Elaborate transcription regulation of the Bacillus subtilis ilv-leu operon involved in the biosynthesis of branched-chain amino acids through global regulators of CcpA, CodY and TnrA

Molecular Microbiology

Volumn 56, Issue 6, 2005, Pages 1560-1573

  Tojo, Shigeo ^a   Satomura, Takenori ^a   Morisaki, Kaori ^a   Deutscher, Josef ^b   Hirooka, Kazutake ^a   Fujita, Yasutaro ^a  

^a FUKUYAMA UNIVERSITY   (Japan)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BRANCHED CHAIN AMINO ACID; CATABOLITE RESPONSIVE ELEMENT; CIS ACTING ELEMENT; GLUTAMIC ACID; GLUTAMINE; NITROGEN; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; AMINO ACID SYNTHESIS; ARTICLE; BACILLUS SUBTILIS; CCPA GENE; CODY GENE; DNA FOOTPRINTING; GENE CONTROL; GENE FUNCTION; ILV LEU GENE; NONHUMAN; OPERON; PRIORITY JOURNAL; PROMOTER REGION; REGULATOR GENE; TNRA GENE; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

AMINO ACIDS, BRANCHED-CHAIN; BACILLUS SUBTILIS; BACTERIAL PROTEINS; BASE SEQUENCE; DNA FOOTPRINTING; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; ISOLEUCINE; LEUCINE; MOLECULAR SEQUENCE DATA; NITROGEN; OPERON; REPRESSOR PROTEINS; RESPONSE ELEMENTS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; VALINE;

BACILLUS SUBTILIS;

EID: 20344400380     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2005.04635.x     Document Type: Article

References (50)

1. Anagnostopoulos, C., and Spizizen, J. (1961) Requirements for transformation of Bacillus subtilis. J Bacteriol 81: 741-746.
2. Atkinson, M.R., Wray, L.V., Jr, and Fisher, S.H. (1990) Regulation of histidine and proline degradation enzymes by amino acid availability in Bacillus subtilis. J Bacteriol 172: 4758-4765.
3. Belitsky, B.R., Wray, L.V., Jr, Fisher, S.H., Bohannon, D.E., and Sonenshein, A.L. (2000) Role of TnrA in nitrogen source-dependent repression of Bacillus subtilis glutamate synthase gene expression. J Bacteriol 182: 5939-5947.
4. Deutscher, J., Galinier, A., and Martin-Verstraete, I. (2002) Carbohydrate uptake and metabolism. In Bacillus Subtilis and its Closest Relatives: from Genes to Cells. Sonenshein, A.L., Hoch, J.A, and Losick, R. (eds). Washington, DC: American Society for Microbiolgy Press, pp. 129-150.
5. Eisermann, R., Fischer, R., Kessler, U., Neubauer, A., and Hengstenberg, W. (1991) Staphylococcal phosphoenolpyruvate-dependent phosphotransferase system. Purification and protein sequencng of the Staphylococcus carnosus histidine-containing protein, and cloning and DNA sequencing of the pfsH gene. Eur J Biochem 197: 9-14.
6. Eymann, C., Homuth, G., Scharf, C., and Hecker, M. (2002) Bacillus subtilis functional genomics: global characterization of the stringent response by proteome and transcriptome analysis. J Bacteriol 184: 2500-2520.
7. Fink, P.S. (1993) Biosynthesis of the branched-chain amino acids. In Bacillus Subtilis and Other Gram-Positive Bacteria. Sonenshein, A.L., Hoch, J.A, and Losick, R. (eds). Washington, DC: American Society for Microbiolgy Press, pp. 307-317.
8. Fujita, Y., and Freese, E. (1979) Purification and properties of fructose-1,6-bisphosphatase of Bacillus subtilis. J Biol Chem 254: 5340-5349.
9. 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.
10. Galinier, A., Haiech, J., Kilhoffer, M.C., Jaquinod, M., Stülke, J., Deutscher, J., and Martin-Verstraete, I. (1997) The Bacillus subtilis crh gene encodes a HPr-like protein involved in carbon catabolite repression. Proc Natl Acad Sci USA 94: 8439-8444.
11. Grandoni, J.A., Zahler, S.A., and Calvo, J.M. (1992) Transcriptional regulation of the ilv-leu operon of Bacillus subtilis. J Bacteriol 174: 3212-3219.
12. Grandoni, J.A., Fulmer, S.B., Brizzio, V., Zahler, S.A., and Calvo, J.M. (1993) Regions of the Bacillus subtilis ilv-leu operon involved in regulation by leucine. J Bacteriol 175: 7581-7593.
13. Grundy, F.J., and Henkin, T.M. (1994) Conservation of a transcription antitermination mechanism in aminoacyl-tRNA synthetase and amino acid biosynthesis genes in Gram-positive bacteria. J Mol Biol 235: 798-804.
14. Henkin, T.M., Grundy, F.J., Nicholson, W.L., and Chambliss, G.H. (1991) Catabolite repression of α-amylase gene expression in Bacillus subtilis involves a trans-acting gene product homologous to the Escherichia coli lacl and galR repressors. Mol Microbiol 5: 575-584.
15. Horinouchi, S., and Weisblum, B. (1982) Nucleotide sequence and functional map of pC194, a plasmid that specifies inducible chloramphenicol resistance. J Bacteriol 150: 815-825.
16. Inaoka, T., and Ochi, K. (2002) RelA protein is involved in induction of genetic competence in certain Bacillus subtilis strains by moderating the level of intracellular GTP. J Bacteriol 184: 3923-3930.
17. Inaoka, T., Takahashi, K., Ohnishi-Kameyama, M., Yoshida, M., and Ochi, K. (2003) Guanine nucleotides guanosine 5′-diphosphate 3′-diphosphate and GTP co-operatively regulate the production of an antibiotic bacilysin in Bacillus subtilis. J Biol Chem 278: 2169-2176.
18. Itaya, M., Kondo, K., and Tanaka, T. (1989) A neomycin resistance gene cassette selectable in a single copy state in the Bacillus subtilis chromosome. Nucl Acids Res 17: 4410.
19. 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.
20. Ludwig, H., Meinken, C., Matin, A., and Stülke, J. (2002) 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.
21. Mäder, U., Homuth, G., Scharf, C., Büttner, K., Bode, R., and Hecker, M. (2002) Transcriptome and proteome analysis of Bacillus subtilis gene expression modulated by amino acid availability. J Bacteriol 184: 4288-4295.
22. Mäder, U., Hennig, S., Hecker, M., and Homuth, G. (2004) Transcriptional organization and posttranscriptional regulation of the Bacillus subtilis branched-chain amino acid biosynthesis genes. J Bacteriol 186: 2240-2252.
23. Marta, P.T., Ladner, R.D., and Grandoni, J.A. (1996) A CUC triplet confers leucine-dependent regulation of the Bacillus subtilis ilv-leu operon. J Bacteriol 178: 2150-2153.
24. de Mendoza, D., Schujman, G.E., and Aguilar, P.S. (2002) Biosynthesis and function of membrane lipids. In Bacillus Subtilis and Its Closest Relatives: from Genes to Cells. Sonenshein, A.L., Hoch, J.A, and Losick, R. (eds). Washington, DC: American Society for Microbiolgy Press, pp. 43-55.
25. Mijakovic, I., Poncet, S., Galinier, A., Monedero, V., Fieulaine, S., Janin, J., et al. (2002) Pyrophosphate-producing protein dephosphorylation by HPr kinase/phosphorylase: a relic of early life? Proc Natl Acad Sci USA 99: 13442-13447.
26. Miwa, Y., and Fujita, Y. (2001) Involvement of two distinct catabolite-responsive elements in catabolite repression of the Bacillus subtilis myoinositol (iol) operon. J Bacteriol 183: 5877-5884.
27. Miwa, Y., Saikawa, M., and Fujita, Y. (1994) Possible function and some properties of the CcpA protein of Bacillus subtilis. Microbiology 140: 2567-2575.
28. Miwa, Y., Nakata, A., Ogiwara, A., Yamamoto, M., and Fujita, Y. (2000) Evaluation and characterization of catabolite-responsive elements (cre) of Bacillus subtilis. Nucl Acids Res 28: 1206-1210.
29. Molle, V., Nakaura, Y., Shivers, R.P., Yamaguchi, H., Losick, R., Fujita, Y., and Sonenshein, A.L. (2003) Additional targets of the Bacillus subtilis global regulator CodY identified by chromatin immunoprecipitation and genome-wide transcript analysis. J Bacteriol 185: 1911-1922.
30. Moreno, M.S., Schneider, B.L., Maile, R.R., Weyler, W., and Saier, M.H., 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.
31. Ochi, K., Kandala, J.C., and Freese, E. (1982) Evidence that Bacillus subtilis sporulation induced by the stringent response is caused by the decrease in GTP or GDP. J Bacteriol 151: 1062-1065.
32. Pelchat, M., and Lapointe, J. (1999) Aminoacyl-tRNA synthetase genes of Bacillus subtilis: organization and regulation. Biochem Cell Biol 77: 343-347.
33. Presecan-Siedel, E., Galinier, A., Longin, R., Deutscher, J., Danchin, A., Glaser, P., and Martin-Verstraete, I. (1999) Catabolite regulation of the pta gene as part of carbon flow pathways in Bacillus subtilis. J Bacteriol 181: 6889-6897.
34. Ratnayake-Lecamwasam, M., Serror, P., Wong, K.W., and Sonenshein, A.L. (2001) Bacillus subtilis CodY represses early-stationary-phase genes by sensing GTP levels. Genes Dev 15: 1093-1103.
35. Renna, M.C., Najimudin, N., Winik, L.R., and Zahler, S.A. (1993) Regulation of the Bacillus subtilis alsS, alsD, and alsR genes involved in post-exponential-phase production of acetoin. J Bacteriol 175: 3863-3875.
36. Sambrook, J., and Russell, D.W. (2001) Molecular Cloning: a Laboratory Manual, 3rd edn. Cold Spring Harbor, New York: Cold Spring Harbor Laboratoy Press.
37. Schilling, C.H., Held, L., Torre, M., and Saier, M.H., 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.
38. Serror, P., and Sonenshein, A.L. (1996) CodY is required for nutritional repression of Bacillus subtilis genetic competence. J Bacteriol 178: 5910-5915.
39. Shivers, R.P., and Sonenshein, A.L. (2004) Activation of the Bacillus subtilis global regulator CodY by direct interaction with branched-chain amino acids. Mol Microbiol 53: 599-611.
40. Shivers, R.P., and Sonenshein, A.L. (2005) Bacillus subtilis ilvB operon: an intersection of global regulons. Mol Microbiol, doi:10.1111/j.1365-2958. 2005.04634.x.
41. Slack, F.J., Serror, P., Joyce, E., and Sonenshein, A.L. (1995) A gene required for nutritional repression of the Bacillus subtilis dipeptide permease operon. Mol Microbiol 15: 689-702.
42. Tojo, S., Satomura, T., Morisaki, K., Yoshida, K., Hirooka, K., and Fujita, Y. (2004) Negative transcriptional regulation of the ilv-leu operon for biosynthesis of branched-chain amino acids through the Bacillus subtilis global regulator TnrA. J Bacteriol 186: 7971-7979.
43. Turinsky, A.J., Grundy, F.J., Kim, J., Chambliss, G.H., and Henkin, T.M. (1998) Transcriptional activation of the Bacillus subtilis ackA gene requires sequences upstream of the promoter. J Bacteriol 180: 5961-5967.
44. Turinsky, A.J., Moir-Blais, T.R., Grundy, F.J., and Henkin, T.M. (2000) Bacillus subtilis ccpA gene mutants specifically defective in activation of acetoin biosynthesis. J Bacteriol 182: 5611-5614.
45. Wach, A. (1996) PCR-synthesis of marker cassettes with long flanking homology regions for gene disruptions in S. cerevisiae. Yeast 12: 259-265.
46. Wray, L.V., Jr, Zalieckas, J.M., and Fisher, S.H. (2001) Bacillus subtilis glutamine synthetase controls gene expression through a protein-protein interaction with transcription factor TnrA. Cell 107: 427-435.
47. Yoshida, K., Ishio, I., Nagakawa, E., Yamamoto, Y., Yamamoto, M., and Fujita, Y. (2000) Systematic study of gene expression and transcription organization in the gntZ-ywaA region of the Bacillus subtilis genome. Microbiology 146: 573-579.
48. Yoshida, K., Kobayashi, K., Miwa, Y., Kang, C., Matsunaga, M., Yamaguchi, H., et al. (2001) Combined transcriptome and proteome analysis as a powerful approach to study genes under glucose repression in Bacillus subtilis. Nucl Acids Res 29: 683-692.
49. Yoshida, K., Yamamoto, Y., Omae, K., Yamamoto, M., and Fujita, Y. (2002) Identification of two myo-inositol transporter genes of Bacillus subtilis. J Bacteriol 184: 983-991.
50. Yoshida, K., Yamaguchi, H., Kinehara, M., Ohki, Y., Nakaura, Y., and Fujita, Y. (2003) Identification of additional TnrA-regulated genes of Bacillus subtilis associated with a TnrA box. Mol Microbiol 49: 157-165.