Catabolite repression and activation in Bacillus subtilis: Dependency on CcpA, HPr, and HprK

Journal of Bacteriology

Volumn 187, Issue 22, 2005, Pages 7826-7839

  Lorca, Graciela L ^a,c   Chung, Yong Joon ^a,d   Barabote, Ravi D ^a   Weyler, Walter ^b   Schilling, Christophe H ^a,e   Saier Jr , Milton H ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b GENENCOR INTERNATIONAL INC   (United States)

^c Banting and Best Department of Medical Research   (Canada)

^d Jeonju University   (South Korea)

^e GENOMATICA INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ACETOIN DEHYDROGENASE; ALANINE DEHYDROGENASE; BACTERIAL RNA; CARRIER PROTEIN; CATALASE; COMPLEMENTARY DNA; GLUCOSE; GLYCEROL KINASE; IRON; ISOCITRATE DEHYDROGENASE; MALATE DEHYDROGENASE; NITROGEN; NUCLEOSIDE DIPHOSPHATASE; OXOGLUTARATE DEHYDROGENASE; PENICILLIN BINDING PROTEIN; PERMEASE; PHOSPHORUS; PROTEIN CRH; PROTEIN HISTIDINE KINASE; PROTEIN HPR; PROTEIN HPRK; PROTEIN KINASE; RIBOSOME PROTEIN; SERINE; SUCCINATE DEHYDROGENASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CCPA; TRANSCRIPTOME; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL FLAGELLUM; BACTERIAL GENOME; CATABOLITE REPRESSION; CHEMOTAXIS; CONTROLLED STUDY; DNA MICROARRAY; GENE EXPRESSION REGULATION; IRON METABOLISM; NITROGEN METABOLISM; NONHUMAN; PHOSPHATE METABOLISM; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REGULON; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STRESS;

ADAPTATION, PHYSIOLOGICAL; BACILLUS SUBTILIS; BACTERIAL PROTEINS; BINDING SITES; DNA-BINDING PROTEINS; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GLUCOSE; NITROGEN; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHORUS; PROMOTER REGIONS (GENETICS); PROTEIN-SERINE-THREONINE KINASES; REPRESSOR PROTEINS; RNA, BACTERIAL; RNA, MESSENGER; TRANSCRIPTION FACTORS;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); POSIBACTERIA;

EID: 27744560433     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.187.22.7826-7839.2005     Document Type: Article

References (83)

1. Adhya, S. 1987. The galactose operon, p. 1503-1512. In F. C. Neidhardt et al. (ed.), Escherichia coli and Salmonella typhimurium: Cellular and molecular biology, vol. 2. ASM Press, Washington, D.C.
2. Aung-Hilbrich, L. M., G. Seidel, A. Wagner, and W. Hillen. 2002. Quantification of the influence of HPr-Ser46-P on CcpA-cre interaction. J. Mol. Biol. 319:77-85.
3. Blencke, H. M., G. Homuth, H. Ludwig, U. Mader, M. Hecker, and J. Stülke. 2003. Transcriptional profiling of gene expression in response to glucose in Bacillus subtilis: regulation of the central metabolic pathways. Metab. Eng. 5:133-149.
4. Böel, G., I. Myakovic, A. Maze, S. Poncet, M. K. Taha, M. Larribe, E. Darbon, A. Khemiri, A. Galinier, and J. Deutscher. 2003. Transcription regulators potentially controlled by HPr kinase/phosphorylase in Gram-negative bacteria. J. Mol. Microbiol. Biotechnol. 5:206-215.
5. Caldwell, R., R. Sapolsky, W. Weyler, R. R. Maile, S. C. Causey, and E. Ferrari. 2001. Correlation between Bacillus subtilis scoC phenotype and gene expression determined using microarrays for transcriptome analysis. J. Bacteriol. 183:7329-7340.
6. Chauvaux, S., I. T. Paulsen, and M. H. Saier, Jr. 1998. CcpB: a novel transcription factor implicated in catabolite repression in Bacillus subtilis. J. Bacteriol. 180:491-497.
