Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1996 Dec;178(24):7031–7036. doi: 10.1128/jb.178.24.7031-7036.1996

Heat induction of hsp18 gene expression in Streptomyces albus G: transcriptional and posttranscriptional regulation.

P Servant 1, P Mazodier 1
PMCID: PMC178612  PMID: 8955381

Abstract

In Streptomyces albus G, HSP18, a protein belonging to the small heat shock protein family, could be detected only at high temperature. The nucleotide sequence of the DNA region upstream from hsp18 contains an open reading frame (orfY) which is in the opposite orientation and 150 bp upstream. This open reading frame encodes a basic protein of 225 amino acids showing no significant similarity to any proteins found in data banks. Disruption of this gene in the S. albus chromosome generated mutants that synthesized hsp18 RNA at 30 degrees C, suggesting that orfY plays either a direct or indirect role in the transcriptional regulation of the hsp18 gene. In addition, thermally induced expression of the hsp18 gene is subject to posttranscriptional regulation. In the orfY mutant, although hsp18 RNA was synthesized at a high level at 30 degrees C, the HSP18 protein could not be detected except after heat shock. Synthesis of the HSP18 protein in the orfY mutant was also heat inducible when transcription was inhibited by rifampin. Furthermore, when wild-type cultures of S. albus were shifted from high temperature to 30 degrees C, synthesis of the gene product could no longer be detected, even though large amounts of hsp18 RNA were present.

Full Text

The Full Text of this article is available as a PDF (3.1 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Booth R. J., Williams D. L., Moudgil K. D., Noonan L. C., Grandison P. M., McKee J. J., Prestidge R. L., Watson J. D. Homologs of Mycobacterium leprae 18-kilodalton and Mycobacterium tuberculosis 19-kilodalton antigens in other mycobacteria. Infect Immun. 1993 Apr;61(4):1509–1515. doi: 10.1128/iai.61.4.1509-1515.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Brandi A., Pietroni P., Gualerzi C. O., Pon C. L. Post-transcriptional regulation of CspA expression in Escherichia coli. Mol Microbiol. 1996 Jan;19(2):231–240. doi: 10.1046/j.1365-2958.1996.362897.x. [DOI] [PubMed] [Google Scholar]
  3. Bucca G., Ferina G., Puglia A. M., Smith C. P. The dnaK operon of Streptomyces coelicolor encodes a novel heat-shock protein which binds to the promoter region of the operon. Mol Microbiol. 1995 Aug;17(4):663–674. doi: 10.1111/j.1365-2958.1995.mmi_17040663.x. [DOI] [PubMed] [Google Scholar]
  4. Bukau B. Regulation of the Escherichia coli heat-shock response. Mol Microbiol. 1993 Aug;9(4):671–680. doi: 10.1111/j.1365-2958.1993.tb01727.x. [DOI] [PubMed] [Google Scholar]
  5. Chang Z., Primm T. P., Jakana J., Lee I. H., Serysheva I., Chiu W., Gilbert H. F., Quiocho F. A. Mycobacterium tuberculosis 16-kDa antigen (Hsp16.3) functions as an oligomeric structure in vitro to suppress thermal aggregation. J Biol Chem. 1996 Mar 22;271(12):7218–7223. [PubMed] [Google Scholar]
  6. Chater K. F., Wilde L. C. Streptomyces albus G mutants defective in the SalGI restriction-modification system. J Gen Microbiol. 1980 Feb;116(2):323–334. doi: 10.1099/00221287-116-2-323. [DOI] [PubMed] [Google Scholar]
  7. Duchêne A. M., Thompson C. J., Mazodier P. Transcriptional analysis of groEL genes in Streptomyces coelicolor A3(2). Mol Gen Genet. 1994 Oct 17;245(1):61–68. doi: 10.1007/BF00279751. [DOI] [PubMed] [Google Scholar]
  8. Fellay R., Frey J., Krisch H. Interposon mutagenesis of soil and water bacteria: a family of DNA fragments designed for in vitro insertional mutagenesis of gram-negative bacteria. Gene. 1987;52(2-3):147–154. doi: 10.1016/0378-1119(87)90041-2. [DOI] [PubMed] [Google Scholar]
  9. Fernández-Moreno M. A., Caballero J. L., Hopwood D. A., Malpartida F. The act cluster contains regulatory and antibiotic export genes, direct targets for translational control by the bldA tRNA gene of Streptomyces. Cell. 1991 Aug 23;66(4):769–780. doi: 10.1016/0092-8674(91)90120-n. [DOI] [PubMed] [Google Scholar]
  10. Gething M. J., Sambrook J. Protein folding in the cell. Nature. 1992 Jan 2;355(6355):33–45. doi: 10.1038/355033a0. [DOI] [PubMed] [Google Scholar]
  11. Gralla J. D. Transcriptional control--lessons from an E. coli promoter data base. Cell. 1991 Aug 9;66(3):415–418. doi: 10.1016/0092-8674(81)90001-5. [DOI] [PubMed] [Google Scholar]
  12. Hartl F. U., Hlodan R., Langer T. Molecular chaperones in protein folding: the art of avoiding sticky situations. Trends Biochem Sci. 1994 Jan;19(1):20–25. doi: 10.1016/0968-0004(94)90169-4. [DOI] [PubMed] [Google Scholar]
  13. Hecker M., Schumann W., Völker U. Heat-shock and general stress response in Bacillus subtilis. Mol Microbiol. 1996 Feb;19(3):417–428. doi: 10.1046/j.1365-2958.1996.396932.x. [DOI] [PubMed] [Google Scholar]
  14. Heidelbach M., Skladny H., Schairer H. U. Heat shock and development induce synthesis of a low-molecular-weight stress-responsive protein in the myxobacterium Stigmatella aurantiaca. J Bacteriol. 1993 Nov;175(22):7479–7482. doi: 10.1128/jb.175.22.7479-7482.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Horwitz J. Alpha-crystallin can function as a molecular chaperone. Proc Natl Acad Sci U S A. 1992 Nov 1;89(21):10449–10453. doi: 10.1073/pnas.89.21.10449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jakob U., Gaestel M., Engel K., Buchner J. Small heat shock proteins are molecular chaperones. J Biol Chem. 1993 Jan 25;268(3):1517–1520. [PubMed] [Google Scholar]
  17. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  18. Lavoie J. N., Gingras-Breton G., Tanguay R. M., Landry J. Induction of Chinese hamster HSP27 gene expression in mouse cells confers resistance to heat shock. HSP27 stabilization of the microfilament organization. J Biol Chem. 1993 Feb 15;268(5):3420–3429. [PubMed] [Google Scholar]
  19. Motamedi H., Shafiee A., Cai S. J. Integrative vectors for heterologous gene expression in Streptomyces spp. Gene. 1995 Jul 4;160(1):25–31. doi: 10.1016/0378-1119(95)00191-8. [DOI] [PubMed] [Google Scholar]
