Skip to main content
NCBI home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1989 May;171(5):2424–2434. doi: 10.1128/jb.171.5.2424-2434.1989

Altered transcriptional patterns affecting several metabolic pathways in strains of Salmonella typhimurium which overexpress the fructose regulon.

A M Chin 1, D A Feldheim 1, M H Saier Jr 1
PMCID: PMC209917  PMID: 2496106

Abstract

Expression of beta-galactosidase in transcriptional fusions with the pps gene (encoding phosphoenolpyruvate [PEP] synthase), the aceBAK operon (encoding malate synthase, isocitrate lyase, and isocitrate dehydrogenase kinase, respectively), and the phs operon (encoding either thiosulfate reductase or a regulatory protein controlling its expression) was studied in Salmonella typhimurium. beta-Galactosidase synthesis in these strains was repressible either by growth in the presence of glucose or by the presence of a fruR mutation, which resulted in the constitutive expression of the fructose (fru) regulon. Five enzymes of gluconeogenesis (PEP synthase, PEP carboxykinase, isocitrate lyase, malate synthase, and fructose-1,6-diphosphatase) were shown to be repressed either by growth in the presence of glucose or the fruR mutation, while the glycolytic enzymes, enzyme I and enzymes II of the phosphotransferase system as well as phosphofructokinase, were induced either by growth in the presence of glucose or the fruR mutation. Overexpression of the cloned fru regulon genes (not including fruR) resulted in parallel repression of representative gluconeogenic, Krebs cycle, and glyoxylate shunt enzymes. Studies with temperature-sensitive mutants of S. typhimurium which synthesized heat-labile IIIFru proteins provided evidence that this protein plays a role in the regulation of gluconeogenic substrate utilization. Other mutant analyses revealed a complex relationship between fru gene expression and the expression of genes encoding gluconeogenic enzymes. Taken together, the results suggest that a number of genes encoding catabolic, biosynthetic, and amphibolic enzymes in enteric bacteria are transcriptionally regulated by a complex catabolite repression/activation mechanism which may involve enzyme IIIFru of the phosphotransferase system as one component of the regulatory system.