7. Dahl, M. K. 2002. CcpA-independent carbon catabolite repression in Bacillus subtilis. J. Mol. Microbiol. Biotechnol. 4:315-321.
8. Darbon, E., P. Servant, S. Poncet, and J. Deutscher. 2002. Antitermination by GlpP, catabolite repression via CcpA and inducer exclusion triggered by P-GlpK dephosphorylation control Bacillus subtilis glpFK expression. Mol. Microbiol. 43:1039-1052.
9. de Saizieu, A., C. Gardes, N. Flint, C. Wagner, M. Kamber, T. J. Mitchell, W. Keck, K. E. Amrein, and R. Lange. 2000. Microarray-based identification of a novel Streptococcus pneumoniae regulon controlled by an autoinduced peptide. J. Bacteriol. 182:4696-4703.
10. Deutscher, J., and M. H. Saier, Jr. 1983. ATP-dependent protein kinase-catalyzed phosphorylation of a seryl residue in HPr, the phosphoryl carrier protein of the phosphotransferase system in Streptococcus pyogenes. Proc. Natl. Acad. Sci. USA 80:6790-6795.
11. Deutscher, J., E. Küster, U. Bergstedt, V. Charrier, and W. Hillen. 1995. Protein kinase-dependent HPr/CcpA interaction links glycolytic activity to carbon catabolite repression in Gram-positive bacteria. Mol. Microbiol. 15:1049-1053.
12. Fieulaine, S., S. Morera, S. Poncet, I. Mijakovic, A. Galinier, J. Janin, J. Deutscher, and S. Nessler. 2002. X-ray structure of a bifunctional protein kinase in complex with its protein substrate HPr. Proc. Natl. Acad. Sci. USA 99:13437-13441.
13. Fisher, S. H., M. A. Strauch, M. R. Atkinson, and L. V. Wray, Jr. 1994. Modulation of Bacillus subtilis catabolite repression by transition state regulatory protein AbrB. J. Bacteriol. 176:1903-1912.
14. Fujita, Y., Y. Miwa, A. Galinier, and J. Deutscher. 1995. Specific recognition of the Bacillus subtilis gnt cis-acting catabolite-responsive element by a protein complex formed between CcpA and seryl-phosphorylated HPr. Mol. Microbiol. 17:953-960.
15. Galinier, A., J. Deutscher, and I. Martin-Verstraete. 1999. Phosphorylation of either Crh or HPr mediates binding of CcpA to the Bacillus subtilis xyn cre and catabolite repression of the xyn operon. J. Mol. Biol. 286:307-314.
16. Galinier, A., J. Haiech, M.-C. Kilhoffer, M. Jaquinod, J. Stülke, J. Deutscher, and I. Martin-Verstraete. 1997. The Bacillus subtilis crh gene encodes a HPR-like protein involved in carbon catabolite repression. Proc. Natl. Acad. Sci. USA 94:8439-8444.
17. Glatz, E., R.-P. Nilsson, L. Rutberg, and B. Rutberg. 1996. A dual role for the Bacillus subtilis glpD leader and the GlpP protein in the regulated expression of glpD: Antitermination and control of mRNA stability. Mol. Microbiol. 19:319-328.
18. Gorke, B., L. Fraysse, and A. Galinier. 2004. Drastic differences in Crh and HPr synthesis levels reflect their different impacts on catabolite repression in Bacillus subtilis. J. Bacteriol. 186:2992-2995.
19. Gösseringer, R., E. Küster, A. Galinier, J. Deutscher, and W. Hillen. 1997. Cooperative and non-cooperative DNA binding modes of catabolite control protein CcpA from Bacillus megaterium result from sensing two different signals. J. Mol. Biol. 266:665-676.
20. Gosset, G., Z. Zhang, S. Nayyar, W. A. Cuevas, and M. H. Saier, Jr. 2004. Transcriptome analysis of Crp-dependent catabolite control of gene expression in Escherichia coli J. Bacteriol. 186:3516-3524.
