Archives of Microbiology

, Volume 149, Issue 3, pp 232–239

Glycine betaine reverses the effects of osmotic stress on DNA replication and cellular division in Escherichia coli

  • J. Meury
Original Papers


The accumulation of glycine betaine to a high internal concentration by Escherichia coli cells in high osmolarity medium restores, within 1 h, a subnormal growth rate. The experimental results support the view that cell adaptation to high osmolarity involves a decrease in the initiation frequency of DNA replication via a stringent response; in contrast, glycine betaine transport and accumulation could suppress the stringent response within 1–2 min and restore a higher initiation frequency. High osmolarity also triggers the cells to lengthen, perhaps via an inhibition of cellular division; glycine betaine also reverses this process. It is inferred that turgor could control DNA replication and cell division in two separate ways. Glycine betaine action is not mediated by K+ ions as the internal level of K+ ions is not modified significantly following glycine betaine accumulation.

Key words

Turgor Glycine betaine K+ Escherichia coli 


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  1. Barron A, May G, Bremer E, Villarejo M (1986) Regulation of envelope protein composition during adaptation to osmotic stress in Escherichia coli. J Bacteriol 167:433–438Google Scholar
  2. Cairney J, Booth IR, Higgins CF (1985a) Osmoregulation of gene expression in Salmonella typhimurium: pro U encodes an osmotically induced betaine transport system. J Bacteriol 164:1224–1232Google Scholar
  3. Cairney J, Booth IR, Higgins CF (1986b) Salmonella typhimurium pro P gene encodes a transport system for the osmoprotectant betaine. J Bacteriol 164:1088–1093Google Scholar
  4. Carl PL (1970) Escherichia coli mutants with temperature-sensitive synthesis of DNA. Mol Gen Genet 109:107–122Google Scholar
  5. Christian JGB (1955) The influence of nutrition on the water relations of Salmonella oranienburg. Aust J Biol Sci 8:75–82Google Scholar
  6. Clark D, Parker J (1984) Proteins induced by high osmotic pressure in Escherichia coli. FEMS Microbiol Lett 25:81–83Google Scholar
  7. Csonka LN (1981) Proline over-production results in enhanced osmotolerance in Salmonella typhimurium. Mol Gen Genet 182:82–86Google Scholar
  8. Csonka LN (1982) A third l-proline permease in Salmonella typhimurium which functions in media of elevated osmotic strength. J Bacteriol 151:1433–1443Google Scholar
  9. Epstein W, Schultz SG (1965) Cation transport in Escherichia coli. V. Regulation of cation content. J Gen Physiol 49:221–234Google Scholar
  10. Gallant JA (1979) Stringent control in Escherichia coli. Ann Rev Genet 13:393–415Google Scholar
  11. Girija R, Ikenaka K, Inouye M (1985) Uncoupling of osmoregulation of the Escherichia coli K-12 omp F gene from omp B-dependent transcription. J Bacteriol 163:82–87Google Scholar
  12. Glass RE, Jones S, Ishihama A (1986) Genetic studies on the β subunit of Escherichia coli RNA polymerase. VII. RNA polymerase is a target for ppGpp. Mol Gen Genet 203:265–268Google Scholar
  13. Gowrishankar Y (1985) Identification of osmo-responsive genes of Escherichia coli: evidence for participation of potassium and proline transport systems in osmoregulation. J Bacteriol 164:434–445Google Scholar
  14. Hecker M, Schroeter A, Mach F (1983) Replication of pBR 322 DNA in stringent and relaxed strains of Escherichia coli. Mol Gen Genet 190:355–357Google Scholar
  15. Jackson BJ, Kennedy EP (1983) The biosynthesis of membrane-derived oligosaccharides. A membrane-bound phosphoglycerol transferase. J Biol Chem 258:2394–2398Google Scholar
  16. Kawaji H, Mizuno T, Mizushima S (1979) Influence of molecular size and osmolarity of sugars and dextrans on the synthesis of outer membrane proteins 0-8 and 0-9 of Escherichia coli K-12. J Bacteriol 140:843–847Google Scholar
  17. Ken-Dror S, Preger R, Avi-Dor Y (1986) Role of betaine in the control of respiration and osmoregulation of a halotolerant bacterium. FEMS Microbiol Rev 39:115–120Google Scholar
  18. Kennedy EP (1982) Osmotic regulation and the biosynthesis of membrane-derived oligosaccharides. Proc Natl Acad Sci USA 79:1092–1095Google Scholar
  19. Koch A, Higgins MC, Doyle R (1981) Surface tension-like forces determine bacterial shapes: Streptococcus faecium. J Bacteriol 147:97–100Google Scholar
  20. Koch A (1984) Shrinkage of growing Escherichia coli cells by osmotic challenge. J Bacteriol 159:919–924Google Scholar
  21. Kogut M, Russel NJ (1984) Growth and phospholipid composition of a moderately halophilic bacterium during adaptation to changes in salinity. Curr Microbiol 10:95–98Google Scholar
  22. Kubitschek HE, Freedman ML, Silver S (1971) Potassium uptake in synchronous and synchronized cultures of Escherichia coli. Biophys J 11:787–795Google Scholar
  23. Laffler T, Gallant JA (1974) A new genetic locus involved in the stringent response in Escherichia coli. Cell 1:27–30Google Scholar
  24. Lebail S (1979) Transport du K+ au cours du cycle cellulaire chez Escherichia coli. Thesis, Université de ParisGoogle Scholar
  25. Legros M, Kepes A (1985) One-step fluorometric microassay of DNA in procaryotes. Anal Biochem 147:497–502Google Scholar
  26. Le Rudulier D, Valentine RC (1982) Genetic engineering in agriculture: osmoregulation. TIBS 7:431–433Google Scholar
  27. Le Rudulier D, Bouillard L (1983) Glycine betaine, an osmotic effector in Klebsiella pneumoniae and other members of the Enterobacteriaceae. Appl Environ Microbiol 46:152–159Google Scholar
  28. Le Rudulier D, Strom AR, Dandekar AM, Smith LT, Valentine RC (1984) Molecular biology of osmoregulation. Science 224:1064–1068Google Scholar
  29. Lin-Chao S, Bremer H (1986) Effect of rel A function on the replication of plasmid pBR322 in Escherichia coli. Mol Gen Genet 203:150–153Google Scholar
  30. Lowry OH, Rosebrough NJ, Farr AL, Randal RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275Google Scholar
  31. Meury J (1976) Potassium transport in Escherichia coli. Thesis, Université de ParisGoogle Scholar
  32. Meury J, Robin A, Monier-Champex P (1985) Turgor-controlled fluxes and their pathways in Escherichia coli. Eur J Biochem 151:613–619Google Scholar
  33. Miller KJ, Kennedy EP, Reinhold VN (1986) Osmotic adaptation by Gram-negative bacteria: possible role for periplasmic oligosaccharides. Science 231:48–51Google Scholar
  34. Munro GF, Bell CA (1973) Effects of external osmolarity on phospholipid metabolism in Escherchiaa coli B. J Bacteriol 166:257–262Google Scholar
  35. Olijhoek AJM, Van Eden CG, Trueba F, Pas E, Anninga N (1982) Plasmolysis during the division cycle of Escherichia coli. J Bacteriol 152:479–484Google Scholar
  36. Perroud B, Le Rudulier D (1985) Glycine betaine transport in Escherichia coli. Osmotic modulation. J Bacteriol 161:393–401Google Scholar
  37. Roth W, Leckie M, Dietzler D (1985a) Osmotic stress drastically inhibits active transport of carbohydrates by Escherichia coli. Biochem Biophys Res Commun 126:434–441Google Scholar
  38. Roth W, Porter S, Leckie M, Porter B, Dietzler D (1985b) Restoration of cell volume and the reversal of carbohydrate transport and growth inhibition of osmotically upshocked Escherichia coli. Biochem Biophys Res Commun 126:442–449Google Scholar
  39. Russel NJ, Kogut M (1985) Haloadaptation: salt sensing and cell-envelope changes. Microbiol Sci 11:345–350Google Scholar
  40. Thiam K, Farve A (1984) Role of the stringent response in the expression and mechanism of near-ultraviolet induced growth delay. Eur J Biochem 145:137–142Google Scholar
  41. Villarejo M, Davis J, Granett S (1983) Osmoregulation of Alkaline phosphatase synthesis in Escherichia coli K-12. J Bacteriol 156:975–978Google Scholar

Copyright information

© Springer-Verlag 1988

Authors and Affiliations

  • J. Meury
    • 1
  1. 1.Genétique et Biochimie, Institut Jacques MonodUniversité Paris VIIParis Cedex O5France

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