Full text

PDF
2424

Selected References

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

  1. Brice C. B., Kornberg H. L. Location of a gene specifying phosphopyruvate synthase activity on the genome of Escherichia coli, K12. Proc R Soc Lond B Biol Sci. 1967 Sep 12;168(1012):281–292. doi: 10.1098/rspb.1967.0066. [DOI] [PubMed] [Google Scholar]
  2. Castilho B. A., Olfson P., Casadaban M. J. Plasmid insertion mutagenesis and lac gene fusion with mini-mu bacteriophage transposons. J Bacteriol. 1984 May;158(2):488–495. doi: 10.1128/jb.158.2.488-495.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Chin A. M., Feucht B. U., Saier M. H., Jr Evidence for regulation of gluconeogenesis by the fructose phosphotransferase system in Salmonella typhimurium. J Bacteriol. 1987 Feb;169(2):897–899. doi: 10.1128/jb.169.2.897-899.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Fraenkel D. G. The phosphoenolpyruvate-initiated pathway of fructose metabolism in Escherichia coli. J Biol Chem. 1968 Dec 25;243(24):6458–6463. [PubMed] [Google Scholar]
  5. Geerse R. H., Ruig C. R., Schuitema A. R., Postma P. W. Relationship between pseudo-HPr and the PEP: fructose phosphotransferase system in Salmonella typhimurium and Escherichia coli. Mol Gen Genet. 1986 Jun;203(3):435–444. doi: 10.1007/BF00422068. [DOI] [PubMed] [Google Scholar]
  6. Goldie A. H., Sanwal B. D. Genetic and physiological characterization of Escherichia coli mutants deficient in phosphoenolpyruvate carboxykinase activity. J Bacteriol. 1980 Mar;141(3):1115–1121. doi: 10.1128/jb.141.3.1115-1121.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Groisman E. A., Casadaban M. J. Mini-mu bacteriophage with plasmid replicons for in vivo cloning and lac gene fusing. J Bacteriol. 1986 Oct;168(1):357–364. doi: 10.1128/jb.168.1.357-364.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hansen E. J., Juni E. Two routes for synthesis of phosphoenolpyruvate from C4-dicarboxylic acids in Escherichia coli. Biochem Biophys Res Commun. 1974 Aug 19;59(4):1204–1210. doi: 10.1016/0006-291x(74)90442-2. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Hughes K. T., Roth J. R. Transitory cis complementation: a method for providing transposition functions to defective transposons. Genetics. 1988 May;119(1):9–12. doi: 10.1093/genetics/119.1.9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ingledew W. J., Poole R. K. The respiratory chains of Escherichia coli. Microbiol Rev. 1984 Sep;48(3):222–271. doi: 10.1128/mr.48.3.222-271.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Krebs A., Bridger W. A. The kinetic properties of phosphoenolpyruvate carboxykinase of Escherichia coli. Can J Biochem. 1980 Apr;58(4):309–318. doi: 10.1139/o80-041. [DOI] [PubMed] [Google Scholar]
  13. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  14. LaPorte D. C., Thorsness P. E., Koshland D. E., Jr Compensatory phosphorylation of isocitrate dehydrogenase. A mechanism for adaptation to the intracellular environment. J Biol Chem. 1985 Sep 5;260(19):10563–10568. [PubMed] [Google Scholar]
  15. Maloy S. R., Bohlander M., Nunn W. D. Elevated levels of glyoxylate shunt enzymes in Escherichia coli strains constitutive for fatty acid degradation. J Bacteriol. 1980 Aug;143(2):720–725. doi: 10.1128/jb.143.2.720-725.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Manayan R., Tenn G., Yee H. B., Desai J. D., Yamada M., Saier M. H., Jr Genetic analyses of the mannitol permease of Escherichia coli: isolation and characterization of a transport-deficient mutant which retains phosphorylation activity. J Bacteriol. 1988 Mar;170(3):1290–1296. doi: 10.1128/jb.170.3.1290-1296.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Saier M. H., Jr, Cox D. F., Moczydlowski E. G. Sugar phosphate:sugar transphosphorylation coupled to exchange group translocation catalyzed by the enzyme II complexes of the phosphoenolpyruvate:sugar phosphotransferase system in membrane vesicles of Escherichia coli. J Biol Chem. 1977 Dec 25;252(24):8908–8916. [PubMed] [Google Scholar]
  18. Saier M. H., Jr, Roseman S. Sugar transport. The crr mutation: its effect on repression of enzyme synthesis. J Biol Chem. 1976 Nov 10;251(21):6598–6605. [PubMed] [Google Scholar]
  19. Sanderson K. E., Roth J. R. Linkage map of Salmonella typhimurium, Edition VI. Microbiol Rev. 1983 Sep;47(3):410–453. doi: 10.1128/mr.47.3.410-453.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Simoni R. D., Roseman S., Saier M. H., Jr Sugar transport. Properties of mutant bacteria defective in proteins of the phosphoenolpyruvate: sugar phosphotransferase system. J Biol Chem. 1976 Nov 10;251(21):6584–6597. [PubMed] [Google Scholar]
  21. Sutrina S. L., Chin A. M., Esch F., Saier M. H., Jr Purification and characterization of the fructose-inducible HPr-like protein, FPr, and the fructose-specific enzyme III of the phosphoenolpyruvate: sugar phosphotransferase system of Salmonella typhimurium. J Biol Chem. 1988 Apr 15;263(11):5061–5069. [PubMed] [Google Scholar]
  22. Wilson R. B., Maloy S. R. Isolation and characterization of Salmonella typhimurium glyoxylate shunt mutants. J Bacteriol. 1987 Jul;169(7):3029–3034. doi: 10.1128/jb.169.7.3029-3034.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Yamada M., Feucht B. U., Saier M. H., Jr Regulation of gluconeogenesis by the glucitol enzyme III of the phosphotransferase system in Escherichia coli. J Bacteriol. 1987 Dec;169(12):5416–5422. doi: 10.1128/jb.169.12.5416-5422.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Yamada M., Saier M. H., Jr Glucitol-specific enzymes of the phosphotransferase system in Escherichia coli. Nucleotide sequence of the gut operon. J Biol Chem. 1987 Apr 25;262(12):5455–5463. [PubMed] [Google Scholar]
  25. Yamada M., Saier M. H., Jr Physical and genetic characterization of the glucitol operon in Escherichia coli. J Bacteriol. 1987 Jul;169(7):2990–2994. doi: 10.1128/jb.169.7.2990-2994.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES