1887

Microbiology Society logo

Volume 142, Issue 9

Stringent and growth-rate-dependent control of the operon of K-12 Free

Abstract

The promoter of the operon has been located by transcript mapping using primer extension with reverse transcriptase. The surrounding nucleotide sequence has features characteristic of promoters under stringent and growth-rate-dependent regulation, namely a GC-rich discriminator next to the − 10 hexamer, an upstream AT-rich sequence (the UP element) and potential FIS-binding sites. Transcriptional activity of the promoter was examined using transcriptional fusions to placed at a single chromosomal location. Expression from was reduced under stringent conditions and varied with growth rate. Growth-rate control was independent of guanine-mediated repression. A fusion in which the GC-rich discriminator was mutated by insertion of an AT-rich oligonucleotide was used to demonstrate the importance of this region in control. Both stringent and growth-rate-dependent controls were abolished by the mutation. Other potential regulatory signals in the vicinity of the promoter are a operator (binding site for the PurR repressor), a operator, a DnaA-binding site and a CRP/FNR-binding sequence. The promoter lies back-to-back with the promoter for (exonuclease VII), the two promoters being separated by only 20 bp.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): Escherichia coli , growth-rate-dependent regulation , gua promoter and stringent control
© Society for General Microbiology 1996
Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-142-9-2429
1996-09-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/micro/142/9/mic-142-9-2429.html?itemId=/content/journal/micro/10.1099/00221287-142-9-2429&mimeType=html&fmt=ahah

References

  1. Ball C. A., Osuna R., Ferguson K. C., Johnson R. C. 1992; Dramatic changes in Fis levels upon nutrient upshift in Escherichia coli. J Bacteriol 174:8043–8056
     [Google Scholar]
  2. Baracchini E., Bremer H. 1988; Stringent and growth control of rRNA synthesis in Escherichia coli are both mediated by ppGpp. J Biol Chem 263:2597–2602
     [Google Scholar]
  3. Beck C. F., Warren R. A. J. 1988; Divergent promoters, a common form of gene organization. Microbiol Rev 52:318–326
     [Google Scholar]
  4. Bell A. I., Gaston K. L., Cole J., Busby S. 1989; Cloning of binding sequences for the Escherichia coli transcription activators, FNR and CRP: location of bases involved in discrimination between FNR and CRP. Nucleic Acids Res 17:3865–3874
     [Google Scholar]
  5. Bertrand K. P., Postle K., Wray L. V. Jr Reznikoff W. S. 1984; Construction of a single-copy promoter vector and its use in analysis of regulation of transposon Tn 10 tetracycline resistance determinant. J Bacteriol 158:910–919
     [Google Scholar]
  6. Bouvier J., Patte J., Stragier P. 1984; Multiple regulatory signals in the control region of the Escherichia coli carAB operon. Proc Natl Acad Sci USA 814139–4143
     [Google Scholar]
  7. Chase J. W., Rabin B. A., Murphy J. B., Stone K. L., Williams K. R. 1986; F.scherichia coli exonuclease VII: cloning and sequencing of the gene encoding the large subunit (xseA). J Biol Chem 261:14929–14935
     [Google Scholar]
  8. Choi K. Y., Zalkin H. 1992; Structural characterization and corepressor binding of the Escherichia coli purine repressor. J Bacteriol 174:6207–6214
     [Google Scholar]
  9. Condon C., Philips J., Fu Z.-Y., Squires C., Squires C. L. 1992; Comparison of the expression of seven ribosomal RNA operons in Escherichia coli . EMBO J 11:4175–4185
     [Google Scholar]
  10. Dickson R. R., Gaal T., deBoer H. A., de Haseth P. L., Gourse R. L. 1989; Identification of promoter mutants defective in growth-rate-dependent regulation of rRNA transcription in Escherichia coli . J Bacteriol 171:4862–4870
     [Google Scholar]
  11. Finkel S. E., Johnson R. C. 1992; The Fis protein: it’s not just for DNA inversion anymore. Mol Microbiol 6:3257–3265
     [Google Scholar]
  12. Freundlich M., Burns R. O., Umbarger H. E. 1962; Control of isoleucine, valine, and leucine biosynthesis I: multi-valent repression. Proc Natl Acad Sci USA 481804–1808
     [Google Scholar]
  13. Gaal T., Barkei J., Dickson R. R., deBoer H. A., deHaseth P. L., Alavi H., Gourse R. L. 1989; Saturation mutagenesis of an Escherichia coli rRNA promoter and initial characterization of promoter variants. J Bacteriol 171:4852–4861
     [Google Scholar]
  14. Gallant J., Harada B. 1969; The control of RNA synthesis in Escherichia coli III: the functional relationship between purine nucleoside triphosphate pool sizes and the rate of ribonucleic acid accumulation. J Biol Chem 244:3125–3132
     [Google Scholar]
  15. Gallant J., Ehrlich H., Hall B., Laffler T. 1970; Analysis of the RC function. Cold Spring Harbor Symp Quant Biol 35:397–405
     [Google Scholar]
  16. Gallant J., Irr J., Cashel M. 1971; The mechanism of amino acid control of guanvlate and adenylate biosynthesis. J Biol Chem 246:5812–5816
     [Google Scholar]
  17. Gilbert H. J., Drabble W. T. 1980; Complementation in vitro between guaB mutants of Escherichia coli K-12. J Gen Microbiol 117:33–45
     [Google Scholar]
  18. Gourse R. L., deBoer H. A., Nomura M. 1986; DNA determinants ol rRNA synthesis in E. coli: growth rate dependent regulation, feedback inhibition, upstream activation, antitermination. Cell 44:197–205
     [Google Scholar]
  19. He B., Shiau A., Choi K. Y., Zalkin H., Smith J. M. 1990; Genes of the Escherichia coli pur regulon are negatively controlled by a repressor-operator interaction. J Bacteriol 172:4555–4562
     [Google Scholar]
  20. Jennings M. P., Beacham I. R. 1993; Co-dependent positive regulation of the asnB promoter of Escherichia coli by CRP and the FNR protein: a molecular analysis. Mol Microbiol 9:155–164
     [Google Scholar]
  21. Kelln R. A., Neuhard J. 1988; Regulation of pyrC expression in Salmonella lyphimurium: identification of a regulatory region. Mol Gen Genet 212:287–294
     [Google Scholar]
  22. Kolb A., Busby S., Buc H., Garges S., Adhya S. 1993; Transcriptional regulation by cAMP and its receptor protein. Annu Rev Biochem 62:749–795
     [Google Scholar]
  23. Lamond A. I., Travers A. A. 1985; Genetically separable iunctional elements mediate the optimal expression and stringent regulation of a bacterial rRNA gene. Cell 40:319–326
     [Google Scholar]
  24. Lindhal L., Zengel J. M. 1986; Ribosomal genes in Escherichia coli . Annu Rev Genet 20:297–326
     [Google Scholar]
  25. Makaroff C. A., Zalkin H. 1985; Regulation of Escherichia coli purF: analysis of the control region of a pur regulon gene. J Biol Chem 260:10378–10387
     [Google Scholar]
  26. Mehra R. K., Drabble W. T. 1981; Dual control of the gua operon of Escherichia coli K12 by adenine and guanine nucleotides. J Gen Microbiol 123:27–37
     [Google Scholar]
  27. Meng L. M., Kilstrup M., Nygaard P. 1990; Autoregulation of PurR repressor synthesis and involvement of purR in the regulation of purB, purC, purL, purMN and guaB A expression in Escherichia coli . Eur J Biochem 187:373–379
     [Google Scholar]
  28. Miller J. H. 1972 Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  29. Miura A., Krueger J. H., Itoh S., deBoer H. A., Nomura M. 1981; Growth-rate-dependent regulation of ribosome biosynthesis in Escherichia coli: expression of the lacZ and galK genes fused to ribosomal promoters. Cell 25:773–782
     [Google Scholar]
  30. Neidhardt F. C. 1987; Chemical composition of Escherichia coli . In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology pp. 3–6 Edited by Neidhardt F. C., Ingraham J. L., Brooks Low K., Magasanik B., Schaechter M., Umbarger H. E. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  31. Pao C. C., Dyess B. T. 1981; Effect of unusual guanosine nucleotides on the activities of some Escherichia coli cellular enzymes. Biochim Biophys Acta 677:358–362
     [Google Scholar]
  32. Piette J., Nyunoya H., Lusty C. J., Cunin R., Weyens G., Crabeel M., Charlier D., Glansdorff N., Piérard A. 1984; DNA sequence of the car A gene and the control region of carAB: tandem promoters, respectively controlled by arginine and the pyrimidines, regulate the synthesis of carbamoyl phosphate synthetase in Escherichia coli K-12. Proc Natl Acad Sci USA 814134–4138
     [Google Scholar]
  33. Rosenberg S. M., Stahl M. M., Kobayashi I., Stahl F. W. 1985; Improved in vitro packaging of coliphage lambda DNA: a one-strain system free from endogenous phage. Gene 38:165–175
     [Google Scholar]
  34. Ross W., Gosink K. K., Solomon J., Igarashi K., Zou C., Ishihama A., Severinov K., Gourse R. L. 1993; A third recognition element in bacterial promoters: DNA binding by the α subunit of RNA polymerase. Science 262:1407–1413
     [Google Scholar]
  35. Schumacher M. A., Choi K. Y., Zalkin H., Brennan R. G. 1994; Crystal structure of LacI member, PurR, bound to DNA: minor groove binding by α helices. Science 266:763–770
     [Google Scholar]
  36. Smith P. K., Krohn R. I., Hermansen G. T., Mallia A. K., Gartner F. H., Provenzano M. D., Fujimoto E. K., Goeke M. N., Olson B. J., Klenc D. C. 1985; Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85
     [Google Scholar]
  37. Spibey N., Drabble W. T. 1981; Construction and characterization of guaB-lacZ fusions in Escherichia coli K12. J Gen Microbiol 126:497–501
     [Google Scholar]
  38. Summers W. C. 1970; A simple method for extracting RNA from Escherichia coli utilizing diethylpyrocarbonate. Anal Biochem 33:459–463
     [Google Scholar]
  39. Teideman A. A., Smith J. M. 1985; Nucleotide sequence of the guaB locus encoding IMP dehydrogenase of Escherichia coli K12. Nucleic Acids Res 13:1303–1316
     [Google Scholar]
  40. Tesfa-Selase F., Drabble W. T. 1992; Regulation of the gua operon of Escherichia coli by the DnaA protein. Mol Gen Genet 231:256–264
     [Google Scholar]
  41. Thomas M. S., Drabble W. T. 1984; Molecular cloning and characterisation of the gua regulatory region of Escherichia coli K12. Mol Gen Genet 195:238–245
     [Google Scholar]
  42. Thomas M. S., Drabble W. T. 1985; Nucleotide sequence and organisation of the gua promoter region of Escherichia coli . Gene 36:45–53
     [Google Scholar]
  43. Travers A. A., Lamond A. I., Weeks J. R. 1986; Alteration of the growth-rate-dependent regulation of Escherichia coli tyrT expression by promoter mutations. J Mol Biol 189:251–255
     [Google Scholar]
  44. Tuerk C., Gauss P., Thermes C., Groebe D. R., Gayle M., Guild N., Stormo G., D´Aubenton-Carafa Y., Uhlenbeck O. C., Tinoco I. Jr Brody E. N., Gold L. 1988; CUUCGG hairpins: extraordinarily stable secondary structures associated with various biochemical processes. Proc Natl Acad Sci USA 851364–1368
     [Google Scholar]
  45. Turnbough C. L. Jr 1983; Regulation of Escherichia coli aspartate transcarbamylase synthesis by guanosine tetraphosphate and pyrimidine ribonucleoside triphosphates. J Bacterial 153:998–1007
     [Google Scholar]
  46. Vogel H. J., Bonner D. M. 1956; Acetylornithase of Escherichia coli partial purification and some properties. J Biol Chem 218:96–106
     [Google Scholar]
  47. Wilson H. R., Chan P. T., Turnbough C. L. Jr 1987; Nucleotide sequence and expression of the pyrC gene of Escherichia coli K-12. J Bacterial 169:3051–3058
     [Google Scholar]
  48. Yanisch-Perron C., Vieira J., Messing J. 1985; Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mpl8 and pUC19 vectors. Gene 33:103–119
     [Google Scholar]
  49. Zacharias M., Gtiringer H. U., Wagner R. 1990; The signal for growth rate control in E. coli is not restricted to a particular sequence motif within the promoter region. Nucleic Acids Res 18:6271–6275
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-142-9-2429
Loading
Stringent and growth-rate-dependent control of the gua operon of Escherichia coli K-12
Microbiology 142, 2429 (1996); https://doi.org/10.1099/00221287-142-9-2429
/content/journal/micro/10.1099/00221287-142-9-2429
/content/journal/micro/10.1099/00221287-142-9-2429
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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