  20. Nagai H., Yuzawa H., Yura T. Interplay of two cis-acting mRNA regions in translational control of sigma 32 synthesis during the heat shock response of Escherichia coli. Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10515–10519. doi: 10.1073/pnas.88.23.10515. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Parsell D. A., Lindquist S. The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet. 1993;27:437–496. doi: 10.1146/annurev.ge.27.120193.002253. [DOI] [PubMed] [Google Scholar]
  22. Petko L., Lindquist S. Hsp26 is not required for growth at high temperatures, nor for thermotolerance, spore development, or germination. Cell. 1986 Jun 20;45(6):885–894. doi: 10.1016/0092-8674(86)90563-5. [DOI] [PubMed] [Google Scholar]
  23. Puglia A. M., Vohradsky J., Thompson C. J. Developmental control of the heat-shock stress regulon in Streptomyces coelicolor. Mol Microbiol. 1995 Aug;17(4):737–746. doi: 10.1111/j.1365-2958.1995.mmi_17040737.x. [DOI] [PubMed] [Google Scholar]
  24. Sauer U., Dürre P. Sequence and molecular characterization of a DNA region encoding a small heat shock protein of Clostridium acetobutylicum. J Bacteriol. 1993 Jun;175(11):3394–3400. doi: 10.1128/jb.175.11.3394-3400.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Schulz A., Schumann W. hrcA, the first gene of the Bacillus subtilis dnaK operon encodes a negative regulator of class I heat shock genes. J Bacteriol. 1996 Feb;178(4):1088–1093. doi: 10.1128/jb.178.4.1088-1093.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Servant P., Mazodier P. Characterization of Streptomyces albus 18-kilodalton heat shock-responsive protein. J Bacteriol. 1995 Jun;177(11):2998–3003. doi: 10.1128/jb.177.11.2998-3003.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Servant P., Thompson C. J., Mazodier P. Post-transcriptional regulation of the groEL1 gene of Streptomyces albus. Mol Microbiol. 1994 May;12(3):423–432. doi: 10.1111/j.1365-2958.1994.tb01031.x. [DOI] [PubMed] [Google Scholar]
  28. Servant P., Thompson C., Mazodier P. Use of new Escherichia coli/Streptomyces conjugative vectors to probe the functions of the two groEL-like genes of Streptomyces albus G by gene disruption. Gene. 1993 Nov 30;134(1):25–32. doi: 10.1016/0378-1119(93)90170-8. [DOI] [PubMed] [Google Scholar]
  29. Thompson C. J., Ward J. M., Hopwood D. A. DNA cloning in Streptomyces: resistance genes from antibiotic-producing species. Nature. 1980 Jul 31;286(5772):525–527. doi: 10.1038/286525a0. [DOI] [PubMed] [Google Scholar]
  30. VanBogelen R. A., Neidhardt F. C. Ribosomes as sensors of heat and cold shock in Escherichia coli. Proc Natl Acad Sci U S A. 1990 Aug;87(15):5589–5593. doi: 10.1073/pnas.87.15.5589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Verbon A., Hartskeerl R. A., Schuitema A., Kolk A. H., Young D. B., Lathigra R. The 14,000-molecular-weight antigen of Mycobacterium tuberculosis is related to the alpha-crystallin family of low-molecular-weight heat shock proteins. J Bacteriol. 1992 Feb;174(4):1352–1359. doi: 10.1128/jb.174.4.1352-1359.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Wright F., Bibb M. J. Codon usage in the G+C-rich Streptomyces genome. Gene. 1992 Apr 1;113(1):55–65. doi: 10.1016/0378-1119(92)90669-g. [DOI] [PubMed] [Google Scholar]
  33. Yanisch-Perron C., Vieira J., Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. doi: 10.1016/0378-1119(85)90120-9. [DOI] [PubMed] [Google Scholar]
  34. Yarchuk O., Jacques N., Guillerez J., Dreyfus M. Interdependence of translation, transcription and mRNA degradation in the lacZ gene. J Mol Biol. 1992 Aug 5;226(3):581–596. doi: 10.1016/0022-2836(92)90617-s. [DOI] [PubMed] [Google Scholar]
  35. Yuan G., Wong S. L. Isolation and characterization of Bacillus subtilis groE regulatory mutants: evidence for orf39 in the dnaK operon as a repressor gene in regulating the expression of both groE and dnaK. J Bacteriol. 1995 Nov;177(22):6462–6468. doi: 10.1128/jb.177.22.6462-6468.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Yura T., Nagai H., Mori H. Regulation of the heat-shock response in bacteria. Annu Rev Microbiol. 1993;47:321–350. doi: 10.1146/annurev.mi.47.100193.001541. [DOI] [PubMed] [Google Scholar]
  37. Yuzawa H., Nagai H., Mori H., Yura T. Heat induction of sigma 32 synthesis mediated by mRNA secondary structure: a primary step of the heat shock response in Escherichia coli. Nucleic Acids Res. 1993 Nov 25;21(23):5449–5455. doi: 10.1093/nar/21.23.5449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. de Jong W. W., Leunissen J. A., Voorter C. E. Evolution of the alpha-crystallin/small heat-shock protein family. Mol Biol Evol. 1993 Jan;10(1):103–126. doi: 10.1093/oxfordjournals.molbev.a039992. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES