Mutations conferring amino acid residue substitutions in the carboxy-terminal domain of RNA polymerase α can suppress clpX and clpP with respect to developmentally regulated transcription in Bacillus subtilis

Molecular Microbiology

Volumn 37, Issue 4, 2000, Pages 869-884

  Nakano, Michiko M ^a   Zhu, Yi ^a   Liu, Jiajian ^a,b   Reyes, Dindo Y ^c   Yoshikawa, Hirofumi ^c   Zuber, Peter ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b LOUISIANA STATE UNIV MEDICAL CENTER   (United States)

^c TOKYO UNIVERSITY OF AGRICULTURE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; PHEROMONE; RNA POLYMERASE;

AMINO ACID SUBSTITUTION; ARTICLE; BACILLUS SUBTILIS; BACTERIAL GROWTH; GENE MUTATION; OPERON; PHENOTYPE; PRIORITY JOURNAL; SPOROGENESIS; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

ADENOSINE TRIPHOSPHATASES; ALLELES; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BACILLUS SUBTILIS; BACTERIAL PROTEINS; BASE SEQUENCE; DNA PRIMERS; DNA-DIRECTED RNA POLYMERASES; ENDOPEPTIDASE CLP; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; MUTATION; OPERON; SEQUENCE HOMOLOGY, AMINO ACID; SERINE ENDOPEPTIDASES; TRANSCRIPTION, GENETIC;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); PROKARYOTA;

EID: 0033865389     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2000.02052.x     Document Type: Article

References (88)

1. Aiyar, S.E., Gourse, R.L., and Ross, W. (1998) Upstream A-tracts increase bacterial promoter activity through interactions with the RNA polymerase alpha subunit. Proc Natl Acad Sci USA 95: 14652-14657.
2. Becker, G., Klauck, E., and Hengge-Aronis, R. (1999) Regulation of RpoS proteolysis in Escherichia coli: the response regulator RssB is a recognition factor that interacts with the turnover element in RpoS. Proc Natl Acad Sci USA 96: 6439-6444.
3. Cosmina, P., Rodriguez, F., de Ferra, F., Grandi, G., Perego, M., Venema, G., et al. (1993) Sequence and analysis of the genetic locus responsible for surfactin synthesis in Bacillus subtilis. Mol Microbiol 8: 821 -831.
4. D'Souza, C., Nakano, M.M., and Zuber, P. (1994) Identification of comS, a gene of the srfA operon that regulates the establishment of genetic competence in Bacillus subtilis. Proc Natl Acad Sci USA 91: 9397-9401.
5. Dubnau, D., and Davidoff-Abelson, R. (1971) Fate of transforming DNA following uptake by competent Bacillus subtilis. I. formation and properties of the donor-recipient complex. J Mol Biol 56: 209-221.
6. Dubnau, D., and Roggianni, M. (1990) Growth medium-independent genetic competence mutants of Bacillus subtilis. J Bacteriol 172: 4048-4055.
7. Dubnau, D., Hahn, J., Roggiani, M., Piazza, R., and Weinrauch, Y. (1994) Two-component regulators and genetic competence in Bacillus subtilis. Res Microbiol 145: 403-411.
8. H). J Bacteriol 170: 1054-1062.
9. van Dyck, L., Dembowski, M., Neupert, W., and Langer, T. (1998) Mcx1p, a ClpX homologue in mitochondria of Saccharomyces cerevisiae. FEBS Lett 438: 250-254.
10. Estrem, S.T., Ross, W., Gaal, T., Chen, Z.W., Niu, W., Ebright, R.H., et al. (1999) Bacterial promoter architecture: subsite structure of UP elements and interactions with the carboxy-terminal domain of the RNA polymerase alpha subunit. Genes Dev 13: 2134-21347.
11. Fouet, A., and Sonenshein, A.L. (1990) A target for carbon source-dependent negative regulation of the citB promoter of Bacillus subtilis. J Bacteriol 172: 835-844.
12. Fuma, S., Fujishima, Y., Corbell, N., D'Souza, C., Nakano, M.M., Zuber, P., et al. (1993) Nucleotide sequence of 5′ portion of srfA that contains the region required for competence establishment in Bacillus subtilis. Nucleic Acids Res 21: 93-97.
13. Gaal, T., Ross, W., Blatter, E.E., Tang, H., Jia, X., Krishnan, V.V., et al. (1996) DNA-binding determinants of the alpha subunit of RNA polymerase: novel DNA-binding domain architecture. Genes Dev 10: 16-26.
14. Gerth, U., Wipat, A., Harwood, C.R., Carter, N., Emmerson, P.T., and Hecker, M. (1996) Sequence and transcriptional analysis of clpX, a class-III heat-shock gene of Bacillus subtilis. Gene181: 77-83.
15. Gerth, U., Kruger, E., Derre, I., Msadek, T., and Hecker, M. (1998) Stress induction of the Bacillus subtilis clpP gene encoding a homologue of the proteolytic component of the Clp protease and the involvement of ClpP and ClpX in stress tolerance. Mol Microbiol; 28: 787-802.
16. Gottesman, S. (1999) Regulation by proteolysis: developmental switches. Curr Opin Microbiol 2: 142-147.
17. Gottesman, S., and Maurizi, M.R. (1992) Regulation by proteolysis: energy-dependent proteases and their targets. Microbiol Rev 56: 592-621.
18. Guerout-Fleury, A.M., Shazand, K., Frandsen, N., and Stragier, P. (1995) Antibiotic-resistance cassettes for Bacillus subtilis. Gene 167: 335-336.
19. Haldenwang, W.G. (1995) The sigma factors of Bacillus subtilis. Microbiol Rev 59: 1-30.
20. Hamoen, L.W., Eshuis, H., Jongbloed, J., Venema, G., and van Sinderen, D. (1995) A small gene, designated comS, located within the coding region of the fourth amino acid-activating domain of srfA, is required for competence development in Bacillus subtilis. Mol Microbiol 15: 55-63.
21. Hoch, J.A. (1993) spo0 genes, the phosphorelay, and the initiation of sporulation. In Bacillus subtilis and Other Gram-Positive Bacteria: Biochemistry, Physiology, and Molecular Genetics. Sonenshein, A.L., Hoch, J.A., and Losick, R. (eds). Washington DC: American Society for Microbiology Press, pp. 747-755.
22. Hoch,J.A. (1995) Control of cellular development in sporulating bacteria by the phosphorelay two-component signal transduction system. In Two-Component Signal Transduction. Hoch, J.A., and Silhavy, T.J. (eds). Washington, DC: American Society for Microbiology Press, pp. 129-144.
23. Jenal,U., and Fuchs, T. (1998) An essential protease involved in bacterial cell-cycle control. EMBO J 17: 5658-5669.
24. Jeon, Y.H., Negishi, T., Shirakawa, M., Yamazaki, T., Fujita, N., Ishihama, A., et al. (1995) Solution structure of the activator contact domain of the RNA polymerase alpha subunit. Science 270: 1495-1497.
25. Jones, J.M., Welty, D.J., and Nakai, H. (1998) Versatile action of Escherichia coli ClpXP as protease or molecular chaperone for bacteriophage Mu transposition. J Biol Chem273: 459-465.
26. Kong, L., and Dubnau, D. (1994) Regulation of competence-specific gene expression by Mec-mediated protein-protein interaction in Bacillus subtilis. Proc Natl Acad Sci USA 91: 5793-5797.
27. Kong, L., Siranosian, K.J., Grossman, A.D., and Dubnau, D. (1993) Sequence and properties of mecA: a negative regulator of genetic competence in Bacillus subtilis. Mol Microbiol 9: 365-373.
28. Konieczny, I., and Helinski, D.R. (1997) The replication initiation protein of the broad-host-range plasmid RK2 is activated by the ClpX chaperone. Proc Natl Acad Sci USA 94: 14378-14382.
29. Kruklitis, R., Welty, D.J., and Nakai, H. (1996) ClpX protein of Escherichia coli activates bacteriophage Mu transposase in the strand transfer complex for initiation of Mu DNA synthesis. EMBO J 15: 935-944.
30. Kunst, F., Ogasawara, N., Moszer, I., Albertini, A.M., Alloni, G., Azevedo, V., et al. (1997) The complete genome sequence of the Gram-positive bacterium Bacillus subtilis. Nature 390: 249-256.
31. Lazazzera, B.A., and Grossman, A.D. (1998) The ins and outs of peptide signaling. Trends Microbiol 6: 288-294.
32. Lazazzera, B.A., Solomon, J.M., and Grossman, A.D. (1997) An exported peptide functions intracellularly to contribute to cell density signaling in B. subtilis. Cell 89: 917-925.
33. Levchenko, I., Luo, L., and Baker, T.A. (1995) Disassembly of the Mu transposase tetramer by the ClpX chaperone. Genes Dev 9: 2399-2408.
34. Li, X., Lindahl, L., Sha, Y., and Zengel, J.M. (1997) Analysis of the Bacillus subtilis S10 ribosomal protein gene cluster identifies two promoters that may be responsible for transcription of the entire 15-kilobase S10-spc-α. J Bacteriol 179: 7046-7054.
35. D-dependent gene expression in Bacillus subtilis. J Bacteriol 180: 4243-4251.
36. H-dependent transcription. Mol Microbiol 37: 885-897.
37. Liu, J., Cosby, W.M., and Zuber, P. (1999) Role of Lon and ClpX in the post-translational regulation of a sigma subunit of RNA polymerase required for cellular differentiation of Bacillus subtilis. Mol Microbiol 33: 415-428.
38. Liu, L., Nakano, M.M., Lee, O.H., and Zuber, P. (1996) Plasmid-amplified comS enhances genetic competence and suppresses sinR in Bacillus subtilis. J Bacteriol 178: 5144-5152.
39. Magnuson, R., Solomon, J., and Grossman, A.D. (1994) Biochemical and genetic characterization of a competence pheromone from Bacillus subtilis. Cell 77: 207-216.
40. Mhammedi-Alaoui, A., Pato, M., Gama, M.J., and Toussaint, A. (1994) A new component of bacteriophage Mu replicative transposition machinery: the Escherichia coli ClpX protein. Mol Microbiol 11: 1109-1116.
41. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
42. Moran, C.P., Jr (1993) RNA polymerase and transcription factors. In Bacillus subtilis and Other Gram-Positive Bacteria: Biochemistry, Physiology, and Molecular Genetics. Sonenshein, A.L., Hoch, J.A., and Losick, R. (eds). Washington, DC: American Society for Microbiology Press, pp. 653-667.
43. Msadek, T., Dartois, V., Kunst, F., Herbaud, M.L., Denizot, F., and Rapoport, G. (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.
44. Murakami, K., Fujita, N., and Ishihama, A. (1996) Transcription factor recognition surface on the RNA polymerase α subunit is involved in contact with the DNA enhancer element. EMBO J 15: 4358-4367.
45. Nakano, M.M., and Zuber, P. (1989) Cloning and characterization of srfB: a regulatory gene involved in surfactin production and competence in Bacillus subtilis. J Bacteriol 171: 5347-5353.
46. Nakano, M.M., and Zuber, P. (1993) Mutational analysis of the regulatory region of the srfA operon in Bacillus subtilis. J Bacteriol 175: 3188-3191.
47. Nakano, M.M., Marahiel, M.A., and Zuber, P. (1988) Identification of a genetic locus required for biosynthesis of the lipopeptide antibiotic surfactin in Bacillus subtilis. J Bacteriol 170: 5662-5668.
48. Nakano, M.M., Xia, L., and Zuber, P. (1991) Transcription initiation region of the srfA operon which is controlled by the comP-comA signal transduction system in Bacillus subtilis. J Bacteriol 173: 5487-5493.
49. Nakano, M.M., Zuber, P., Glaser, P., Danchin, A., and Hulett, F.M. (1996) Two-component regulatory proteins ResD-ResE are required for transcriptional activation of fnr upon oxygen limitation in Bacillus subtilis. J Bacteriol 178: 3796-3802.
50. Nanamiya, H., Ohashi, Y., Asai, K., Moriya, S., Ogasawara, N., Fujita, M., et al. (1998) ClpC regulates the fate of a sporulation initiation sigma factor, sigmaH protein in Bacillus subtilis at elevated temperatures. Mol Microbiol 29: 505-513.
51. Ogura, M., Liu, L., LaCelle, M., Nakano, M.M., and Zuber, P. (1999) Mutational analysis of ComS: Evidence for the interaction of ComS and MecA in the regulation of competence development in Bacillus subtilis. Mol Microbiol 32: 799-812.
52. Pak, M., Hoskins, J.R., Singh, S.K., Maurizi, M.R., and Wickner, S. (1999) Concurrent chaperone and protease activities of ClpAP and the requirement for the N-terminal ClpA ATP binding site for chaperone activity. J Biol Chem 274: 19316-19322.
53. Perego, M. (1997) A peptide export-import control circuit modulating bacterial development regulates protein phosphatases of the phosphorelay. Proc Natl Acad Sci USA 94: 8612-8617.
54. Perego, M. (1998) Kinase-phosphatase competition regulates Bacillus subtilis development. Trends Microbiol 6: 366-370.
55. Perego, M., Higgins, C.F., Pearce, S.R., Gallagher, M.P., and Hoch, J.A. (1991) The oligopeptide transport system of Bacillus subtilis plays a role in the initiation of sporulation. Mol Microbiol 5: 173-185.
56. Persuh, M., Turgay, K., Mandic-Mulec, I., and Dubnau, D. (1999) The N-and C-terminal domains of MecA recognize different partners in the competence molecular switch. Mol Microbiol 33: 886-894.
57. Piazza, F., Tortosa, P., and Dubnau, D. (1999) Mutational analysis and membrane topology of ComP, a quorum-sensing histidine kinase of Bacillus subtilis controlling competence development. J Bacteriol 181: 4540-4548.
58. Pratt, L.A., and Silhavy, T.J. (1996) The response regulator SprE controls the stability of RpoS. Proc Natl Acad Sci USA 93: 2488-2492.
59. Price, C., Boylan, S., Duncan, M., Kalman, S., Suh, J.W., Thomas, S., et al. (1988) Use of λgt11 and antibody probes to isolate genes encoding RNA polymerase subunits from Bacillus subtilis. In Genetics and Biotechnology of Bacilli, Vol. 2. Ganesan, A.T., and Hoch, J.A. (eds). San Diego: Academic Press, pp. 183-188.
60. Roggiani, M., and Dubnau, D. (1993) ComA, a phosphorylated response regulator protein of Bacillus subtilis, binds to the promoter region of srfA. J Bacteriol 175: 3182-3187.
61. Ross, W., Gosink, K.K., Salomon, J., Igarashi, K., Zou, C., Ishihama, A., et al. (1993) A third recognition element in bacterial promoters: DNA binding by the alpha subunit of RNA polymerase. Science 262: 1407-1413.
62. Rudner, D.Z., Ledeaux, J.R., Ireton, K., and Grossman, A.D. (1991) The spo0K locus of Bacillus subtilis is homologous to the oligopeptide permease locus and is required for sporulation and competence. J Bacteriol 173: 1388-1398.
63. Santagata, S., Bhattacharyya, D., Wang, F.H., Singha, N., Hodtsev, A., and Spanopoulou, E. (1999) Molecular cloning and characterization of a mouse homolog of bacterial ClpX, a novel mammalian class II member of the Hsp100/Clp chaperone family. J Biol Chem 274: 16311-16319.
64. Schweder, T., Lee, K.H., Lomovskaya, O., and Matin, A. (1996) Regulation of Escherichia coli starvation sigma factor (sigma s) by ClpXP protease. J Bacteriol 178: 470-476.
65. Sekiguchi, J., Akeo, K., Yamamoto, H., Khasanov, F.K., Alonso, J.C., and Kuroda, A. (1995) Nucleotide sequence and regulation of a new putative cell wall hydrolase gene, cwlD, which affects germination in Bacillus subtilis. J Bacteriol 177: 5582-5589.
66. Serror, P., and Sonenshein, A.L. (1996) CodY is required for nutritional repression of Bacillus subtilis genetic competence. J Bacteriol 178: 5910-5915.
67. van Sinderen, D., and Venema, G. (1994) comK acts as an autoregulatory control switch in the signal transduction route to competence in Bacillus subtilis. J Bacteriol 176: 5762-5770.
68. van Sinderen, D., Galli, G., Cosmina, P., de Ferra, F., Withoff, S., Venema, G., et al. (1993) Characterization of the srfA locus of Bacillus subtilis: only the valine-activating domain of srfA is involved in the establishment of genetic competence. Mol Microbiol 8: 833-841.
69. van Sinderen, D., Luttinger, A., Kong, L., Dubnau, D., Venema, G., and Hamoen, L. (1995) comK encodes the competence transcription factor, the key regulatory protein for competence development in Bacillus subtilis. Mol Microbiol 15: 455-462.
70. Solomon, J.M., Magnuson, R., Srivastava, A., and Grossman, A.D. (1995) Convergent sensing pathways mediate response to two extracellular competence factors in Bacillus subtilis. Genes Dev 9: 547-558.
71. Solomon, J.M., Lazazzera, B.A., and Grossman, A.D. (1996) Purification and characterization of an extracellular peptide factor that affects two different developmental pathways in Bacillus subtilis. Genes Dev 10: 2014-2024.
72. Steinmetz, M., and Richter, R. (1994) Plasmids designed to alter the antibiotic resistance expressed by insertion mutations in Bacillus subtilis, through in vivo recombination. Gene 142: 79-83.
73. Suh, J.W., Boylan, S.A., Oh, S.H., and Price, C.W. (1996) Genetic and transcriptional organization of the Bacillus subtilis spc-α region. Gene 169: 17-23.
74. Sun, G., Sharkova, E., Chesnut, R., Birkey, S., Duggan, M.F., Sorokin, A., et al. (1996) Regulators of aerobic and anaerobic respiration in Bacillus subtilis. J Bacteriol 178: 1374-1385.
75. Tang, H., Severinov, K., Goldfarb, A., Fenyo, D., Chait, B., and Ebright, R.H. (1994) Location, structure, and function of the target of a transcriptional activator protein. Genes Dev 8: 3058-3067.
76. Turgay, K., Hamoen, L.W., Venema, G., and Dubnau, D. (1997) Biochemical characterization of a molecular switch involving the heat shock protein ClpC, which controls the activity of ComK, the competence transcription factor of Bacillus subtilis. Genes Dev 11: 119-128.
77. Turgay, K., Hahn, J., Burghoorn, J., and Dubnau, D. (1998) Competence in Bacillus subtilis is controlled by regulated proteolysis of a transcription factor. EMBO J 17: 6730-6738.
78. Vollenbroich, D., Mehta, N., Zuber, P., Vater, J., and Kamp, R.M. (1994) Analysis of surfactin synthetase subunits in srfA mutants of Bacillus subtilis OKB105. J Bacteriol 176: 395-400.
79. Wawrzynow, A., Wojtkowiak, D., Marszalek, J., Banecki, B., Jonsen, M., Graves, B., et al. (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.
80. Weinrauch, Y., Guillen, N., and Dubnau, D.A. (1989) Sequence and transcription mapping of Bacillus subtilis competence genes comB and comA, one of which is related to a family of bacterial regulatory determinants. J Bacteriol 171: 5362-5375.
81. Weinrauch, Y., Penchev, R., Dubnau, E., Smith, I., and Dubnau, D. (1990) A Bacillus subtilis regulatory gene product for genetic competence and sporulation resembles sensor protein members of the bacterial two-component signal-transduction systems. Genes Dev 4: 860-872.
82. Yansura, D.G., and Henner, D.J. (1985) Use of the E. coli lac repressor and operator to control gene expression in Bacillus subtilis. Proc Natl Acad Sci USA 81: 439-443.
83. Yon, J.R., Sammons, R.L., and Smith, D.A. (1989) Cloning and sequencing of the gerD gene of Bacillus subtilis. J Gen Microbiol 135: 3431-3445.
84. Youngman, P., Poth, H., Green, B., York, K., Olmedo, G., and Smith, K. (1989) Methods for genetic manipulation, cloning, and functional analysis of sporulation genes in Bacillus subtilis. In Regulation of Procaryotic Development. Smith, I., Slepecky, R.A., and Setlow, P. (eds). Washington, DC: American Society for Microbiology Press, pp. 65-87.
85. Zhou, Y., and Gottesman, S. (1998) Regulation of proteolysis of the stationary-phase sigma factor RpoS. J Bacteriol 180: 1154-1158.
86. Zou, C., Thomas, M.S., Keen, J., and Glass, R.E. (1997) A nested set of C-terminal deletions of the α subunit of Escherichia coli RNA polymerase define regions concerned with assembly, proteolysis, stabilization and transcriptional activation in vivo. Genes Cells 2: 81-94.
87. Zuber, P., and Losick, R. (1983) Use of a lacZ fusion to study the role of the spo0 genes of Bacillus subtilis in developmental regulation. Cell 35: 275-283.
88. Zuber, P., and Losick, R. (1987) Role of AbrB in the Spo0A-and Spo0B-dependent utilization of a sporulation promoter in Bacillus subtilis. J Bacteriol 169: 2223-2230.