1887

Abstract

The expression of the genes involved in the degradation of the aromatic compound 3-(3-hydroxyphenyl)propionic acid (3HPP) in is dependent on the MhpR transcriptional activator at the promoter. This catabolic promoter is also subject to catabolic repression in the presence of glucose mediated by the cAMP–CRP complex. The promoter drives the MhpR-independent expression of the regulatory gene. and experiments have shown that transcription from the promoter is downregulated by the addition of glucose and this catabolic repression is also mediated by the cAMP–CRP complex. The activation role of the cAMP–CRP regulatory system was further investigated by DNase I footprinting assays, which showed that the cAMP–CRP complex binds to the promoter sequence, protecting a region centred at position −40.5, which allowed the classification of as a class II CRP-dependent promoter. Open complex formation at the promoter is observed only when RNA polymerase and cAMP–CRP are present. Finally, by transcription assays we have demonstrated the absolute requirement of the cAMP–CRP complex for the activation of the promoter.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.043620-0
2011-02-01
2024-04-16
Loading full text...

Full text loading...

/deliver/fulltext/micro/157/2/593.html?itemId=/content/journal/micro/10.1099/mic.0.043620-0&mimeType=html&fmt=ahah

References

  1. Belyaeva T. A., Wade J. T., Webster C. L., Howard V. J., Thomas M. S., Hyde E. I., Busby S. J. W. 2000; Transcription activation at the Escherichia coli melAB promoter: the role of MelR and the cyclic AMP receptor protein. Mol Microbiol 36:211–222
    [Google Scholar]
  2. Bordes P., Repolla F., Kolb A., Gutierrez C. 2000; Involvement of differential efficiency of transcription by E σ S and E σ 70 RNA polymerase holoenzymes in growth phase regulation of the Escherichia coli osmE promoter. Mol Microbiol 35:845–853
    [Google Scholar]
  3. Busby S., Ebright R. H. 1997; Transcription activation at Class II CAP-dependent promoters. Mol Microbiol 23:853–859
    [Google Scholar]
  4. Busby S., Ebright R. H. 1999; Transcription activation by catabolite activator protein (CAP. J Mol Biol 293:199–213
    [Google Scholar]
  5. Chapon C., Kolb A. 1983; Action of CAP on the malT promoter in vitro. J Bacteriol 156:1135–1143
    [Google Scholar]
  6. Dal S., Steiner I., Gerischer U. 2002; Multiple operons connected with catabolism of aromatic compounds in Acinetobacter sp. strain ADP1 are under carbon catabolite repression. J Mol Microbiol Biotechnol 4:389–404
    [Google Scholar]
  7. de Crombrugghe B., Busby S., Buc H. 1984; Cyclic AMP receptor protein: role in transcription activation. Science 224:831–838
    [Google Scholar]
  8. DiMarco A. A., Ornston L. N. 1994; Regulation of p -hydroxybenzoate hydroxylase synthesis by PobR bound to an operator in Acinetobacter calcoaceticus . J Bacteriol 176:4277–4284
    [Google Scholar]
  9. Ferrández A., García J. L., Díaz E. 1997; Genetic characterization and expression in heterologous hosts of the 3-(3-hydroxyphenyl) propionate catabolic pathway of Escherichia coli K-12. J Bacteriol 179:2573–2581
    [Google Scholar]
  10. Ferrández A., García J. L., Díaz E. 2000; Transcriptional regulation of the divergent paa catabolic operons for phenylacetic acid degradation in Escherichia coli . J Biol Chem 275:12214–12222
    [Google Scholar]
  11. Galán B., Kolb A., García J. L., Prieto M. A. 2001; Superimposed levels of regulation of the 4-hydroxyphenylacetate catabolic pathway in Escherichia coli . J Biol Chem 276:37060–37068
    [Google Scholar]
  12. Galán B., Manso I., Kolb A., García J. L., Prieto M. A. 2008; The role of FIS protein in the physiological control of the expression of the Escherichia coli meta-hpa operon. Microbiology 154:2151–2160
    [Google Scholar]
  13. Gerischer U., Segura A., Ornston L. N. 1998; PcaU, a transcriptional activator of genes for protocatechuate utilization in Acinetobacter . J Bacteriol 180:1512–1524
    [Google Scholar]
  14. Ghosaini L. R., Brown A. M., Sturtevant J. M. 1988; Scanning calorimetric study of the thermal unfolding of catabolite activator protein from Escherichia coli in the absence and presence of cyclic mononucleotides. Biochemistry 27:5257–5261
    [Google Scholar]
  15. Gulati A., Mahadevan S. 2000; Mechanism of catabolite repression in the bgl operon of Escherichia coli : involvement of the anti-terminator BglG, CRP-cAMP and EIIAGlc in mediating glucose effect downstream of transcription initiation. Genes Cells 5:239–250
    [Google Scholar]
  16. Guo Z., Houghton J. E. 1999; PcaR-mediated activation and repression of pca genes from Pseudomonas putida are propagated by its binding to both the −35 and the −10 promoter elements. Mol Microbiol 32:253–263
    [Google Scholar]
  17. Holcroft C. C., Egan S. M. 2000; Roles of cyclic AMP receptor protein and the carboxyl-terminal domain of the α subunit in transcription activation of the Escherichia coli rhaBAD operon. J Bacteriol 182:3529–3535
    [Google Scholar]
  18. Kallipolitis B. H., Valentin-Hansen P. 1998; Transcription of rpoH, encoding the Escherichia coli heat-shock regulator σ 32, is negatively controlled by the cAMP–CRP/CytR nucleoprotein complex. Mol Microbiol 29:1091–1099
    [Google Scholar]
  19. 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]
  20. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
    [Google Scholar]
  21. Lavigne M., Kolb A., Buc H. 1992; Transcription activation by cAMP receptor protein (CRP) at the Escherichia coli gal P1 promoter. Crucial role for the spacing between the CRP binding site and the −10 region. Biochemistry 31:9647–9656
    [Google Scholar]
  22. Lee S. K., Newman J., Keasling J. 2005; Catabolic repression of the propionate catabolic genes in Escherichia coli and Salmonella enterica : evidence for involvement of the cyclic AMP receptor protein. J Bacteriol 187:2793–2800
    [Google Scholar]
  23. Manso I., Torres B., Andreu J. M., Menéndez M., Rivas G., Alfonso C., Díaz E., García J. L., Galán B. 2009; 3-Hydroxyphenylpropionate and phenylpropionate are synergistic activators of the MhpR transcriptional regulator from Escherichia coli . J Biol Chem 284:21218–21228
    [Google Scholar]
  24. Marqués S., Manzanera M., Gónzalez-Pérez M. M., Gallegos M. T., Ramos J. L. 1999; The XylS-dependent Pm promoter is transcribed in vivo by RNA polymerase with sigma 32 or sigma 38 depending on the growth phase. Mol Microbiol 31:1105–1113
    [Google Scholar]
  25. Marschall C., Labrousse V., Kreimer M., Weichart D., Kolb A., Hengge-Aronis R. 1998; Molecular analysis of the regulation of csiD , a carbon starvation-inducible gene in Escherichia coli that is exclusively dependent on σ s and requires activation by cAMP–CRP. J Mol Biol 276:339–353
    [Google Scholar]
  26. Martín A. C., López R., García P. 1996; Analysis of the complete nucleotide sequence and functional organization of the genome of Streptococcus pneumoniae bacteriophage Cp-1. J Virol 70:3678–3687
    [Google Scholar]
  27. Maxam A. M., Gilbert W. 1977; A new method for sequencing DNA. Proc Natl Acad Sci U S A 74:560–564
    [Google Scholar]
  28. Miller J. H. 1972 Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  29. Nasser W., Schneider R., Travers A., Muskhelishvili G. 2001; CRP modulates fis transcription by alternate formation of activating and repressing nucleoprotein complexes. J Biol Chem 276:17878–17886
    [Google Scholar]
  30. Plumbridge J. 1998; Control of the expression of the manXYZ operon in Escherichia coli : Mlc is a negative regulator of the mannose PTS. Mol Microbiol 27:369–380
    [Google Scholar]
  31. Prieto M. A., García J. L. 1997; Identification of a novel positive regulator of the 4-hydroxyphenylacetate catabolic pathway of Escherichia coli . Biochem Biophys Res Commun 232:759–765
    [Google Scholar]
  32. Richet E. 2000; Synergistic transcription activation: a dual role for CRP in the activation of an Escherichia coli promoter depending on MalT and CRP. EMBO J 19:5222–5232
    [Google Scholar]
  33. Richet E., Sogaard-Andersen L. 1994; CRP induces the repositioning of MalT at the Escherichia coli malKp promoter primarily through DNA bending. EMBO J 13:4558–4567
    [Google Scholar]
  34. Saier M. H., Ramseier T. M., Reizer J. 1996; In Escherichia coli and Salmonella: Cellular and Molecular Biology. pp 1325–1343 Edited by Neidhardt F. C., Curtiss R. III, Ingraham J. L., Lin E. C. C., Low K. B., Magasanik B., Reznikoff W. S., Riley M., Schaechter M., Umbarger H. E. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  35. Samarasinghe S., Samir M., El-Robh M. S., Grainger D. C., Zhang W., Soultanas P., Busby S. J. W. 2008; Autoregulation of the Escherichia coli melR promoter: repression involves four molecules of MelR. Nucleic Acids Res 36:2667–2676
    [Google Scholar]
  36. Sambrook J., Russell D. W. 2001 Molecular Cloning: a Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  37. Sasse-Dwight S., Gralla J. D. 1989; KMnO4 as a probe for lac promoter DNA melting and mechanism in vivo . J Biol Chem 264:8074–8081
    [Google Scholar]
  38. Savery N., Belyaeva T., Busby S. 1996; Introduction to protein : DNA interactions, DNase I footprinting, hydroxyl radical footprinting, permanganate footprinting and supplementary protocols. In Essential Techniques: Gene Transcription pp. 1–521–33 Edited by Docherty K. Oxford: BIOS Scientific Publishers;
    [Google Scholar]
  39. Siehler S. Y., Dal S., Fischer R., Patz P., Gerischer U. 2007; Multiple-level regulation of genes for protocatechuate degradation in Acinetobacter baylyi includes cross-regulation. Appl Environ Microbiol 73:232–242
    [Google Scholar]
  40. Tobin J. F., Schleif R. F. 1990a; Transcription from the rha operon psr promoter. J Mol Biol 211:1–4
    [Google Scholar]
  41. Tobin J. F., Schleif R. F. 1990b; Purification and properties of RhaR, the positive regulator of the l-rhamnose operons of Escherichia coli . J Mol Biol 211:75–89
    [Google Scholar]
  42. Torres B., Porras G., García J. L., Díaz E. 2003; Regulation of the mhp cluster responsible for 3-(3-hydroxyphenyl)propionic acid degradation in Escherichia coli . J Biol Chem 278:27575–27585
    [Google Scholar]
  43. Trautwein G., Gerischer U. 2001; Effects exerted by transcriptional regulator PcaU from Acinetobacter sp. strain ADP1. J Bacteriol 183:873–881
    [Google Scholar]
  44. Turlin E., Perrotte-piquemal M., Danchin A., Biville F. 2001; Regulation of the early steps of 3-phenylpropionate catabolism in Escherichia coli . J Mol Microbiol Biotechnol 3:127–133
    [Google Scholar]
  45. Weber I. T., Steitz T. 1984; Model of specific complex between catabolite gene activator protein and B-DNA suggested by electrostatic complementarity. Proc Natl Acad Sci U S A 81:3973–3977
    [Google Scholar]
  46. Webster C., Gaston K., Busby S. 1988; Transcription from the Escherichia coli melR promoter is dependent on the cyclic AMP receptor protein. Gene 68:297–305
    [Google Scholar]
  47. Weickert M. J., Adhya S. 1993; Control of transcription of gal repressor and isorepressor genes in Escherichia coli . J Bacteriol 175:251–258
    [Google Scholar]
  48. Wickstrum J. R., Santangelo T. J., Egan S. M. 2005; Cyclic AMP receptor protein and RhaR synergistically activate transcription from the l-rhamnose-responsive rhaSR promoter in Escherichia coli . J Bacteriol 187:6708–6718
    [Google Scholar]
  49. Yamashita M., Azakami H., Yokoro N., Roh J. H., Suzuki H., Kumagai H., Murooka Y. 1996; maoB , a gene that encodes a positive regulator of the monoamine oxidase gene ( maoA ) in Escherichia coli . J Bacteriol 178:2941–2947
    [Google Scholar]
  50. Zheng D., Constantinidou C., Hobman J. L., Minchin S. D. 2004; Identification of the CRP regulon using in vitro and in vivo transcriptional profiling. Nucleic Acids Res 32:5874–5893
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.043620-0
Loading
/content/journal/micro/10.1099/mic.0.043620-0
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