Regulation of the activity of the Bacillus subtilis antiterminator LicT by multiple PEP-dependent, enzyme I- and HPr-catalysed phosphorylation

Molecular Microbiology

Volumn 31, Issue 3, 1999, Pages 995-1006

  Lindner, Cordula ^a,b   Galinier, Anne ^a   Hecker, Michael ^b   Deutscher, Josef ^a  

^a CNRS   (France)

^b UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; BACTERIAL PROTEIN; HISTIDINE; PHOSPHOENOLPYRUVATE; POLYACRYLAMIDE GEL; UREA;

AMINO TERMINAL SEQUENCE; ARTICLE; BACILLUS SUBTILIS; CATABOLITE REPRESSION; CONTROLLED STUDY; ISOTOPE LABELING; MASS SPECTROMETRY; NONHUMAN; OPERON; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; REVERSED PHASE LIQUID CHROMATOGRAPHY;

AMINO ACID SEQUENCE; BACILLUS SUBTILIS; BACTERIAL PROTEINS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GENE EXPRESSION REGULATION, BACTERIAL; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PHOSPHOENOLPYRUVATE SUGAR PHOSPHOTRANSFERASE SYSTEM; PHOSPHORYLATION; PHOSPHOTRANSFERASES (NITROGENOUS GROUP ACCEPTOR); SEQUENCE HOMOLOGY, AMINO ACID; TIME FACTORS; TRANSCRIPTION FACTORS;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); POSIBACTERIA; TRIXIS;

EID: 0032905438     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1999.01262.x     Document Type: Article

References (52)

