Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1995 Jan;177(2):413–422. doi: 10.1128/jb.177.2.413-422.1995

UDP-glucose is a potential intracellular signal molecule in the control of expression of sigma S and sigma S-dependent genes in Escherichia coli.

J Böhringer 1, D Fischer 1, G Mosler 1, R Hengge-Aronis 1
PMCID: PMC176605  PMID: 7814331

Abstract

The sigma S subunit of RNA polymerase is the master regulator of a regulatory network that controls stationary-phase induction as well as osmotic regulation of many genes in Escherichia coli. In an attempt to identify additional regulatory components in this network, we have isolated Tn10 insertion mutations that in trans alter the expression of osmY and other sigma S-dependent genes. One of these mutations conferred glucose sensitivity and was localized in pgi (encoding phosphoglucose isomerase). pgi::Tn10 strains exhibit increased basal levels of expression of osmY and otsBA in exponentially growing cells and reduced osmotic inducibility of these genes. A similar phenotype was also observed for pgm and galU mutants, which are deficient in phosphoglucomutase and UDP-glucose pyrophosphorylase, respectively. This indicates that the observed effects on gene expression are related to the lack of UDP-glucose (or a derivative thereof), which is common to all three mutants. Mutants deficient in UDP-galactose epimerase (galE mutants) and trehalose-6-phosphate synthase (otsA mutants) do not exhibit such an effect on gene expression, and an mdoA mutant that is deficient in the first step of the synthesis of membrane-derived oligosaccharides, shows only a partial increase in the expression of osmY. We therefore propose that the cellular content of UDP-glucose serves as an internal signal that controls expression of osmY and other sigma S-dependent genes. In addition, we demonstrate that pgi, pgm, and galU mutants contain increased levels of sigma S during steady-state growth, indicating that UDP-glucose interferes with the expression of sigma S itself.

Full Text

The Full Text of this article is available as a PDF (320.9 KB).

