, A. and Haldenwang, W.G. (1995a). The Bacillus subtilis rsbU gene product is necessary for RsbX-dependent regulation of s^B. j. Bacteriol. 177: 114-122.

Voelker, U., Voelker, A., Maul, B., Hecker, M., Dufour, A. and Haldenwang, W.G. (1995b). Separate mechanisms activate s^B of Bacillus subtilis in response to environmental and metabolic stresses. j. Bacteriol. 177: 3771-3780.

Wetzstein, M. and Schumann, W. (1990). Promoters of major Escherichia coli heat shock genes seem non-functional in Bacillus subtilis. FEMS Microbiol. Lett. 72: 55-58.

Wetzstein, M., Völker, U., Dedio, J., Löbau, S., Zuber, U., Schiesswohl, M., Herget, C., Hecker, M. and Schumann, W. (1992). Cloning, sequencing, and molecular analysis of the dnaK locus from Bacillus subtilis. j. Bacteriol. 174: 3300-3310.

Wise, A.A. and Price, C.W. (1995). Four additional genes in the sigB operon of Bacillus subtilis that control activity of the general stress factor c in response to environmental signals. j. Bacteriol. 177: 123-133.

Yuan, G. and Wong, S.L. (1995a). Isolation and characterization of Bacillus subtilis regulatory mutants: evidence for orf39 in the dnaK operon as a repressor gene in regulating the expression of both groE and dnaK. j. Bacteriol. 177: 6462-6468.

Yuan, G. and Wong, S.L. (1995b). Regulation of groE expression in Bacillus subtilis: the involvement of the <font face="Symbol">s</font>^A-like promoter and the roles of the inverted repeat sequence (CIRCE). j. Bacteriol. 177: 5427-5433.

Yura, T., Nagai, H. and Mori, H. (1993). Regulation of the heat-shock response in bacteria. Annu. Rev. Microbiol. 47: 321-350.

Yuzawa, H., Nagai, H., Mori, H. and Yura, T. (1993). Heat induction of <font face="Symbol">s</font>³² synthesis mediated by mRNA secondary structure: A primary step of the heat shock response in Escherichia coli. Nucleic Acids Res. 21: 5449-5455.

Zuber, U. and Schumann, W. (1994). CIRCE, a novel heat shock element involved in regulation of heat shock operon dnaK of Bacillus subtilis . j. Bacteriol. 176: 1359-1363.