1. Arnaud, M., Vary, P., Zagorec, M., Klier, A., Débarbouillé, M., Postma, P.W., et al. (1992) Regulation of the sacPA operon of Bacillus subtilis: Identification of phosphotransferase system components involved in SacT activity. J Bacteriol 174: 3161-3170.
2. Arnaud, M., Débarbouillé, M., Rapoport, G., Saier, Jr, M.H., and Reizer, J. (1996) In vitro reconstitution of transcriptional antitermination by the SacT and SacY proteins of Bacillus subtilis. J Biol Chem 271: 18966-18972.
3. Aymerich, S., and Steinmetz, M. (1992) Specificity determinants and structural features in the RNA target of the bacterial antiterminator proteins of the BglG/SacY family. Proc Natl Acad Sci USA 89: 10410-10414.
4. Bachem, S., and Stülke, J. (1998) Regulation of the Bacillus subtilis GIcT antiterminator protein by components of the phosphotransferase system. J Bacteriol 180: 5319-5326.
5. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
6. Chen, Q., Arents, J.C., Bader, R., Postma, P.W., and Amster-Choder, O. (1997a) BgIF, the sensor of the E. coli bgl system, uses the same site to phosphorylate both a sugar and a regulatory protein. EMBO J 16: 4617-4627.
7. Chen, Q., Engelberg-Kulka, H., and Amster-Choder, O. (1997b) The localization of the phosphorylation site of BgIG, the response regulator of the Escherichia coli bgl sensory system. J Biol Chem 272: 17263-17268.
8. Crutz, A.M., Steinmetz, M., Aymerich, S., Richter, R., and Le Coq, D. (1990) Induction of levansucrase in Bacillus subtilis: an antitermination mechanism negatively controlled by the phosphotransferase system. J Bacteriol 172: 1043-1050.
9. Débarbouillé, M., Arnaud, M., Fouet, A., Klier, A., and Rapoport, G. (1990) The sacT gene regulating the sacPA operon in Bacillus subtilis shares strong homology with transcriptional antiterminators. J Bacteriol 172: 3966-3973.
10. Deutscher, J., and Engelmann, R. (1984) Purification and characterization of an ATP-dependent protein kinase from Streptococcus faecalis. FEMS Microbiol Lett 23: 157-162.
11. Deutscher, J., and Saier, Jr, M.H. (1984) ATP-dependent, protein kinase-catalysed phosphorylation of a seryl residue in HPr, the phosphoryl carrier protein of the phosphotransferase system in Streptococcus pyogenes. Proc Natl Acad Sci USA 80: 6790-6794.
12. Deutscher, J., and Sauerwald, H. (1986) Stimulation of dihydroxyacetone and glycerol kinase activity in Streptococcus faecalis by phosphoenolpyruvate-dependent phosphorylation catalysed by enzyme I and HPr of the phosphotransferase system. J Bacteriol 163: 829-8361.
13. lac, a trimeric phosphocarrier protein that also acts as a phase transfer catalyst. Biochemistry 21: 4867-4873.
14. Deutscher, J., Pevec, B., Beyreuther, K., Kiltz, H.-H., and Hengstenberg, W. (1986) Streptococcal phosphoenolpyruvate-sugar phosphotransferase system: amino acid sequence and site of ATP-dependent phosphorylation of HPr. Biochemistry 25: 6543-6551.
15. Deutscher, J., Bauer, B., and Sauerwald, H. (1993) Regulation of glycerol metabolism in Enterococcus faecalis by phosphoenolpyruvate-dependent phosphorylation of glycerol kinase catalyzed by enzyme I and HPr of the phosphotransferase system. J Bacteriol 175: 3730-3733.
16. Deutscher, J., Reizer, J., Fischer, C., Galinier, A., Saier, Jr, M.H., and Steinmetz, M. (1994) Loss of protein kinase-catalysed phosphorylation of HPr, a phosphocarrier protein of the phosphotransferase system, by mutation of the ptsH gene confers catabolite repression resistance to several catabolic genes of Bacillus subtilis. J Bacteriol 176: 3336-3344.
17. Deutscher, J., Küster, E., Bergstedt, U., Charrier, V., and Hillen, W. (1995) Protein kinase-dependent HPr/CcpA interaction links glycolytic activity to carbon catabolite repression in Gram-positive bacteria. Mol Microbiol 15: 1049-1053.
18. Eisermann, R., Deutscher, J., Gonzy-Tréboul, G., and Hengstenberg, W. (1988) Site-directed mutagenesis with the ptsH gene of Bacillus subtilis: Isolation and characterization of heat stable proteins altered at the ATP-dependent regulatory phosphorylation site. J Biol Chem 263: 17050-17054.
19. El Hassouni, M., Henrissat, B., Chippaux, M., and Barras, F. (1992) Nucleotide sequences of the arb genes, which control beta-glucoside utilization in Erwinia chrysanthemi: comparison with the Escherichia coli bgl operon and evidence for a new beta-glycohydrolase family including enzymes from eubacteria, archeabacteria, and humans. J Bacteriol 174: 765-777.
20. Fujita, Y., Miwa, Y., Galinier, A., and Deutscher, J. (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.
21. Galinier, A., Haiech, J., Kilhoffer, M.-C., Jaquinod, M., Stülke, J., Deutscher, J., et al. (1997). The Bacillus subtilis crh gene encodes a HPr-like protein involved in carbon catabolite repression. Proc Natl Acad Sci USA 94: 8439-8444.
22. Galinier, A., Kravanja, M., Engelmann, R., Hengstenberg, W., Kilhoffer, M.C., Deutscher, J., et al. (1998) New protein kinase and protein phosphatase families mediate signal transduction in bacterial catabolite repression. Proc Natl Acad Sci USA 95: 1823-1828.
23. Gösseringer, R., Küster, E., Galinier, A., Deutscher, J., and Hillen, W. (1997) Cooperative and non-cooperative binding modes of catabolite control protein CcpA from Bacillus megaterium result from sensing two different signals. J Mol Biol 266: 665-676.
24. Gough, J.A., and Murray, N.E. (1983) Sequence diversity among related genes for recognition of specific targets in DNA molecules. J Mol Biol 166: 1-19.
