The Oenococcus oeni clpX homologue is a heat shock gene preferentially expressed in exponential growth phase

Journal of Bacteriology

Volumn 181, Issue 21, 1999, Pages 6634-6641

  Jobin, Michel Philippe ^a   Garmyn, Dominique ^a   Diviès, Charles ^a   Guzzo, Jean ^a  

^a CEMAGREF   (France)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN;

ARTICLE; BACTERIAL GROWTH; NONHUMAN; OENOCOCCUS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS;

OENOCOCCUS OENI;

EID: 0032729809     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.181.21.6634-6641.1999     Document Type: Article

References (60)

1. Antelmann, H., S. Engelmann, R. Schmid, and M. Hecker. 1996. General and oxidative stress responses in Bacillus subtilis: cloning, expression, and mutation of the alky1 hydroperoxide reductase operon. J. Bacteriol. 178: 6571-6578.
2. Boutibonnes, P. 1996. Les protéines de choc thermique chez Lactococcus lactis: synthèse et régulation; thermotolérance. Lait 76:111-128.
3. Cavin, J.-F., H. Prevost, J. Lin, P. Schmitt, and C. Diviès. 1989. Medium for screening Leuconostoc oenos strains defective in malolactic fermentation. Appl. Environ. Microbiol. 55:751-753.
4. Chen, J. D., and D. A. Morrisson. 1988. Construction and properties of a new insertion vector, pJDC9, that is protected by transcriptional terminators and useful for cloning of DNA from Streptococcus pneumonia. Gene 64:155-164.
5. Chen, L.-H., S. A. Emory, A. L. Bricker, P. Bouvet, and J. G. Belasco. 1991. Structure and function of a bacterial mRNA stabilizer: analysis of the 5′ untranslated region of ompA mRNA. J. Bacteriol. 173:4578-4586.
6. Derré, I., G. Rapoport, and T. Msadek. 1999. CtsR, a novel regulator of stress and heat shock response, controls clp and molecular chaperone gene expression in Gram-positive bacteria. Mol. Microbiol. 31:117-131.
7. Deuerling, E., A. Mogk, C. Richter, M. Purucker, and W. Schumann. 1997. The ftsH gene of Bacillus subtilis is involved in major cellular processes such as sporulation, stress adaptation and secretion. Mol. Microbiol. 23:921-933.
8. Dufour, S. A., A. Amory, and A. Goffeau. 1998. Plasma membrane ATPase from the yeast Schizosaccharomyces pombe. Methods Enzymol. 157:513-528.
9. Emory, S. A., and J. G. Belasco. 1990. The ompA 5′ untranslated RNA segment functions in Escherichia coli as a growth-rate-regulated mRNA stabilizer whose activity is unrelated to translational efficiency. J. Bacteriol. 172:4472-4481.
10. Fleischmann, R. D., M. D. Adams, O. White, R. A. Clayton, E. F. Kirkness, A. R. Kerlavage, C. J. Bult, J.-F. Tomb, B. A. Dougherty, J. M. Merrick, K. McKenney, G. Sutton, W. Fitzugh, C. A. Field, J. D. Gocayne, J. D. Scott, R. Shirley, L.-I. Liu, A. Glodek, J. M. Kelley, J. F. Weidman, C. A. Phillips, T. Spriggs, E. Hedblom, M. D. Cotton, T. R. Utterback, M. C. Hanna, D. T. Nguyen, D. M. Saudek, R. Brandon, L. D. Fine, J. L. Fritchman, J. L. Fuhrmann, N. S. N. Geoghagen, C. L. Gnehm, L. A. McDonald, K. V. Small, C. M. Fraser, H. O. Smith, and J. C. Venter. 1995. Whole-genome random sequencing and assembly of Haemophilus influenzae. Science 269:496-512.
11. Frees, D., and H. Ingmer. 1999. ClpP participates in the degradation of misfolded protein in Lactococcus lactis. Mol. Microbiol. 31:79-87.
12. Gerth, U., E. Krüger, I. Derré, T. Msadek, and M. Hecker. 1998. Stress induction of the Bacillus subtilis clpP gene encoding a homologue of the proteolytic component of the Clp protease and the involvement of CIpP and ClpX in stress tolerance. Mol. Microbiol. 28:787-802.
13. Gerth, U., A. Wipat, C. R. Harwood, N. Carter, P. T. Emmerson, and M. Hecker. 1996. Sequence and transcriptional analysis of clpX, a class-III heat-shock gene of Bacillus subtilis. Gene 181:77-83.
14. Gibson, T. J. 1984. Studies on the Epstein-Barr virus genome. Ph.D. thesis. Cambridge University, Cambridge, England.
15. Gottesman, S., W. P. Clark, V. de Crecy-Lagard, and M. Maurizi. 1993. ClpX, an alternative subunit for the ATP-dependent Clp protease of Escherichia coli. J. Biol. Chem. 268:22618-22626.
16. Gottesman, S., C. Squires, E. Pichersky, M. Carrington, M. Hobbs, J. S. Mattick, B. Dalrymple, H. Kuramitsu, T. Shiroza, T. Foster, W. P. Clark, B. Ross, C. L. Squires, and M. R. Maurizi. 1990. Conservation of the regulatory subunit for the ATP-dependent protease in prokaryotes and eukaryotes. Proc. Natl. Acad. Sci. USA 87:3513-3517.
17. Griffiths, P., R. Park, and I. Connerton. 1995. The gene for Campylobacter trigger factor: evidence for multiple transcription start sites and protein products. Microbiology 141:1359-1367.
18. Grimaud, R., M. Kessel, F. Beuron, A. C. Steven, and M. R. Maurizi. 1998. Enzymatic and structural similarities between the Escherichia coli ATP-dependent proteases, ClpXP and ClpAP. J. Biol. Chem. 273:12476-12481.
19. Guthrie, B., and W. Wickner. 1990. Trigger factor depletion or overproduction causes defective cell division but does not block protein export. J. Bacteriol. 172:5555-5562.
20. Guzzo, J., J.-F. Cavin, and C. Diviès. 1994. Induction of stress proteins in Leuconostoc oenos to perform direct inoculation of wine. Biotechnol. Lett. 16:1189-1194.
21. Guzzo, J., F. Delmas, F. Pierre, M.-P. Jobin, B. Samyn, J. Van Beeumen, J.-F. Cavin, and C. Diviès. 1997. A small heat shock protein from Leuconostoc oenos induced by multiple stresses and during stationary growth phase. Lett. Appl. Microbiol. 24:393-396.
22. Guzzo, J., M.-P. Jobin, and C. Diviès. 1998. Increase of sulfite tolerance in Oenococcus oeni by means of acidic adaptation. FEMS Microbiol. Lett. 160:43-47.
23. Hecker, M., W. Schumann, and U. Völker. 1996. Heat-shock and general stress response in Bacillus subtilis. Mol. Microbiol. 19:417-428.
24. Henkin, T. M. 1996. Control of transcription termination in prokaryotes. Annu. Rev. Genet. 30:35-57.
25. Hesterkamp, T., and B. Bukau. 1996. The Escherichia coli trigger factor. FEBS Lett. 389:32-34.
26. Jacobson, M. R., K. E. Brigle, L. T. Bennett, R. A. Setterquist, M. S. Wilson, V. L. Cash, J. Beynon, W. E. Newton, and D. R. Dean. 1989. Physical and genetic map of the major nif gene cluster from Azotobacter vinelandii. J. Bacteriol. 171:1017-1027.
27. Jobin, M.-P., F. Delmas, D. Garmyn, C. Diviès, and J. Guzzo. 1997. Molecular characterization of the gene encoding an 18-kilodalton small heat shock protein associated with the membrane of Leuconostoc oenos. Appl. Environ. Microbiol. 63:609-614.
