1887

Abstract

Analysis of the response to arginine of the K-12 transcriptome by microarray hybridization and real-time quantitative PCR provides the first coherent quantitative picture of the ArgR-mediated repression of arginine biosynthesis and uptake genes. Transcriptional repression was shown to be the major control mechanism of the biosynthetic genes, leaving only limited room for additional transcriptional or post-transcriptional regulation. The genes, encoding the specific arginine uptake system, are subject to ArgR-mediated repression, with strong repression of , encoding the periplasmic binding protein of the system. The genes of the histidine transporter (part of the lysine-arginine-ornithine uptake system) were discovered to be a part of the arginine regulon. Analysis of their control region with reporter gene fusions and electrophoretic mobility shift in the presence of pure ArgR repressor showed the involvement in repression of the ArgR protein and an ARG box 120 bp upstream of . No repression of the genes of the third uptake system, arginine-ornithine, was observed. Finally, comparison of the time course of arginine repression of gene transcription with the evolution of the specific activities of the cognate enzymes showed that while full genetic repression was achieved 2 min after arginine addition, enzyme concentrations were diluted at the rate of cell division. This emphasizes the importance of feedback inhibition of the first enzymic step in the pathway in controlling the metabolic flow through biosynthesis in the period following the onset of repression.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.29088-0
2006-11-01
2019-11-18
Loading full text...

Full text loading...

/deliver/fulltext/micro/152/11/3343.html?itemId=/content/journal/micro/10.1099/mic.0.29088-0&mimeType=html&fmt=ahah

References

  1. Abadjieva, A., Pauwels, K., Hilven, P. & Crabeel, M. ( 2001; ). A new yeast metabolon involving at least the two first enzymes of arginine biosynthesis: acetylglutamate synthase activity requires complex formation with acetylglutamate kinase. J Biol Chem 276, 42869–42880.[CrossRef]
    [Google Scholar]
  2. Ames, G. F. ( 1986; ). Bacterial periplasmic transport systems: structure, mechanism, and evolution. Annu Rev Biochem 55, 397–425.[CrossRef]
    [Google Scholar]
  3. Bachmann, B. J. ( 1987; ). Derivations and genotypes of some mutant derivatives of Escherichia coli K-12. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn, pp. 1190 – 1224. Edited by F. C. Neidhardt and others. Washington, DC: American Society for Microbiology.
  4. Benjamini, Y. & Hochberg, Y. ( 1995; ). Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57, 289–300.
    [Google Scholar]
  5. Beny, G., Cunin, R., Glansdorff, N., Boyen, A., Charlier, J. & Kelker, N. ( 1982; ). Transcription of regions within the divergent argECBH operon of Escherichia coli: evidence for lack of an attenuation mechanism. J Bacteriol 151, 58–61.
    [Google Scholar]
  6. Braxton, B. L., Mullins, L. S., Raushel, F. M. & Reinhart, G. D. ( 1992; ). Quantifying the allosteric properties of Escherichia coli carbamyl phosphate synthetase: determination of thermodynamic linked-function parameters in an ordered kinetic mechanism. Biochemistry 31, 2309–2316.[CrossRef]
    [Google Scholar]
  7. Caldara, M., Verbrugghe, K., De Vuyst, L., Crabeel, M., Dupont, G., Goldbeter, A. & Cunin, R. ( 2005; ). Experimental manipulation and mathematical modelling of arginine biosynthesis in Escherichia coli. Abstract in Systems Biology: From Molecules & Modelling to Cells (FEBS Course, Gosau, Austria), p. 145.
  8. Celis, R. T. ( 1999; ). Repression and activation of arginine transport genes in Escherichia coli K-12 by the ArgP protein. J Mol Biol 294, 1087–1095.[CrossRef]
    [Google Scholar]
  9. Celis, R. T., Leadlay, P. F., Roy, I. & Hansen, A. ( 1998; ). Phosphorylation of the periplasmic binding protein in two transport systems for arginine incorporation in Escherichia coli K-12 is unrelated to the function of the transport system. J Bacteriol 180, 4828–4833.
    [Google Scholar]
  10. Celis, T. F. ( 1977a; ). Independent regulation of transport and biosynthesis of arginine in Escherichia coli K-12. J Bacteriol 130, 1244–1252.
    [Google Scholar]
  11. Celis, T. F. ( 1977b; ). Properties of an Escherichia coli K-12 mutant defective in the transport of arginine and ornithine. J Bacteriol 130, 1234–1243.
    [Google Scholar]
  12. Celis, T. F., Rosenfeld, H. J. & Maas, W. K. ( 1973; ). Mutant of Escherichia coli K-12 defective in the transport of basic amino acids. J Bacteriol 116, 619–626.
    [Google Scholar]
  13. Charlier, D. ( 2004; ). Arginine regulation in Thermotoga neapolitana and Thermotoga maritima. Biochem Soc Trans 32, 310–313.[CrossRef]
    [Google Scholar]
  14. Charlier, D. & Glansdorff, N. ( 2004; ). Biosynthesis of arginine and polyamines. In EcoSal (www.ecosal.org), Section 3.6.1.10. Edited by R. Curtiss III. Washington, DC: American Society for Microbiology.
  15. Charlier, D., Roovers, M., Van Vliet, F., Boyen, A., Cunin, R., Nakamura, Y., Glansdorff, N. & Pierard, A. ( 1992; ). Arginine regulon of Escherichia coli K-12. A study of repressor-operator interactions and of in vitro binding affinities versus in vivo repression. J Mol Biol 226, 367–386.[CrossRef]
    [Google Scholar]
  16. Cunin, R., Eckhardt, T., Piette, J., Boyen, A., Pierard, A. & Glansdorff, N. ( 1983; ). Molecular basis for modulated regulation of gene expression in the arginine regulon of Escherichia coli K-12. Nucleic Acids Res 11, 5007–5019.[CrossRef]
    [Google Scholar]
  17. Cunin, R., Glansdorff, N., Pierard, A. & Stalon, V. ( 1986; ). Biosynthesis and metabolism of arginine in bacteria. Microbiol Rev 50, 314–352.
    [Google Scholar]
  18. Datsenko, K. A. & Wanner, B. L. ( 2000; ). One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97, 6640–6645.[CrossRef]
    [Google Scholar]
  19. Devroede, N., Thia-Toong, T. L., Gigot, D., Maes, D. & Charlier, D. ( 2004; ). Purine and pyrimidine-specific repression of the Escherichia coli carAB operon are functionally and structurally coupled. J Mol Biol 336, 25–42.[CrossRef]
    [Google Scholar]
  20. Fried, M. G. & Crothers, D. M. ( 1983; ). CAP and RNA polymerase interaction with lac promoter: binding stoichiometry and long range effects. Nucleic Acids Res 11, 141–158.[CrossRef]
    [Google Scholar]
  21. Gallant, J. A. ( 1979; ). Stringent control in E. coli. Annu Rev Genet 13, 393–415.[CrossRef]
    [Google Scholar]
  22. Gentleman, C. G., Carey, V. J., Bates, D. M., Bolstad, B., Dettling, M., Dudoit, S. & 19 other authors ( 2004; ). Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5, R80.[CrossRef]
    [Google Scholar]
  23. Glansdorff, N. ( 1965; ). Topography of cotransducible arginine mutations in Escherichia coli K-12. Genetics 51, 167–179.
    [Google Scholar]
  24. Glansdorff, N. & Sand, G. ( 1965; ). Coordination of enzyme synthesis in the arginine pathway of Escherichia coli K-12. Biochim Biophys Acta 108, 308–311.[CrossRef]
    [Google Scholar]
  25. Irizarry, R. A., Hobbs, B., Collin, F., Beazer-Barclay, Y. D., Antonellis, K. J., Scherf, U. & Speed, T. P. ( 2003; ). Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249–264.[CrossRef]
    [Google Scholar]
  26. Jishage, M., Iwata, A., Ueda, S. & Ishihama, A. ( 1996; ). Regulation of RNA polymerase sigma subunit synthesis in Escherichia coli: intracellular levels of four species of sigma under various growth conditions. J Bacteriol 178, 5447–5451.
    [Google Scholar]
  27. Kelker, N. & Eckhardt, T. ( 1977; ). Regulation of argA operon expression in Escherichia coli K-12: cell-free synthesis of β-galactosidase under argA control. J Bacteriol 132, 67–72.
    [Google Scholar]
  28. Kiupakis, A. K. & Reitzer, L. ( 2002; ). ArgR-independent induction and ArgR-dependent superinduction of the astCADBE operon in Escherichia coli. J Bacteriol 184, 2940–2950.[CrossRef]
    [Google Scholar]
  29. Krin, E., Laurent-Winter, C., Bertin, P. N., Danchin, A. & Kolb, A. ( 2003; ). Transcription regulation coupling of the divergent argG and metY promoters in Escherichia coli K-12. J Bacteriol 185, 3139–3146.[CrossRef]
    [Google Scholar]
  30. Kustu, S. G. & Ames, G. F. ( 1973; ). The HisP protein, a known histidine transport component in Salmonella typhimurium, is also an arginine transport component. J Bacteriol 116, 107–113.
    [Google Scholar]
  31. Kustu, S. G., McFarland, N. C., Hui, S. P., Esmon, B. & Ames, G. F. ( 1979; ). Nitrogen control of Salmonella typhimurium: co-regulation of synthesis of glutamine synthetase and amino acid transport systems. J Bacteriol 138, 218–234.
    [Google Scholar]
  32. Liu, P. Q. & Ames, G. F. ( 1998; ). In vitro disassembly and reassembly of an ABC transporter, the histidine permease. Proc Natl Acad Sci U S A 95, 3495–3500.[CrossRef]
    [Google Scholar]
  33. Lu, C.-D. ( 2006; ). Pathways and regulation of bacterial arginine metabolism and perspectives for obtaining arginine overproducing strains. Appl Microbiol Biotechnol 70, 261–272.[CrossRef]
    [Google Scholar]
  34. Maas, W. K. & Clark, A. J. ( 1964; ). Studies on the mechanism of repression or arginine biosynthesis in Escherichia coli. II. Dominance of repressibility in diploids. J Mol Biol 8, 365–370.[CrossRef]
    [Google Scholar]
  35. Makarova, K. S., Mironov, A. A. & Gelfand, M. S. ( 2001; ). Conservation of the binding site for the arginine repressor in all bacterial lineages. Genome Biol 2, 1–8.
    [Google Scholar]
  36. Marvil, D. K. & Leisinger, T. ( 1977; ). N-Acetylglutamate synthase of Escherichia coli: purification, characterization, and molecular properties. J Biol Chem 252, 3295–3303.
    [Google Scholar]
  37. Miller, H. J. ( 1972; ). Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  38. Nandineni, M. R. & Gowrishankar, J. ( 2004; ). Evidence for an arginine exporter encoded by yggA (argO) that is regulated by the LysR-type transcriptional regulator ArgP in Escherichia coli. J Bacteriol 186, 3539–3546.[CrossRef]
    [Google Scholar]
  39. Piérard, A., Glansdorff, N., Mergeay, M. & Wiame, J. M. ( 1965; ). Control of the biosynthesis of carbamoyl phosphate in Escherichia coli. J Mol Biol 14, 23–36.[CrossRef]
    [Google Scholar]
  40. Piette, J., Nyunoya, H., Lusty, C. J., Cunin, R., Weyens, G., Crabeel, M., Charlier, D., Glansdorff, N. & Pierard, A. ( 1984; ). DNA sequence of the carA 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 U S A 81, 4134–4138.[CrossRef]
    [Google Scholar]
  41. Reitzer, L. J. ( 1996; ). Sources of nitrogen and their utilization. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn, pp. 380–390. Edited by F. C. Neidhardt and others. Washington, DC: American Society for Microbiology.
  42. Robin, J. P., Penverne, B. & Hervé, G. ( 1989; ). Carbamoyl phosphate biosynthesis and partition in pyrimidine and arginine pathways of Escherichia coli. In situ properties of carbamoyl-phosphate synthase, ornithine transcarbamylase and aspartate transcarbamylase in permeabilized cells. Eur J Biochem 183, 519–528.[CrossRef]
    [Google Scholar]
  43. Rosen, B. P. ( 1971; ). Basic amino acid transport in Escherichia coli. J Biol Chem 246, 3653–3662.
    [Google Scholar]
  44. Rosen, B. P. ( 1973; ). Basic amino acid transport in Escherichia coli: properties of canavanine-resistant mutants. J Bacteriol 116, 627–635.
    [Google Scholar]
  45. Simmons, A. J., Rauwls, J. M., Piskur, J. & Davidson, J. N. ( 1999; ). A mutation that uncouples allosteric regulation of carbamyl phosphate synthetase in Drosophila. J Mol Biol 287, 277–285.[CrossRef]
    [Google Scholar]
  46. Whipple, F. W. ( 1998; ). Genetic analysis of prokaryotic and eukaryotic DNA-binding proteins in Escherichia coli. Nucleic Acids Res 26, 3700–3706.[CrossRef]
    [Google Scholar]
  47. Wissenbach, U., Keck, B. & Unden, G. ( 1993; ). Physical map location of the new artPIQMJ genes of Escherichia coli, encoding a periplasmic arginine transport system. J Bacteriol 175, 3687–3688.
    [Google Scholar]
  48. Wissenbach, U., Six, S., Bongaerts, J., Ternes, D., Steinwachs, S. & Unden, G. ( 1995; ). A third periplasmic transport system for l-arginine in Escherichia coli: molecular characterization of the artPIQMJ genes, arginine binding and transport. Mol Microbiol 17, 675–686.[CrossRef]
    [Google Scholar]
  49. Xu, Y., Sun, Y., Huysveld, N., Gigot, D., Glansdorff, N. & Charlier, D. ( 2003; ). Regulation of arginine biosynthesis in the psychropiezophilic bacterium Moritella profunda: in vivo repressibility and in vitro repressor-operator contact probing. J Mol Biol 326, 353–369.[CrossRef]
    [Google Scholar]
  50. Zidwick, M. J., Korshus, J. & Rogers, P. ( 1984; ). Positive control of expression of the argECBH gene cluster in vivo by 5′-diphosphate 3′-diphosphate. J Bacteriol 159, 647–651.
    [Google Scholar]
  51. Zimmer, D. P., Soupene, E., Lee, H. L., Wendisch, V. F., Khodursky, A. B., Peter, B. J., Bender, R. A. & Kustu, S. ( 2000; ). Nitrogen regulatory protein C-controlled genes of Escherichia coli: scavenging as a defense against nitrogen limitation. Proc Natl Acad Sci U S A 97, 14674–14679.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.29088-0
Loading
/content/journal/micro/10.1099/mic.0.29088-0
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