Selected References

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

  1. Adhya S., Schwartz M. Phosphoglucomutase mutants of Escherichia coli K-12. J Bacteriol. 1971 Nov;108(2):621–626. doi: 10.1128/jb.108.2.621-626.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Almirón M., Link A. J., Furlong D., Kolter R. A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Genes Dev. 1992 Dec;6(12B):2646–2654. doi: 10.1101/gad.6.12b.2646. [DOI] [PubMed] [Google Scholar]
  3. Andrews K. J., Lin E. C. Thiogalactoside transacetylase of the lactose operon as an enzyme for detoxification. J Bacteriol. 1976 Oct;128(1):510–513. doi: 10.1128/jb.128.1.510-513.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Atlung T., Brøndsted L. Role of the transcriptional activator AppY in regulation of the cyx appA operon of Escherichia coli by anaerobiosis, phosphate starvation, and growth phase. J Bacteriol. 1994 Sep;176(17):5414–5422. doi: 10.1128/jb.176.17.5414-5422.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Atlung T., Nielsen A., Hansen F. G. Isolation, characterization, and nucleotide sequence of appY, a regulatory gene for growth-phase-dependent gene expression in Escherichia coli. J Bacteriol. 1989 Mar;171(3):1683–1691. doi: 10.1128/jb.171.3.1683-1691.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bohin J. P., Kennedy E. P. Regulation of the synthesis of membrane-derived oligosaccharides in Escherichia coli. Assay of phosphoglycerol transferase I in vivo. J Biol Chem. 1984 Jul 10;259(13):8388–8393. [PubMed] [Google Scholar]
  7. Boos W., Ehmann U., Bremer E., Middendorf A., Postma P. Trehalase of Escherichia coli. Mapping and cloning of its structural gene and identification of the enzyme as a periplasmic protein induced under high osmolarity growth conditions. J Biol Chem. 1987 Sep 25;262(27):13212–13218. [PubMed] [Google Scholar]
  8. Boos W., Ehmann U., Forkl H., Klein W., Rimmele M., Postma P. Trehalose transport and metabolism in Escherichia coli. J Bacteriol. 1990 Jun;172(6):3450–3461. doi: 10.1128/jb.172.6.3450-3461.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Boyd D., Manoil C., Beckwith J. Determinants of membrane protein topology. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8525–8529. doi: 10.1073/pnas.84.23.8525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Brand B., Boos W. Maltose transacetylase of Escherichia coli. Mapping and cloning of its structural, gene, mac, and characterization of the enzyme as a dimer of identical polypeptides with a molecular weight of 20,000. J Biol Chem. 1991 Jul 25;266(21):14113–14118. [PubMed] [Google Scholar]
  11. Bremer E., Silhavy T. J., Weinstock G. M. Transposition of lambda placMu is mediated by the A protein altered at its carboxy-terminal end. Gene. 1988 Nov 15;71(1):177–186. doi: 10.1016/0378-1119(88)90089-3. [DOI] [PubMed] [Google Scholar]
  12. Brøndsted L., Atlung T. Anaerobic regulation of the hydrogenase 1 (hya) operon of Escherichia coli. J Bacteriol. 1994 Sep;176(17):5423–5428. doi: 10.1128/jb.176.17.5423-5428.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Böck A., Neidhardt F. C. Properties of a Mutant of Escherichia coli with a Temperature-sensitive Fructose-1,6-Diphosphate Aldolase. J Bacteriol. 1966 Aug;92(2):470–476. doi: 10.1128/jb.92.2.470-476.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Csonka L. N. Physiological and genetic responses of bacteria to osmotic stress. Microbiol Rev. 1989 Mar;53(1):121–147. doi: 10.1128/mr.53.1.121-147.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Dassa J., Fsihi H., Marck C., Dion M., Kieffer-Bontemps M., Boquet P. L. A new oxygen-regulated operon in Escherichia coli comprises the genes for a putative third cytochrome oxidase and for pH 2.5 acid phosphatase (appA) Mol Gen Genet. 1991 Oct;229(3):341–352. doi: 10.1007/BF00267454. [DOI] [PubMed] [Google Scholar]
  16. FUKASAWA T., JOKURA K., KURAHASHI K. A new enzymic defect of galactose metabolism in Escherichia coli K-12 mutants. Biochem Biophys Res Commun. 1962 Apr 3;7:121–125. doi: 10.1016/0006-291x(62)90158-4. [DOI] [PubMed] [Google Scholar]
  17. Gentry D. R., Hernandez V. J., Nguyen L. H., Jensen D. B., Cashel M. Synthesis of the stationary-phase sigma factor sigma s is positively regulated by ppGpp. J Bacteriol. 1993 Dec;175(24):7982–7989. doi: 10.1128/jb.175.24.7982-7989.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Giaever H. M., Styrvold O. B., Kaasen I., Strøm A. R. Biochemical and genetic characterization of osmoregulatory trehalose synthesis in Escherichia coli. J Bacteriol. 1988 Jun;170(6):2841–2849. doi: 10.1128/jb.170.6.2841-2849.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. Hengge-Aronis R., Klein W., Lange R., Rimmele M., Boos W. Trehalose synthesis genes are controlled by the putative sigma factor encoded by rpoS and are involved in stationary-phase thermotolerance in Escherichia coli. J Bacteriol. 1991 Dec;173(24):7918–7924. doi: 10.1128/jb.173.24.7918-7924.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hengge-Aronis R., Lange R., Henneberg N., Fischer D. Osmotic regulation of rpoS-dependent genes in Escherichia coli. J Bacteriol. 1993 Jan;175(1):259–265. doi: 10.1128/jb.175.1.259-265.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hengge-Aronis R. Survival of hunger and stress: the role of rpoS in early stationary phase gene regulation in E. coli. Cell. 1993 Jan 29;72(2):165–168. doi: 10.1016/0092-8674(93)90655-a. [DOI] [PubMed] [Google Scholar]
  23. Hengge R., Boos W. Maltose and lactose transport in Escherichia coli. Examples of two different types of concentrative transport systems. Biochim Biophys Acta. 1983 Aug 11;737(3-4):443–478. doi: 10.1016/0304-4157(83)90009-6. [DOI] [PubMed] [Google Scholar]
  24. Irani M. H., Maitra P. K. Properties of Escherichia coli mutants deficient in enzymes of glycolysis. J Bacteriol. 1977 Nov;132(2):398–410. doi: 10.1128/jb.132.2.398-410.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Jung J. U., Gutierrez C., Martin F., Ardourel M., Villarejo M. Transcription of osmB, a gene encoding an Escherichia coli lipoprotein, is regulated by dual signals. Osmotic stress and stationary phase. J Biol Chem. 1990 Jun 25;265(18):10574–10581. [PubMed] [Google Scholar]
  26. Kaasen I., Falkenberg P., Styrvold O. B., Strøm A. R. Molecular cloning and physical mapping of the otsBA genes, which encode the osmoregulatory trehalose pathway of Escherichia coli: evidence that transcription is activated by katF (AppR) J Bacteriol. 1992 Feb;174(3):889–898. doi: 10.1128/jb.174.3.889-898.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kleckner N., Barker D. F., Ross D. G., Botstein D. Properties of the translocatable tetracycline-resistance element Tn10 in Escherichia coli and bacteriophage lambda. Genetics. 1978 Nov;90(3):427–461. doi: 10.1093/genetics/90.3.427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Kohara Y., Akiyama K., Isono K. The physical map of the whole E. coli chromosome: application of a new strategy for rapid analysis and sorting of a large genomic library. Cell. 1987 Jul 31;50(3):495–508. doi: 10.1016/0092-8674(87)90503-4. [DOI] [PubMed] [Google Scholar]
  29. Lacroix J. M., Loubens I., Tempête M., Menichi B., Bohin J. P. The mdoA locus of Escherichia coli consists of an operon under osmotic control. Mol Microbiol. 1991 Jul;5(7):1745–1753. doi: 10.1111/j.1365-2958.1991.tb01924.x. [DOI] [PubMed] [Google Scholar]
  30. Lacroix J. M., Tempête M., Menichi B., Bohin J. P. Molecular cloning and expression of a locus (mdoA) implicated in the biosynthesis of membrane-derived oligosaccharides in Escherichia coli. Mol Microbiol. 1989 Sep;3(9):1173–1182. doi: 10.1111/j.1365-2958.1989.tb00267.x. [DOI] [PubMed] [Google Scholar]
  31. Lange R., Barth M., Hengge-Aronis R. Complex transcriptional control of the sigma s-dependent stationary-phase-induced and osmotically regulated osmY (csi-5) gene suggests novel roles for Lrp, cyclic AMP (cAMP) receptor protein-cAMP complex, and integration host factor in the stationary-phase response of Escherichia coli. J Bacteriol. 1993 Dec;175(24):7910–7917. doi: 10.1128/jb.175.24.7910-7917.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Lange R., Hengge-Aronis R. Identification of a central regulator of stationary-phase gene expression in Escherichia coli. Mol Microbiol. 1991 Jan;5(1):49–59. doi: 10.1111/j.1365-2958.1991.tb01825.x. [DOI] [PubMed] [Google Scholar]
  33. Lange R., Hengge-Aronis R. The cellular concentration of the sigma S subunit of RNA polymerase in Escherichia coli is controlled at the levels of transcription, translation, and protein stability. Genes Dev. 1994 Jul 1;8(13):1600–1612. doi: 10.1101/gad.8.13.1600. [DOI] [PubMed] [Google Scholar]
  34. Lange R., Hengge-Aronis R. The nlpD gene is located in an operon with rpoS on the Escherichia coli chromosome and encodes a novel lipoprotein with a potential function in cell wall formation. Mol Microbiol. 1994 Aug;13(4):733–743. doi: 10.1111/j.1365-2958.1994.tb00466.x. [DOI] [PubMed] [Google Scholar]
  35. Loewen P. C., von Ossowski I., Switala J., Mulvey M. R. KatF (sigma S) synthesis in Escherichia coli is subject to posttranscriptional regulation. J Bacteriol. 1993 Apr;175(7):2150–2153. doi: 10.1128/jb.175.7.2150-2153.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. May G., Dersch P., Haardt M., Middendorf A., Bremer E. The osmZ (bglY) gene encodes the DNA-binding protein H-NS (H1a), a component of the Escherichia coli K12 nucleoid. Mol Gen Genet. 1990 Oct;224(1):81–90. doi: 10.1007/BF00259454. [DOI] [PubMed] [Google Scholar]