28. Jobin, M.-P., D. Garmyn, C. Diviès, and J. Guzzo. 1999. Expression of the Oenococcus oeni trxA gene is induced by hydrogen peroxide and heat shock. Microbiology 145:1245-1251.
29. Kaneko, T., S. Sato, H. Kotani, A. Tanaka, E. Asamizu, Y. Nakamura, N. Miyajima, M. Hirosawa, M. Sugiura, S. Sasamoto, T. Kimura, T. Hosouchi, A. Matsuno, A. Muraki, N. Nakazaki, K. Naruo, S. Okumura, S. Shimpo, C. Takeuchi, T. Wada, A. Watanabe, M. Yamada, M. Yasuda, and S. Tabata. 1996. Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions (supplement). DNA Res. 3:185-209.
30. Krüger, E., and M. Hecker. 1998. The first gene of the Bacillus subtilis clpC operon, ctsR, encodes a negative regulator of its own operon and other class III heat shock genes. J. Bacteriol. 180:6681-6688.
31. Kunkee, R. E. 1991. Some roles of malic acid in the malolactic fermentation in wine making. FEMS Microbiol. Rev. 88:55-72.
32. Labarre, C., C. Diviès, and J. Guzzo. 1996. Genetic organization of the mle locus and identification of a mleR-like gene from Leuconostoc oenos. Appl. Environ. Microbiol. 62:4493-4498.
33. Labarre, C., J. Guzzo, J.-F. Cavin, and C. Diviès. 1996. Cloning and characterization of the genes encoding the malolactic enzyme and the malate permease of Leuconostoc oenos. Appl. Environ. Microbiol. 62:1274-1282.
34. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
35. Lundberg, U., A. von Gabain, and Ö. Melefors. 1990. Cleavages in the 5′ region of the ompA and bla mRNA control stability: studies with an E. coli mutant altering mRNA stability and a novel endoribonuclease. EMBO J. 9:2731-2741.
36. Matin, A. 1991. The molecular basis of a carbon-starvation-induced general resistance in Escherichia coli. Mol. Microbiol. 5:3-10.
37. Maurizi, M. R. 1993. ATP-dependent proteases, p. 65-71. In J. S. Bond and A. J. Barrett (ed.), Proteolysis and protein turnover. Portland Press Proceedings Series, vol. 6. California/Princeton Fulfillment Services, Ewing, N.J.
38. Maurizi, M. R., W. P. Clark, Y. Katayama, Z. S. Rudikoff, J. Pumphrey, B. Bowers, and S. Gottesman. 1990. Sequence and structure of ClpP, the proteolytic component of the ATP-dependent Clp protease of Escherichia coli. J. Biol. Chem. 265:12536-12545.
39. Msadek, T., V. Dartois, F. Kunst, M. L. Herbaud, F. Denizot, and G. Rapoport. 1998. ClpP of Bacillus subtilis is required for competence development, motility, degradative enzyme synthesis, growth at high temperature and sporulation. Mol. Microbiol. 27:899-914.
40. Riethdorf, S., U. Völker, U. Gerth, A. Winkler, S. Engelman, and M. Hecker. 1994. Cloning, nucleotide sequence, and expression of the Bacillus subtilis lon gene. J. Bacteriol. 176:6518-6527.
41. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
42. Sanger, F., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74:5463-5467.
43. Scharf, C., S. Riethdorf, H. Ernst, S. Engelmann, U. Völker, and M. Hecker. 1998. Thioredoxin is an essential protein induced by multiple stresses in Bacillus subtilis. J. Bacteriol. 180:1869-1877.
44. Schearman, C. A., K. L. Jury, and M. J. Gasson. 1994. Controlled expression and structural organization of a Lactococcus lactis bacteriophage lysin encoded by two overlapping genes. Appl. Environ. Microbiol. 60:3063-3073.
