Skip to main content
NCBI home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1996 Feb;178(4):1012–1017. doi: 10.1128/jb.178.4.1012-1017.1996

Coordinate genetic regulation of glycogen catabolism and biosynthesis in Escherichia coli via the CsrA gene product.

H Yang 1, M Y Liu 1, T Romeo 1
PMCID: PMC177760  PMID: 8576033

Abstract

The carbon storage regulator gene, csrA, encodes a factor which negatively modulates the expression of the glycogen biosynthetic gene glgC by enhancing the decay of its mRNA (M. Y. Liu, H. Yang, and T. Romeo, J. Bacteriol. 177:2663-2672, 1995). When endogenous glycogen levels in isogenic csrA+ and csrA::kanR strains were quantified during the growth curve, both the rate of glycogen accumulation during late exponential or early stationary phase and its subsequent rate of degradation were found to be greatly accelerated by the csrA::kanR mutation. The expression of the biosynthetic genes glgA (glycogen synthase) and glgS was observed to be negatively modulated via csrA. Thus, csrA is now known to control all of the known glycogen biosynthetic genes (glg), which are located in three different operons. Similarly, the expression of the degradative enzyme glycogen phosphorylase, which is encoded by glgY, was found to be negatively regulated via csrA in vivo. The in vitro transcription-translation of glgY was also specifically inhibited by the purified CsrA gene product. These results demonstrate that localization of glycogen biosynthetic and degradative genes within the Escherichia coli glgCAY operon facilitates their coordinate genetic regulation, as previously hypothesized (T. Romeo, A. Kumar, and J. Preiss, Gene 70:363-376, 1988). The csrA gene did not affect glycogen debranching enzyme, which is now shown to be encoded by the gene glgX.

Full Text

The Full Text of this article is available as a PDF (250.0 KB).

