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. 1978 Feb;133(2):830–843. doi: 10.1128/jb.133.2.830-843.1978

Promoter- and attenuator-related metabolic regulation of the Salmonella typhimurium histidine operon.

M E Winkler, D J Roth, P E Hartman
PMCID: PMC222095  PMID: 342509

Abstract

Expression of the histidine (his) operon in Salmonella typhimurium was found to be positively correlated with the intracellular level of guanosine tetraphosphate (ppGpp). Limitation for amino acids other than histidine elicited a histidine-independent metabolic regulation of the operon. In bacteria grown at decreased growth rates, his operon expression was metabolically regulated up to a point, after which further decreases in growth rate no longer resulted in further enhancement of operon expression. Studies using strains carrying various regulatory and deletion mutations indicated that metabolic regulation is achieved predominantly by increased RNA chain initiations at the primary (P1) and internal (P2) promoters. Metabolic regulation ordinarly did not involve changes in RNA chain terminations at the attenuator site of the his operon. A model is proposed that involves ppGpp-induced changes in RNA polymerase initiation specificity at particular promoters. A second, special form of metabolic regulation may operate which also is histidine independent, but does involve relief of attenuation.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. AMES B. N., HARTMAN P. E., JACOB F. Chromosomal alterations affecting the regulation of histidine biosynthetic enzymes in Salmonella. J Mol Biol. 1963 Jul;7:23–42. doi: 10.1016/s0022-2836(63)80016-9. [DOI] [PubMed] [Google Scholar]
  2. Anderson R. P., Miller C. G., Roth J. R. Tandem duplications of the histidine operon observed following generalized transduction in Salmonella typhimurium. J Mol Biol. 1976 Aug 5;105(2):201–218. doi: 10.1016/0022-2836(76)90107-8. [DOI] [PubMed] [Google Scholar]
  3. Artz S. W., Broach J. R. Histidine regulation in Salmonella typhimurium: an activator attenuator model of gene regulation. Proc Natl Acad Sci U S A. 1975 Sep;72(9):3453–3457. doi: 10.1073/pnas.72.9.3453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bertrand K., Korn L., Lee F., Platt T., Squires C. L., Squires C., Yanofsky C. New features of the regulation of the tryptophan operon. Science. 1975 Jul 4;189(4196):22–26. doi: 10.1126/science.1094538. [DOI] [PubMed] [Google Scholar]
  5. Bertrand K., Yanofsky C. Regulation of transcription termination in the leader region of the tryptophan operon of Escherichia coli involves tryptophan or its metabolic product. J Mol Biol. 1976 May 15;103(2):339–349. doi: 10.1016/0022-2836(76)90316-8. [DOI] [PubMed] [Google Scholar]
  6. Boquet P. L., Devynck M. A., Monnier C., Fromageot P. Inhibition of stable RNA synthesis by levallorphan in Escherichia coli. Implication of compounds MS I and MS II. Eur J Biochem. 1973 Dec 3;40(1):31–42. doi: 10.1111/j.1432-1033.1973.tb03166.x. [DOI] [PubMed] [Google Scholar]
  7. Bruni C. B., Colantuoni V., Sbordone L., Cortese R., Blasi F. Biochemical and regulatory properties of Escherichia coli K-12 hisT mutants. J Bacteriol. 1977 Apr;130(1):4–10. doi: 10.1128/jb.130.1.4-10.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cashel M., Lazzarini R. A., Kalbacher B. An improved method for thin-layer chromatography of nucleotide mixtures containing 32P-labelled orthophosphate. J Chromatogr. 1969 Mar 11;40(1):103–109. doi: 10.1016/s0021-9673(01)96624-5. [DOI] [PubMed] [Google Scholar]
  9. Chang G. W., Roth J. R., Ames B. N. Histidine regulation in Salmonella typhimurium. 8. Mutations of the hisT gene. J Bacteriol. 1971 Oct;108(1):410–414. doi: 10.1128/jb.108.1.410-414.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cortese R., Kammen H. O., Spengler S. J., Ames B. N. Biosynthesis of pseudouridine in transfer ribonucleic acid. J Biol Chem. 1974 Feb 25;249(4):1103–1108. [PubMed] [Google Scholar]
  11. Ely B., Ciesla Z. Internal promoter P2 of the histidine operon of Salmonella typhimurium. J Bacteriol. 1974 Nov;120(2):984–986. doi: 10.1128/jb.120.2.984-986.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ely B., Fankhauser D. B., Hartman P. E. A fine structure map of the salmonella histidine operator-promoter. Genetics. 1974 Oct;78(2):607–631. doi: 10.1093/genetics/78.2.607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ely B. Physiological studies of salmonella histidine operator-promoter mutants. Genetics. 1974 Oct;78(2):593–606. doi: 10.1093/genetics/78.2.593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fink G. R., Klopotowski T., Ames B. N. Histidine regulatory mutants in Salmonella typhimurium. IV. A positive selection for polar histidine-requiring mutants from histidine operator constitutive mutants. J Mol Biol. 1967 Nov 28;30(1):81–95. doi: 10.1016/0022-2836(67)90245-8. [DOI] [PubMed] [Google Scholar]
  15. Fink G. R., Roth J. R. Histidine regulatory mutants in Salmonella typhiumium. VI. Dominance studies. J Mol Biol. 1968 May 14;33(3):547–557. doi: 10.1016/0022-2836(68)90305-7. [DOI] [PubMed] [Google Scholar]
  16. Goldberger R. F. Autogenous regulation of gene expression. Science. 1974 Mar 1;183(4127):810–816. doi: 10.1126/science.183.4127.810. [DOI] [PubMed] [Google Scholar]
  17. Hartman P. E. Some improved methods in P22 transduction. Genetics. 1974 Apr;76(4):625–631. doi: 10.1093/genetics/76.4.625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kaempfer R. O., Magasanik B. Effect of infection with T-even phage on the inducible synthesis of beta-glactosidase in Escherichia coli. J Mol Biol. 1967 Aug 14;27(3):453–468. doi: 10.1016/0022-2836(67)90051-4. [DOI] [PubMed] [Google Scholar]
  19. Kasai T. Regulation of the expression of the histidine operon in Salmonella typhimurium. Nature. 1974 Jun 7;249(457):523–527. doi: 10.1038/249523a0. [DOI] [PubMed] [Google Scholar]
  20. Korn L. J., Yanofsky C. Polarity suppressors increase expression of the wild-type tryptophan operon of Escherichia coli. J Mol Biol. 1976 May 15;103(2):395–409. doi: 10.1016/0022-2836(76)90319-3. [DOI] [PubMed] [Google Scholar]
  21. Lawther R. P., Hatfield W. Biochemical characterization of an Escherichia coli hisT strain. J Bacteriol. 1977 Apr;130(1):552–557. doi: 10.1128/jb.130.1.552-557.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lazzarini R. A., Cashel M., Gallant J. On the regulation of guanosine tetraphosphate levels in stringent and relaxed strains of Escherichia coli. J Biol Chem. 1971 Jul 25;246(14):4381–4385. [PubMed] [Google Scholar]
  23. Lewis J. A., Ames B. N. Histidine regulation in Salmonella typhimurium. XI. The percentage of transfer RNA His charged in vivo and its relation to the repression of the histidine operon. J Mol Biol. 1972 Apr 28;66(1):131–142. doi: 10.1016/s0022-2836(72)80011-1. [DOI] [PubMed] [Google Scholar]
  24. Martin R. G. Polarity in relaxed strains of Salmonella typhimurium. J Mol Biol. 1968 Jan 14;31(1):127–134. doi: 10.1016/0022-2836(68)90060-0. [DOI] [PubMed] [Google Scholar]
  25. Morse D. E., Morse A. N. Dual-control of the tryptophan operon is mediated by both tryptophanyl-tRNA synthetase and the repressor. J Mol Biol. 1976 May 15;103(2):209–226. doi: 10.1016/0022-2836(76)90310-7. [DOI] [PubMed] [Google Scholar]
  26. Morton D. P., Parsons S. M. Synergistic inhibition of ATP phosphoribosyltransferase by guanosine tetraphosphate and histidine. Biochem Biophys Res Commun. 1977 Jan 10;74(1):172–177. doi: 10.1016/0006-291x(77)91390-0. [DOI] [PubMed] [Google Scholar]
  27. Murray M. L., Klopotowski T. Genetic map position of the gluconate-6-phosphate dehydrogenase gene in Salmonella typhimurium. J Bacteriol. 1968 Apr;95(4):1279–1282. doi: 10.1128/jb.95.4.1279-1282.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Raué H. A., Gruber M. Control of RNA synthesis in Escherichia coli. IV. Effect of levallorphan on guanosine 3'-diphosphate 5'-diphosphate metabolism in spoT+ and spoT minus strains. Biochim Biophys Acta. 1974 Oct 28;366(3):279–287. [PubMed] [Google Scholar]
  29. Rose J. K., Yanofsky C. Metabolic regulation of the tryptophan operon of Escherichia coli: repressor-independent regulation of transcription initiation frequency. J Mol Biol. 1972 Aug 14;69(1):103–118. doi: 10.1016/0022-2836(72)90026-5. [DOI] [PubMed] [Google Scholar]
  30. Roth J. R., Antón D. N., Hartman P. E. Histidine regulatory mutants in Salmonella typhimurium. I. Isolation and general properties. J Mol Biol. 1966 Dec 28;22(2):305–323. doi: 10.1016/0022-2836(66)90134-3. [DOI] [PubMed] [Google Scholar]
  31. Scott J. F., Roth J. R., Artz S. W. Regulation of histidine operon does not require hisG enzyme. Proc Natl Acad Sci U S A. 1975 Dec;72(12):5021–5025. doi: 10.1073/pnas.72.12.5021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Singer C. E., Smith G. R., Cortese R., Ames B. N. [Mutant tRNA His ineffective in repression and lacking two pseudouridine modifications]. Nat New Biol. 1972 Jul 19;238(81):72–74. doi: 10.1038/newbio238072a0. [DOI] [PubMed] [Google Scholar]
  33. Sokawa Y., Sokawa J., Kaziro Y. Regulation of stable RNA synthesis and ppGpp levels in growing cells of Escherichia coli. Cell. 1975 May;5(1):69–74. doi: 10.1016/0092-8674(75)90093-8. [DOI] [PubMed] [Google Scholar]
  34. St Pierre M. L. Mutations creating a new initiation point for expression of the histidine operon in Salmonella typhimurium. J Mol Biol. 1968 Jul 14;35(1):71–82. doi: 10.1016/s0022-2836(68)80037-3. [DOI] [PubMed] [Google Scholar]
  35. Stephens J. C., Artz S. W., Ames B. N. Guanosine 5'-diphosphate 3'-diphosphate (ppGpp): positive effector for histidine operon transcription and general signal for amino-acid deficiency. Proc Natl Acad Sci U S A. 1975 Nov;72(11):4389–4393. doi: 10.1073/pnas.72.11.4389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Straus D. S. Selection for a large genetic duplication in Salmonella typhimurium. Genetics. 1975 Jun;80(2):227–237. doi: 10.1093/genetics/80.2.227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Travers A. Modulation of RNA polymerase specificity by ppGpp. Mol Gen Genet. 1976 Aug 19;147(2):225–232. doi: 10.1007/BF00267575. [DOI] [PubMed] [Google Scholar]
  38. Travers A. RNA polymerase specificity and the control of growth. Nature. 1976 Oct 21;263(5579):641–646. doi: 10.1038/263641a0. [DOI] [PubMed] [Google Scholar]
  39. VOGEL H. J., BONNER D. M. Acetylornithinase of Escherichia coli: partial purification and some properties. J Biol Chem. 1956 Jan;218(1):97–106. [PubMed] [Google Scholar]
  40. Wanner B. L., Kodaira R., Neidhardt F. C. Physiological regulation of a decontrolled lac operon. J Bacteriol. 1977 Apr;130(1):212–222. doi: 10.1128/jb.130.1.212-222.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wyche J. H., Ely B., Cebula T. A., Snead M. C., Hartman P. E. Histidyl-transfer ribonucleic acid synthetase in positive control of the histidine operon in Salmonella typhimurium. J Bacteriol. 1974 Feb;117(2):708–716. doi: 10.1128/jb.117.2.708-716.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. van Ooyen A. J., Gruber M., Jorgensen P. The mechanism of action of ppGpp on rRNA synthesis in vitro. Cell. 1976 May;8(1):123–128. doi: 10.1016/0092-8674(76)90193-8. [DOI] [PubMed] [Google Scholar]

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