  37. McCann M. P., Fraley C. D., Matin A. The putative sigma factor KatF is regulated posttranscriptionally during carbon starvation. J Bacteriol. 1993 Apr;175(7):2143–2149. doi: 10.1128/jb.175.7.2143-2149.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Mulvey M. R., Switala J., Borys A., Loewen P. C. Regulation of transcription of katE and katF in Escherichia coli. J Bacteriol. 1990 Dec;172(12):6713–6720. doi: 10.1128/jb.172.12.6713-6720.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Preiss J., Romeo T. Physiology, biochemistry and genetics of bacterial glycogen synthesis. Adv Microb Physiol. 1989;30:183–238. doi: 10.1016/s0065-2911(08)60113-7. [DOI] [PubMed] [Google Scholar]
  40. SUNDARARAJAN T. A., RAPIN A. M., KALCKAR H. M. Biochemical observations on E. coli mutants defective in uridine diphosphoglucose. Proc Natl Acad Sci U S A. 1962 Dec 15;48:2187–2193. doi: 10.1073/pnas.48.12.2187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Schellhorn H. E., Stones V. L. Regulation of katF and katE in Escherichia coli K-12 by weak acids. J Bacteriol. 1992 Jul;174(14):4769–4776. doi: 10.1128/jb.174.14.4769-4776.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Schulman H., Kennedy E. P. Identification of UDP-glucose as an intermediate in the biosynthesis of the membrane-derived oligosaccharides of Escherichia coli. J Biol Chem. 1977 Sep 25;252(18):6299–6303. [PubMed] [Google Scholar]
  43. Singer M., Baker T. A., Schnitzler G., Deischel S. M., Goel M., Dove W., Jaacks K. J., Grossman A. D., Erickson J. W., Gross C. A. A collection of strains containing genetically linked alternating antibiotic resistance elements for genetic mapping of Escherichia coli. Microbiol Rev. 1989 Mar;53(1):1–24. doi: 10.1128/mr.53.1.1-24.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Singer M., Rossmiessl P., Cali B. M., Liebke H., Gross C. A. The Escherichia coli ts8 mutation is an allele of fda, the gene encoding fructose-1,6-diphosphate aldolase. J Bacteriol. 1991 Oct;173(19):6242–6248. doi: 10.1128/jb.173.19.6242-6248.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Singer M., Walter W. A., Cali B. M., Rouviere P., Liebke H. H., Gourse R. L., Gross C. A. Physiological effects of the fructose-1,6-diphosphate aldolase ts8 mutation on stable RNA synthesis in Escherichia coli. J Bacteriol. 1991 Oct;173(19):6249–6257. doi: 10.1128/jb.173.19.6249-6257.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Styrvold O. B., Strøm A. R. Synthesis, accumulation, and excretion of trehalose in osmotically stressed Escherichia coli K-12 strains: influence of amber suppressors and function of the periplasmic trehalase. J Bacteriol. 1991 Feb;173(3):1187–1192. doi: 10.1128/jb.173.3.1187-1192.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Tanaka K., Takayanagi Y., Fujita N., Ishihama A., Takahashi H. Heterogeneity of the principal sigma factor in Escherichia coli: the rpoS gene product, sigma 38, is a second principal sigma factor of RNA polymerase in stationary-phase Escherichia coli. Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3511–3515. doi: 10.1073/pnas.90.8.3511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Way J. C., Davis M. A., Morisato D., Roberts D. E., Kleckner N. New Tn10 derivatives for transposon mutagenesis and for construction of lacZ operon fusions by transposition. Gene. 1984 Dec;32(3):369–379. doi: 10.1016/0378-1119(84)90012-x. [DOI] [PubMed] [Google Scholar]
  49. Weichart D., Lange R., Henneberg N., Hengge-Aronis R. Identification and characterization of stationary phase-inducible genes in Escherichia coli. Mol Microbiol. 1993 Oct;10(2):407–420. [PubMed] [Google Scholar]
  50. Weissborn A. C., Liu Q., Rumley M. K., Kennedy E. P. UTP: alpha-D-glucose-1-phosphate uridylyltransferase of Escherichia coli: isolation and DNA sequence of the galU gene and purification of the enzyme. J Bacteriol. 1994 May;176(9):2611–2618. doi: 10.1128/jb.176.9.2611-2618.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Yim H. H., Brems R. L., Villarejo M. Molecular characterization of the promoter of osmY, an rpoS-dependent gene. J Bacteriol. 1994 Jan;176(1):100–107. doi: 10.1128/jb.176.1.100-107.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Yim H. H., Villarejo M. osmY, a new hyperosmotically inducible gene, encodes a periplasmic protein in Escherichia coli. J Bacteriol. 1992 Jun;174(11):3637–3644. doi: 10.1128/jb.174.11.3637-3644.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES