1887

Abstract

Silencing of , the second structural gene of the tricistronic levansucrase operon encoding the endolevanase LevB, decreases the level of levansucrase expression in . Conversely, independent expression of greatly stimulates operon expression. This autogenous effect is mediated by the transcript, which carries an internal sequence (5′-AAAGCAGGCAA-3′) involved in the enhancing effect. , the transcript displays an affinity for the N-terminal fragment of SacY ( 0·2 μM), the regulatory protein that prevents transcription termination of the levansucrase operon. This positive-feedback loop leads to an increase in the operon expression when is growing in the presence of high sucrose concentrations. Under these conditions, extracellular levan synthesized by the fructosyl polymerase activity of levansucrase can be degraded mainly into levanbiose by the action of LevB. Levanbiose is neither taken up nor metabolized by the bacteria. This work modifies the present view of the status of levansucrase in physiology.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.27366-0
2004-11-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/150/11/mic1503669.html?itemId=/content/journal/micro/10.1099/mic.0.27366-0&mimeType=html&fmt=ahah

References

  1. Aymerich S., 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 U S A 89:10410–10414 [CrossRef]
    [Google Scholar]
  2. Aymerich S, Gonzy-Tréboul G., Steinmetz M. 1986; 5′-noncoding region sacR is the target of all identified regulation affecting the levansucrase gene in Bacillus subtilis. J Bacteriol 166:993–998
    [Google Scholar]
  3. Chambert R., Gonzy-Tréboul G. 1976; Levansucrase of Bacillus subtilis: kinetic and thermodynamic aspects of transfructosylation processes. Eur J Biochem 62:55–64 [CrossRef]
    [Google Scholar]
  4. Chambert R., Petit-Glatron M. F. 1984; Hyperproduction of exocellular levansucrase by Bacillus subtilis: examination of the phenotype of a sacUh strain. J Gen Microbiol 130:3143–3152
    [Google Scholar]
  5. Chambert R., Petit-Glatron M. F. 1988; Secretion mechanism of Bacillus subtilis levansucrase: characterization of the second step. J Gen Microbiol 134:1205–1214
    [Google Scholar]
  6. Chambert R., Petit-Glatron M. F. 1993; Immobilisation of levansucrase on calcium phosphate gel strongly increases its polymerase activity. Carbohydr Res 244:129–136 [CrossRef]
    [Google Scholar]
  7. Chambert R., Dedonder R, Tréboul G. 1974; Kinetic studies of levansucrase of Bacillus subtilis. Eur J Biochem 41:285–300 [CrossRef]
    [Google Scholar]
  8. Chambert R., Rain-Guion M. C., Petit-Glatron M. F. 1992; Readthrough of the Bacillus subtilis levansucrase stop codon produces an extended enzyme displaying a higher polymerase activity. Biochim Biophys Acta 1132:145–153 [CrossRef]
    [Google Scholar]
  9. Crutz A. M., Steinmetz M., Aymerich S., Richter R., Le Coq D. 1990; Induction of levansucrase in Bacillus subtilis: an antitermination mechanism negatively controlled by the phosphotransferase system. J Bacteriol 172:1043–1050
    [Google Scholar]
  10. Débarbouillé M., Martin-Verstraete I., Arnaud M., Klier A., Rapoport G. 1991; Positive and negative regulation controlling expression of the sac genes in Bacillus subtilis . Res Microbiol 142:757–764 [CrossRef]
    [Google Scholar]
  11. Declerck N., Minh N. L., Yang Y., Bloch V., Kochoyan M., Aymerich S. 2002; RNA recognition by transcriptional antiterminators of the BglG/SacY family: mapping of SacY RNA binding site. J Mol Biol 319:1035–1048 [CrossRef]
    [Google Scholar]
  12. Dedonder R. 1966; Levansucrase from Bacillus subtilis. Methods Enzymol 8:500–506
    [Google Scholar]
  13. Goldberger R. F. 1974; Autogenous regulation of gene expression. Science 183:810–816 [CrossRef]
    [Google Scholar]
  14. Henkin T. M., Yanofsky C. 2002; Regulation by transcription attenuation in bacteria: how RNA provides instructions for transcription termination/antitermination decisions. Bioessays 24:700–707 [CrossRef]
    [Google Scholar]
  15. Hesselberth J. R., Ellington A. D. 2002; A (ribo)switch in the paradigms of genetic regulation. Nat Struct Biol 9:891–893 [CrossRef]
    [Google Scholar]
  16. Idelson M., Amster-Choder O. 1998; SacY, a transcriptional antiterminator from Bacillus subtilis, is regulated by phosphorylation in vivo . J Bacteriol 180:660–666
    [Google Scholar]
  17. Kunst F., Ogasawara N., Moszer I. 148 other authors 1997; The complete genome sequence of the Gram-positive bacterium Bacillus subtilis. Nature 390:249–256 [CrossRef]
    [Google Scholar]
  18. Le Hir H., Nott A., Moore M. J. 2003; How introns influence and enhance eukaryotic gene expression. Trends Biochem Sci 28:215–220 [CrossRef]
    [Google Scholar]
  19. Leloup L., Haddaoui el-A., Chambert R., Petit-Glatron M. F. 1997; Characterization of the rate-limiting step of the secretion of Bacillus subtilis α-amylase overproduced during the exponential phase of growth. Microbiology 143:3295–3303 [CrossRef]
    [Google Scholar]
  20. Leloup L., Le Saux J., Petit-Glatron M. F., Chambert R. 1999; Kinetics of the secretion of Bacillus subtilis levanase overproduced during the exponential phase of growth. Microbiology 145:613–619 [CrossRef]
    [Google Scholar]
  21. Lepesant J. A., Kunst F., Lepesant-Kejzlarova J., Dedonder R. 1972; Chromosomal location of mutations affecting sucrose metabolism in Bacillus subtilis Marburg. Mol Gen Genet 118:135–160
    [Google Scholar]
  22. Lepesant J. A., Kunst F., Pascal M., Lepesant-Kejzlarova J., Steinmetz M., Dedonder R. 1976; Specific and pleiotropic regulatory mechanism in the sucrose system of Bacillus subtilis. In Microbiology–1976 pp 58–69 Edited by Schlessinger D. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  23. Manival X., Yang Y., Strub M. P., Kochoyan M., Steinmetz M., Aymerich S. 1997; From genetic to structural characterization of a new class of RNA-binding domain within the SacY/BglG family of antiterminator proteins. EMBO J 16:5019–5029 [CrossRef]
    [Google Scholar]
  24. Nudler E., Mironov A. S. 2004; The riboswitch control of bacterial metabolism. Trends Biochem Sci 29:11–17 [CrossRef]
    [Google Scholar]
  25. Pereira Y., Chambert R., Leloup L., Daguer J. P., Petit-Glatron M. F. 2001a; Transcripts of the genes sacB, amyE, sacC and csn expressed in Bacillus subtilisunder the control of the 5′ untranslated sacR region display different stabilities that can be modulated. Microbiology 147:1331–1341
    [Google Scholar]
  26. Pereira Y., Petit-Glatron M. F., Chambert R. 2001b; yveB, encoding endolevanase LevB, is part of the sacByveByveA levansucrase tricistronic operon in Bacillus subtilis. Microbiology 147:3413–3419
    [Google Scholar]
  27. Petit-Glatron M. F., Chambert R. 1992; Peptide carrier potentiality of Bacillus subtilis levansucrase. J Gen Microbiol 138:1089–1095 [CrossRef]
    [Google Scholar]
  28. Rapoport G., Dedonder R. 1963; La lévane saccharase de Bacillus subtilis. II. Hydrolyse et transfert à partir des lévanes. Bull Soc Chim Biol (Paris) 45:493–513 (in French
    [Google Scholar]
  29. Rolland F., Moore B., Sheen J. 2002; Sugar sensing and signaling in plants. Plant Cell 14:S185–S205
    [Google Scholar]
  30. Rygus T., Scheler A., Allmansberger R., Hillen W. 1991; Molecular cloning, structure, promoters and regulatory elements for transcription of the Bacillus megaterium encoded regulon for xylose utilization. Arch Microbiol 155:535–542 [CrossRef]
    [Google Scholar]
  31. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  32. Serfling E. 1989; Autoregulation – a common property of eukaryotic transcription factors?. Trends Genet 5:131–133 [CrossRef]
    [Google Scholar]
  33. Smeekens S. 2000; Sugar-induced signal transduction in plants. Annu Rev Plant Physiol Plant Mol Biol 51:49–81 [CrossRef]
    [Google Scholar]
  34. Steinmetz M., Le Coq D., Aymerich S., Gay P, Gonzy-Tréboul G. 1985; The DNA sequence of the gene for the secreted Bacillus subtilis enzyme levansucrase and its genetic control sites. Mol Gen Genet 200:220–228 [CrossRef]
    [Google Scholar]
  35. Tortosa P., Le Coq D. 1995; A ribonucleic antiterminator sequence (RAT) and a distant palindrome are both involved in sucrose induction of the Bacillus subtilis sacXY regulatory operon. Microbiology 141:2921–2927 [CrossRef]
    [Google Scholar]
  36. Tortosa P., Aymerich S., Lindner C., Reizer J., Le Coq D, Saier M. H. Jr 1997; Multiple phosphorylation of SacY, a Bacillus subtilis transcriptional antiterminator negatively controlled by the phosphotransferase system. J Biol Chem 272:17230–17237 [CrossRef]
    [Google Scholar]
  37. Yang Y., Declerck N., Manival X., Aymerich S., Kochoyan M. 2002; Solution structure of the LicT-RNA antitermination complex: CAT clamping RAT. EMBO J 21:1987–1997 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.27366-0
Loading
/content/journal/micro/10.1099/mic.0.27366-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error