25. Hoch, J.A. (1991) Genetic analysis in Bacillus subtilis. Methods Enzymol 204: 305-320.
26. Hueck, C.J., Hillen, W., and Saier, Jr, M.H. (1994) Analysis of a cis-active sequence mediating catabolite repression in gram-positive bacteria. Res Microbiol 145: 503-518.
27. Kohlbrecher, D., Eisermann, R., and Hengstenberg, W. (1992) Staphylococcal phosphoenolpyruvate-dependent phosphotransferase system: molecular cloning and nucleotide sequence of the Staphylococcus carnosus ptsl gene and expression and complementation studies of the gene product. J Bacteriol 174: 2208-2214.
28. Krüger, S., and Hecker, M. (1995) Regulation of the putative bglPH operon for aryl-β-glucoside utilization in Bacillus subtilis. J Bacteriol 177: 5590-5597.
29. Krüger, S., Gertz, S., and Hecker, M. (1996) Transcriptional analysis of bglPH expression in Bacillus subtilis: evidence for two distinct pathways mediating carbon catabolite repression. J Bacteriol 178: 2637-2644.
30. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
31. Le Coq, D., Lindner, C., Krüger, S., Steinmetz, M., and Stülke, J. (1995) New β-glucoside (bgl) genes in Bacillus subtilis: the bglP gene product has both transport and regulatory functions similar to those of BglF, its Escherichia coli homolog. J Bacteriol 177: 1527-1535.
32. Lindner, C. (1998) The bglPH operon from Bacillus subtilis and its regulation by the antiterminator protein LicT (in German). Doctoral Thesis, University of Greifswald, Germany.
33. Mahadevan, S., and Wright, A. (1987) A bacterial gene involved in transcription antitermination: regulation at a rho-independent terminator in the bgl operon of E. coli. Cell 50: 485-494.
34. Martin, I., Debarbouille, M., Klier, A., and Rapoport, G. (1989) Induction and metabolite regulation of levanase synthesis in Bacillus subtilis. J Bacteriol 171: 1885-1892.
35. Martin-Verstraete, I., Charrier, V., Stülke, J., Galinier, A., Rapoport, G., and Deutscher, J. (1998) Antagonistic effects on the activity of the Bacillus subtilis transcriptional activator LevR by dual PTS-catalysed phosphorylation. Mol Microbiol 28: 293-304.
36. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
37. Postma, P.W., Lengeler, J.W., and Jacobson, G.R. (1993) Phosphoenolpyruvate: carbohydrate phosphotransferase systems of bacteria. Microbiol Rev 57: 543-594.
38. Reizer, J., Hoischen, C., Titgemeyer, F., Rivolta, C., Rabus, R., Stülke, J., et al. (1998) A novel protein kinase that controls carbon catabolite repression in bacteria. Mol Microbiol 27: 1157-1169.
39. 32P] phosphoenolpyruvate via the pyruvate kinase exchange reaction at equilibrium. Biochim Biophys Acta 760: 185-187.
40. Saier, Jr, M.H., and Reizer, J. (1992) Proposed uniform nomenclature for the proteins and protein domains of the bacterial phosphoenolpyruvate: sugar phosphotransferase system. J Bacteriol 174: 1433-1438.
41. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning, a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
42. Sanger, F., Nicklen, S., and Coulson, A.R. (1977) DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74: 5463-5467.
43. Schnetz, K., Toloczyki, C., and Rak, B. (1987) Beta-glucoside (bgl) operon of Escherichia coli K-12: nucleotide sequence, genetic organization, and possible evolutionary relationship to regulatory components of two Bacillus subtilis genes. J Bacteriol 169: 2579-2590.
44. Schnetz, K., Stülke, J., Gertz, S., Krüger, S., Krieg, M., Hecker, M., et al. (1996) LicT, a Bacillus subtilis transcriptional antiterminator protein of the BglG family. J Bacteriol 178: 1971-1979.
45. Schön, U., and Schumann, W. (1994) Construction of His6-tagging vectors allowing single-step purification of GroES and other polypeptides produced in Bacillus subtilis. Gene 147: 91-94.
46. Steinmetz, M. (1993) Carbohydrate catabolism: Pathways, enzymes, genetic regulation, and evolution. 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. 157-170.
47. Stülke, J., Martin-Verstraete, I., Zagorec, M., Rose, M., Klier, A., and Rapoport, G. (1997) Induction of the Bacillus subtilis ptsGHI operon by glucose is controlled by a novel antiterminator, GlcT. Mol Microbiol 25: 65-78.
48. Stülke, J., Arnaud, M., Rapoport, G., and Martin-Verstraete, I. (1998) PRD - a protein domain involved in PTS-dependent induction and carbon catabolite repression of catabolic operons in bacteria. Mol Microbiol 28: 865-874.
49. Tobisch, S., Glaser, P., Krüger, S., and Hecker, M. (1997) Identification and characterization of a new β-glucoside utilization system in Bacillus subtilis. J Bacteriol 179: 496-506.
50. Tortosa, P., Aymerich, S., Lindner, C., Saier, Jr, M.H., Reizer, J., and Le Coq, D. (1997) Multiple phosphorylation of SacY, a Bacillus subtilis transcriptional antiterminator negatively controlled by the phosphotransferase system. J Biol Chem 272: 17230-17237.
51. Waygood, E.B., Mattoo, R.L, Erickson, E., and Vadeboncoeur, C. (1986) Phosphoproteins and the phosphoenolpyruvate: sugar phosphotransferase system of Streptococcus salivarius. Detection of two different ATP-dependent phosphorylations of the phosphocarrier protein HPr. Can J Microbiol 32: 310-318.
52. Zukowski, M.M., Miller, L., Cosgwell, P., Chen, K., Aymerich, S., and Steinmetz, M. (1990) Nucleotide sequence of the sacS locus of Bacillus subtilis reveals the presence of two regulatory genes. Gene 90: 153-155.