45. Schneider, T. D., G. D. Stormo, and L. Gold. 1986. Information content of binding sites on nucleotide sequences. J. Mol. Biol. 188:415-431.
46. Schulz, A., and W. Schumann. 1996. hrcA, the first gene of the Bacillus subtilis dnaK operon encodes a negative regulator of class I heat shock genes. J. Bacteriol. 178:1088-1093.
47. Schulz, A., S. Schwab, G. Homuth, S. Versteeg, and W. Schumann. 1997. The htpG gene of Bacillus subtilis belongs to class III heat shock genes and is under negative control. J. Bacteriol. 179:3103-3109.
48. Schweder, T., K.-H. Lee, O. Lomovskaya, and A. Matin. 1996. Regulation of Escherichia coli starvation sigma factor (σS) by ClpXP protease. J. Bacteriol. 178:470-476.
49. Sussman, J. K., E. L. Simons, and R. W. Simons. 1996. Escherichia coli translation initiation factor 3 discriminates the initiation codon in vivo. Mol. Microbiol. 21:347-360.
50. Szabo, A., R. Korszum, F. U. Hartl, and J. Flanagan. 1996. A zinc finger-like domain of the molecular chaperone DnaJ is involved in binding to denatured protein substrates. EMBO J. 15:408-417.
51. Tatsuta, T., T. Tomoyasu, B. Bukau, M. Kitagawa, H. Mori, K. Karata, and T. Ogura. 1998. Heat shock regulation in the ftsH null mutant of Escherichia coli: dissection of stability and activity control mechanisms of sigma32 in vivo. Mol. Microbiol. 30:583-593.
52. Thompson, M. W., and M. R. Maurizi. 1994. Activity and specificity of Escherichia coli ClpAP protease in cleaving model peptide substrates. J. Biol. Chem. 269:18201-18208.
53. Tinoco, I., Jr., P. N. Borer, B. Dengler, M. D. Levine, O. C. Uhlenbeck, D. M. Crothers, and J. Gralla. 1973. Improved estimation of secondary structure in ribonucleic acids. Nat. New Biol. 246:40-41.
54. Wawrzynow, A., B. Banecki, and M. Zylicz. 1996. The Clp ATPases define a novel class of molecular chaperones. Mol. Microbiol. 21:895-899.
55. Wawrzynow, A., D. Wojtkowiak, J. Marszalek, B. Banecki, M. Jonsen, B. Graves, C. Georgopoulous, and M. Zylicz. 1995. The ClpX heat-shock protein of Escherichia coli, the ATP-dependent substrate specificity component of the ClpP-ClpX protease, is a novel molecular chaperone. EMBO J. 14: 1867-1877.
56. Wojtkowiak, D., C. Georgopoulos, and M. Zylicz. 1993. Isolation and characterization of ClpX, a new ATP-dependent specificity component of the CIp protease of Escherichia coli. J. Biol. Chem. 268:22609-22617.
57. Woo, K. M., W. J. Chung, D. B. Ha, A. L. Goldberg, and C. H. Chung. 1989. Protease Ti from Escherichia coli requires ATP hydrolysis for protein breakdown but not for hydrolysis of small peptides. J. Biol. Chem. 264:2088-2091.
58. Yang, D., and C. R. Woese. 1989. Phylogenetic structure of the Leuconostoc: an interesting case of a rapidly evolving organism. Syst. Appl. Microbiol. 12:145-149.
59. Yuan, G., and S. L. Wong. 1995. Regulation of groE expression in Bacillus subtilis: the involvement of the sigma A-like promoter and the roles of the inverted repeat sequence (CIRCE). J. Bacteriol. 177:5427-5433.
60. Zuber, U., and W. Schumann. 1994. CIRCE, a novel heat shock element involved in regulation of heat shock operon dnaK of Bacillus subtilis. J. Bacteriol. 176:1359-1363.