Selected References

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

  1. Baecker P. A., Furlong C. E., Preiss J. Biosynthesis of bacterial glycogen. Primary structure of Escherichia coli ADP-glucose synthetase as deduced from the nucleotide sequence of the glg C gene. J Biol Chem. 1983 Apr 25;258(8):5084–5088. [PubMed] [Google Scholar]
  2. Baecker P. A., Greenberg E., Preiss J. Biosynthesis of bacterial glycogen. Primary structure of Escherichia coli 1,4-alpha-D-glucan:1,4-alpha-D-glucan 6-alpha-D-(1, 4-alpha-D-glucano)-transferase as deduced from the nucleotide sequence of the glg B gene. J Biol Chem. 1986 Jul 5;261(19):8738–8743. [PubMed] [Google Scholar]
  3. Chen G. S., Segel I. H. Escherichia coli polyglucose phosphorylases. Arch Biochem Biophys. 1968 Sep 20;127(1):164–174. doi: 10.1016/0003-9861(68)90213-0. [DOI] [PubMed] [Google Scholar]
  4. Chen G. S., Segel I. H. Purification and properties of glycogen phosphorylase from Escherichia coli. Arch Biochem Biophys. 1968 Sep 20;127(1):175–186. doi: 10.1016/0003-9861(68)90214-2. [DOI] [PubMed] [Google Scholar]
  5. Cui Y., Chatterjee A., Liu Y., Dumenyo C. K., Chatterjee A. K. Identification of a global repressor gene, rsmA, of Erwinia carotovora subsp. carotovora that controls extracellular enzymes, N-(3-oxohexanoyl)-L-homoserine lactone, and pathogenicity in soft-rotting Erwinia spp. J Bacteriol. 1995 Sep;177(17):5108–5115. doi: 10.1128/jb.177.17.5108-5115.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Fleischmann R. D., Adams M. D., White O., Clayton R. A., Kirkness E. F., Kerlavage A. R., Bult C. J., Tomb J. F., Dougherty B. A., Merrick J. M. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science. 1995 Jul 28;269(5223):496–512. doi: 10.1126/science.7542800. [DOI] [PubMed] [Google Scholar]
  7. Hengge-Aronis R., Fischer D. Identification and molecular analysis of glgS, a novel growth-phase-regulated and rpoS-dependent gene involved in glycogen synthesis in Escherichia coli. Mol Microbiol. 1992 Jul;6(14):1877–1886. doi: 10.1111/j.1365-2958.1992.tb01360.x. [DOI] [PubMed] [Google Scholar]
  8. Hofnung M., Schwartz M., Hatfield D. Complementation studies in the maltose-A region of the Escherichia coli K12 genetic map. J Mol Biol. 1971 Nov 14;61(3):681–694. doi: 10.1016/0022-2836(71)90072-6. [DOI] [PubMed] [Google Scholar]
  9. Jeanningros R., Creuzet-Sigal N., Frixon C., Cattaneo J. Purification and properties of a debranching enzyme from Escherichia coli. Biochim Biophys Acta. 1976 Jun 7;438(1):186–199. doi: 10.1016/0005-2744(76)90235-7. [DOI] [PubMed] [Google Scholar]
  10. Kumar A., Larsen C. E., Preiss J. Biosynthesis of bacterial glycogen. Primary structure of Escherichia coli ADP-glucose:alpha-1,4-glucan, 4-glucosyltransferase as deduced from the nucleotide sequence of the glgA gene. J Biol Chem. 1986 Dec 5;261(34):16256–16259. [PubMed] [Google Scholar]
  11. Lee E. Y. The action of sweet potato -amylase on glycogen and amylopectin: formation of a novel limit dextrin. Arch Biochem Biophys. 1971 Oct;146(2):488–492. doi: 10.1016/0003-9861(71)90153-6. [DOI] [PubMed] [Google Scholar]
  12. Liu M. Y., Yang H., Romeo T. The product of the pleiotropic Escherichia coli gene csrA modulates glycogen biosynthesis via effects on mRNA stability. J Bacteriol. 1995 May;177(10):2663–2672. doi: 10.1128/jb.177.10.2663-2672.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Okita T. W., Rodriguez R. L., Preiss J. Biosynthesis of bacterial glycogen. Cloning of the glycogen biosynthetic enzyme structural genes of Escherichia coli. J Biol Chem. 1981 Jul 10;256(13):6944–6952. [PubMed] [Google Scholar]
  14. Preiss J. Bacterial glycogen synthesis and its regulation. Annu Rev Microbiol. 1984;38:419–458. doi: 10.1146/annurev.mi.38.100184.002223. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Raha M., Kawagishi I., Müller V., Kihara M., Macnab R. M. Escherichia coli produces a cytoplasmic alpha-amylase, AmyA. J Bacteriol. 1992 Oct;174(20):6644–6652. doi: 10.1128/jb.174.20.6644-6652.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Romeo T., Gong M. Genetic and physical mapping of the regulatory gene csrA on the Escherichia coli K-12 chromosome. J Bacteriol. 1993 Sep;175(17):5740–5741. doi: 10.1128/jb.175.17.5740-5741.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Romeo T., Gong M., Liu M. Y., Brun-Zinkernagel A. M. Identification and molecular characterization of csrA, a pleiotropic gene from Escherichia coli that affects glycogen biosynthesis, gluconeogenesis, cell size, and surface properties. J Bacteriol. 1993 Aug;175(15):4744–4755. doi: 10.1128/jb.175.15.4744-4755.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Romeo T., Kumar A., Preiss J. Analysis of the Escherichia coli glycogen gene cluster suggests that catabolic enzymes are encoded among the biosynthetic genes. Gene. 1988 Oct 30;70(2):363–376. doi: 10.1016/0378-1119(88)90208-9. [DOI] [PubMed] [Google Scholar]
  20. Romeo T., Preiss J. Genetic regulation of glycogen biosynthesis in Escherichia coli: in vitro effects of cyclic AMP and guanosine 5'-diphosphate 3'-diphosphate and analysis of in vivo transcripts. J Bacteriol. 1989 May;171(5):2773–2782. doi: 10.1128/jb.171.5.2773-2782.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Sabnis N. A., Yang H., Romeo T. Pleiotropic regulation of central carbohydrate metabolism in Escherichia coli via the gene csrA. J Biol Chem. 1995 Dec 8;270(49):29096–29104. doi: 10.1074/jbc.270.49.29096. [DOI] [PubMed] [Google Scholar]
  22. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Schneider E., Freundlieb S., Tapio S., Boos W. Molecular characterization of the MalT-dependent periplasmic alpha-amylase of Escherichia coli encoded by malS. J Biol Chem. 1992 Mar 15;267(8):5148–5154. [PubMed] [Google Scholar]
  24. Schwartz M. Location of the maltose A and B loci on the genetic map of Escherichia coli. J Bacteriol. 1966 Oct;92(4):1083–1089. doi: 10.1128/jb.92.4.1083-1089.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Yanisch-Perron C., Vieira J., Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. doi: 10.1016/0378-1119(85)90120-9. [DOI] [PubMed] [Google Scholar]
  26. Yu F., Jen Y., Takeuchi E., Inouye M., Nakayama H., Tagaya M., Fukui T. Alpha-glucan phosphorylase from Escherichia coli. Cloning of the gene, and purification and characterization of the protein. J Biol Chem. 1988 Sep 25;263(27):13706–13711. [PubMed] [Google Scholar]

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

RESOURCES