21. Grundy, F. J., D. A. Waters, S. H. G. Allen, and T. M. Henkin. 1993. Regulation of the Bacillus subtilis acetate kinase gene by CcpA. J. Bacteriol. 175:7348-7355.
22. Hanson, K. G., K. Steinhauer, J. Reizer, W. Hillen, and J. Stülke. 2002. HPr kinase/phosphatase of Bacillus subtilis: expression of the gene and effects of mutations on enzyme activity, growth and carbon catabolite repression. Microbiology 148:1805-1811.
23. Henkin, T. M. 1996. The role of CcpA transcriptional regulator in carbon metabolism in Bacillus subtilis. FEMS Microbiol. Lett. 135:9-15.
24. Henkin, T. M., F. J. Grundy, W. L. Nicholson, and G. H. Chambliss. 1991. Catabolite repression of α-amylase gene expression in Bacillus subtilis involves a trans-acting gene product homologous to the Escherichia coli lacI and galR repressors. Mol. Microbiol. 5:575-584.
25. Hueck, C. J., and W. Hillen. 1995. Catabolite repression in Bacillus subtilis: A global regulatory mechanism for the Gram-positive bacteria? Mol. Microbiol. 15:395-401.
26. Hueck, C. J., W. Hillen, and M. H. Saier, Jr. 1994. Analysis of a cis-active sequence mediating catabolite repression in Gram-positive bacteria. Res. Microbiol. 145:503-518.
27. Ito, M., D. B. Hicks, T. M. Henkin, A. A. Guffanti, B. D. Powers, U Zvi, K. Uematsu, and T. A. Krulwich. 2004. MotPS is the stator-force generator for motility of alkaliphilic Bacillus, and its homologue is a second functional Mot in Bacillus subtilis. Mol. Microbiol. 53:1035-1049.
28. Keener, J., and M. Nomura. 1996. Regulation of ribosome synthesis, p. 1417-1431. In F. C. Neidhardt et al. (ed.), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed. ASM Press, Washington, D.C.
29. Kim, J.-H., A. Roux, and A. L. Sonenshein. 2002. Direct and indirect roles of CcpA in regulation of Bacillus subtilis Krebs cycle genes. Mol. Microbiol. 45:179-190.
30. Kim, J.-H., M. I. Voskuil, and G. H. Chambliss. 1998. NADP, a compressor for the Bacillus catabolite control protein CcpA. Proc. Natl. Acad. Sci. USA 95:9590-9595.
31. Kraus, A., C. Hueck, D. Gartner, and W. Hillen. 1994. Catabolite repression of the Bacillus subtilis xyl operon involves a cis element functional in the context of an unrelated sequence, and glucose exerts additional xylR-dependent repression. J. Bacteriol. 176:1738-1745.
32. Kravanja, M., R. Engelmann, V. Dossonnet, M. Blüggel, H. E. Meyer, R. Frank, A. Galinier, J. Deutscher, N. Schnell, and W. Hengstenberg. 1999. The hprK gene of Enterococcus faecalis encodes a novel bifunctional enzyme: The HPr kinase/phosphatase. Mol. Microbiol. 31:59-66.
33. Kunst, F., N. Ogasawara, I. Mozer, A. M. Albertini, G. Alloni, V. Azevedo., et al. 1997. The complete genome sequence of the Gram-positive bacterium Bacillus subtilis. Nature 390;249-256.
34. Lee, J. M., S. Zhang, S. Saha, S. Santa Anna, C. Jiang, and J. Perkins. 2001. RNA expression analysis using an antisense Bacillus subtilis genome array. J. Bacteriol. 183:7371-7380.
35. Liu, X., and H. W. Taber. 1998. Catabolite regulation of the Bacillus subtilis ctaBCDEF gene cluster. J. Bacteriol. 180:6154-6163.
36. Lockhart, D. J., H. Dong, M. C. Byrne, M. Follettie, M. V. Gallo, M. S. Chee, M. Mittmann, C. Wang, M. Kobayashi, H. Horton, and E. L. Brown. 1996. Expression monitoring by hybridization to high-density oligonucleotide arrays. Nat. Biotechnol. 14:675-1680.
37. Ludwig, H., C. Meinken, A. Matin, and J. Stülke. 2002a. Insufficient expression of the ilv-leu operon encoding enzymes of branched-chain amino acid biosynthesis limits growth of a Bacillus subtilis ccpA mutant. J. Bacteriol. 184:5174-5178.
38. Ludwig, H., N. Rebhan, H.-M. Blencke, M. Merzbacher, and J. Stülke. 2002b. Control of the glycolytic gapA operon by the catabolite control protein A in Bacillus subtilis: a novel mechanism of CcpA-mediated regulation. Mol. Microbiol. 45:543-553.
39. Magasanik, B. 1970. Glucose effects: inducer exclusion and repression, p. 189-219. In J. R. Beckwith and D. Zipser (ed.), The lactose operon. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
40. Mahr, K., C. D. Esteban, W. Hillen, F. Titgemeyer, and G. Perez-Martinez. 2002. Cross communication between components of carbon catabolite repression of Lactobacillus casei and Bacillus megatenum. J. Mol. Microbiol. Biotechnol. 4:489-494.
41. Martin-Verstraete, I., J. Deutscher, and A. Galinier. 1999. Phosphorylation of HPr and Crh by HprK, early steps in the catabolite repression signalling pathway for the Bacillus subtilis levanase operon. J. Bacteriol. 181:2966-2969.
42. Meinken, C, H. M. Blencke, H. Ludwig, and J. Stülke,. 2003. Expression of the glycolytic gapA operon in Bacillus subtilis: differential syntheses of proteins encoded by the operon. Microbiology 149:751-761.
43. Miwa, Y., and Y. Fujita. 1990. Determination of the cis sequence involved in catabolite repression of the Bacillus subtilis gnt operon: implication of a consensus sequence involved in catabolite repression in the genus Bacillus. Nucleic Acids Res. 18:7049-7053.
44. Miwa, Y., and Y. Fujita. 1993. Promoter-independent catabolite repression of the Bacillus subtilis gnt operon. J. Biochem. 113:665-671.
45. Miwa, Y., K. Nagura, S. Eguchi, H. Fukuda, J. Deutscher, and Y. Fujita. 1997. Catabolite repression of the Bacillus subtilis gnt operon exerted by two catabolite-responsive elements. Mol. Microbiol. 23:1203-1213.
46. Miwa, Y., A. Nakata, A. Ogiwara, M. Yamamoto, and Y. Fujita. 2000. Evaluation and characterization of catabolite-responsive elements (cre) of Bacillus subtilis. Nucleic Acids Res. 28:1206-1210.
47. Moreno, M. S., B. L. Schneider, R. R. Maile, W. Weyler, and M. H. Saier, Jr. 2001. Catabolite repression mediated by the CcpA protein in Bacillus subtilis: Novel modes of regulation revealed by whole genome analyses. Mol. Microbiol. 39:1366-1381.
48. Nessler, S., S. Fieulaine, S. Poncet, A. Galinier, J. Deutscher, and J. Janin. 2003. HPr kinase/phosphorylase, the sensor enzyme of catabolite repression in gram-positive bacteria: structural aspects of the enzyme and the complex with its protein substrate. J. Bacteriol. 185:4003-4010.
49. Nihashi, J.-I., and Y. Fujita. 1984. Catabolite repression of inositol dehydrogenase and gluconate kinase syntheses in Bacillus subtilis. Biochim. Biophys. Acta 789:88-95.
50. + symporter. J. Bacteriol. 180:498-504.
51. Poncet, S., I. Myakovic, S. Nessler, V. Gueguen-Chaignon, V. Chaptal, A. Galinier, G. Böel, A., Maze, and J. Deutscher. 2004. HPr kinase/phosphorylase, a Walker motif A-containing bifunctional sensor enzyme controlling catabolite repression in Gram-positive bacteria. Biochim. Biophys. Acta 1697:123-135.
52. Presecan-Siedel, E., A. Galinier, R. Longin, J. Deutscher, A. Danchin, P. Glaser, and I. Martin-Verstraete. 1999. The catabolite regulation of the pta gene as part of the carbon flow pathways in Bacillus subtilis. J. Bacteriol. 181:6889-6897.
53. Ramseier, T. M., D. Nègre, J.-C. Cortay, M. Scarabel, A. J. Cozzone, and M. H. Saier, Jr. 1993. In vitro binding of the pleiotropic transcriptional regulatory protein, FruR, to the fru, pps, pts, icd and ace operons of Escherichia coli and Salmonella typhimunum. J. Mol. Biol. 234:28-44.
54. Ramseier, T. M., J. Reizer, E. Küster, W. Hillen, and M. H. Saier, Jr. 1995. In vitro binding of the CcpA protein of Bacillus megaterium to cis-acting catabolite responsive elements (CREs) of Gram-positive bacteria. FEMS Microbiol. Lett. 129:207-214.
55. Ramseier, T. M., and M. H. Saier, Jr. 1995. cAMP-cAMP receptor protein complex: Five binding sites in the control region of the Escherichia coli mannitol operon. Microbiology 141:1901-1907.
56. Reizer, J., C. Hoischen, F. Titgemeyer, C. Rivolta, R. Rabus, J. Stülke, D. Karamata, M. H. Saier, Jr., and W. Hillen. 1998. A novel protein kinase that controls carbon catabolite repression in bacteria. Mol. Microbiol. 27:1157-1169.
57. Reizer, J., M. J. Novotny, C. Panos, and M. H. Saier, Jr. 1983. Mechanism of inducer expulsion in Streptococcus pyogenes: a two-step process activated by ATP. J. Bacteriol. 156:354-361.
58. Reizet, J., S. L. Sutrina, M. H. Saier, Jr., G. C. Stewart, A. Peterkofsky, and P. Reddy. 1989. Mechanistic and physiological consequences of HPr(ser) phosphorylation on the activities of the phosphoenolpyruvate:sugar phosphotransferase system in Gram-positive bacteria: studies with site-specific mutants of HPr. EMBO J. 8:2111-2120.
59. Saier, M. H., Jr. 1989. Protein phosphorylation and allosteric control of inducer exclusion and catabolite repression by the bacterial phosphoenolpyruvate:sugar phosphotransferase system. Microbiol. Rev. 53:109-120.
60. Saier, M. H., Jr., S. Chauvaux, G. M. Cook, J. Deutscher, I. T. Paulsen, J. Reizer, and J.-J. Ye. 1996a. Catabolite repression and inducer control in Gram-positive bacteria. Microbiology 142:217-230.
61. Saier, M. H., Jr., S. Chauvaux, J. Deutscher, J. Reizer, and J.-J. Ye. 1995. Protein phosphorylation and the regulation of carbon metabolism: Comparisons in Gram-negative versus Gram-positive bacteria. Trends Biochem. Sci. 20:267-271.
62. Saier, M. H., Jr., T. M. Ramseier, and J. Reizer. 1996b. Regulation of carbon utilization, p. 1325-1343. In F. C. Neidhardt et al. (ed.), Escherichia coli and Salmonella typhimurium: cellular and molecular biology, 2nd ed. ASM Press, Washington, D.C.
63. Schilling, C. H., L. Held, M. Torre, and M. H. Saier, Jr. 2000. GRASP-DNA: A web application to screen prokaryotic genomes for specific DNA-binding sites and repeat motifs. J. Mol. Microbiol. Biotechnol. 2:495-500.
64. Servant, P., D. Le Coq, and S. Aymerich. 2005. CcpN (YqzB), a novel regulator for CcpA-independent catabolite repression of Bacillus subtilis gluconeogenic genes. Mol. Microbiol. 55:1435-1451.
65. Strauch, M. A. 1995. AbrB modulates expression and catabolite repression of a Bacillus subtilis ribose transport operon. J. Bacteriol. 177:6727-6731.
66. Stülke, J. 2002. Control of transcription termination in bacteria by RNA-binding proteins that modulate RNA structures. Arch. Microbiol. 177:433-440.
67. Stülke, J., M. Arnaud, G. Rapoport, and I. Martin-Verstraete. 1998. PRD -a protein domain involved in PTS-dependent induction and carbon catabolite repression of catabolic operons in bacteria. Mol. Microbiol. 28:865-874.
68. Stülke, J., and W. Hillen. 1998. Coupling physiology and gene regulation in bacteria: The phosphotransferase sugar uptake system delivers the signals. Naturwissenschaften 85:583-592.
69. Stülke, J., and W. Hillen. 1999. Carbon catabolite repression in bacteria. Curr. Opin. Microbiol. 2:195-201.
70. Stülke, J., and W. Hillen. 2000. Regulation of carbon catabolism in Bacillus species. Annu. Rev. Microbiol. 54:849-880.
71. Tangney, M., A. Galinier, J. Deutscher, and W. J. Mitchell. 2003. Analysis of the elements of catabolite repression in Clostridium acetobutylicum ATCC 824. J. Mol. Microbiol. Biotechnol. 6:6-11.
72. Titgemeyer, F., and W. Hillen. 2002. Global control of sugar metabolism: a Gram-positive solution. Antonie Van Leeuwenhoek 82:59-71.
73. Tobisch, S., J. Stülke, and M. Hecker. 1999. Regulation of the lic operon of Bacillus subtilis and characterization of potential phosphorylation sites of the LicR regulator protein by site-directed mutagenesis. J. Bacteriol. 181:4995-5003.
74. Turinsky, A. J., F. J. Grundy, J.-H. Kim, G. H. Chambliss, and T. M. Henkin. 1998. Transcriptional activation of the Bacillus subtilis ackA gene requires sequences upstream of the promoter. J. Bacteriol. 180:5961-5967.
75. Wacker, I., H. Ludwig, I. Reif, H. M. Blencke, C. Detsch, and J. Stülke. 2003. The regulatory link between carbon and nitrogen metabolism in Bacillus subtilis: regulation of the gltAB operon by the catabolite control protein CcpA. Microbiology 149:3001-3009.
76. Warner, J. B., and J. S. Lolkema. 2003a. CcpA-dependent carbon catabolite repression in bacteria. Microbiol. Mol. Biol. Rev. 67:475-490.
77. Warner, J. B., and J. S. Lolkema. 2003b. A Crh-specific function in carbon catabolite repression in Bacillus subtilis. FEMS Microbiol. Lett. 220:277-280.
78. 2+-citrate transporter gene citM by arginine metabolism in Bacillus subtilis. J. Bacteriol. 185:854-859.
79. Wodicka, L., H. Dong, M. Mittmann, M.-H. Ho, and D. J. Lockhart. 1997. Genome-wide expression monitoring in Saccharomyces cerevisiae. Nat. Biotechnol. 15:1359-1367.
80. Yoshida, K., K. Kobayashi, Y. Miwa, C.-M. Kang, M. Matsunaga, H. Yamaguchi, S. Tojo, M. Yamamoto, R. Nishi, N. Ogasawara, T. Nakayama, and Y. Fujita. 2001. Combined transcriptome and proteome analysis as a powerful approach to study genes under glucose repression in Bacillus subtilis. Nucleic Acids Res. 29:683-692.
81. Zalieckas, J. M., L. V. Wray, Jr., A. E. Person, and S. H. Fisher. 1998a. Transcription-repair coupling factor is involved in carbon catabolite repression of the Bacillus subtilis hut and gnt operons. Mol. Microbiol. 27:1031-1038.
82. Zalieckas, J. M., L. V. Wray, Jr., and S. H. Fisher. 1998b. Expression of the Bacillus subtilis acsA gene: Position and sequence context affect cre-mediated carbon catabolite repression. J. Bacteriol. 180:6649-6654.
83. Zhang, Z., G. Gosset, R. Barabote, W. A. Cuevas, and M. H. Saier, Jr. 2005. Functional interactions between Crp and Fur in E. coli. J. Bacteriol. 187:980-990.