Skip to main content
Log in

Osmoregulation in Escherichia coli by accumulation of organic osmolytes: betaines, glutamic acid, and trehalose

  • Original Papers
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

It has been shown previously that externally added glycine betaine is accumulated in Escherichia coli in response to the external osmotic strength. Here we have shown, by using nuclear magnetic resonance spectroscopy and radiochemical methods, that E. coli growing in a glucose-mineral medium of elevated osmotic strength generated with NaCl, had the same capacity to accumulate proline betaine and glycine betaine. Its capacity to accumulate γ-butyrobetaine was, however, 40 to 50% lower. Accordingly, externally added proline betaine and glycine betaine stimulated aerobic growth of osmotically stressed cells equally well, and they were more osmoprotective than γ-butyrobetaine. In cells grown at an osmotic strength of 0.64, 1.01, or 1.47 osmolal, respectively, the molal cytoplasmic concentration of the two former betaines corresponded to 29, 38, or 58% of the external osmotic strength. Nuclear magnetic resonance spectroscopy revealed that trehalose and glutamic acid were the only species of organic osmolytes accumulated in significant amounts in cells grown under osmotic stress in glucosemineral medium without betaines. Their combined molal concentration in the cytoplasm of cells grown at 1.01 osmolal corresponded to 27% of the external osmotic strength.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alemohammad MM, Knowles CJ (1974) Osmotically induced volume and turbidity changes of Escherichia coli due to salts, sucrose and glycerol, with particular reference to rapid permeation of glycerol into the cell. J Gen Microbiol 82:125–142

    Google Scholar 

  • Andersson L, Kühler T, Nilsson M (1981) Preparation of 3-carboxy-N,N,N-trimethylpropanaminium chloride (γ-butyrobetaine hydrochloride). Synthesis 468–469

  • Britten RJ, McClure FT (1962) The amino acid pool in Escherichia coli. Bacteriol Rev 26:292–335

    Google Scholar 

  • Cairney J, Booth IR, Higgins CF (1985a) Salmonella typhimurium proP gene encodes a transport system for the osmoprotectant betaine. J Bacteriol 164:1218–1223

    Google Scholar 

  • Cairney J, Booth IR, Higgins CF (1985b) Osmoregulation of gene expression in Salmonella typhimurium: proU encodes an osmotically induced betaine transport system. J Bacteriol 164:1224–1232

    Google Scholar 

  • Crowe JH, Crowe LM, Chapman D (1984) Preservation of membranes in anhydrobiotic organisms: the role of trehalose. Science 223:701–703

    Google Scholar 

  • Csonka LN (1981) Proline over-production results in enhanced osmotolerance in Salmonella typhimurium. Mol Gen Genet 182:82–86

    Google Scholar 

  • Epstein W (1986) Osmoregulation by potassium transport in Escherichia coli. FEMS Microbiol Rev 39:73–78

    Google Scholar 

  • Epstein W, Schultz SG (1965) Cation transport in Escherichia coli. V. Regulation of cation content. J Gen Physiol 49:221–234

    Google Scholar 

  • Galinski EA, Pfeiffer HP, Trüper HG (1985) 1,4,5,6-Tetrahydro-2-methyl-4-pyrimidinecarboxylic acid. A novel cyclic amino acid from halophilic phototrophic bacteria of the genus Ectothiorhodospira. Eur J Biochem 149:135–139

    Google Scholar 

  • Gowrishankar J (1986) proP-mediated proline transport also plays a role in Escherichia coli osmoregulation. J Bacteriol 166:331–333

    Google Scholar 

  • Herbert D, Phipps PJ, Strange RE (1971) Chemical analysis of microbial cells. In: Norris JR, Ribbons DW (eds) Methods in microbiology, vol 5B. Academic Press, London, pp 209–344

    Google Scholar 

  • Koch AL (1984) Shrinkage of growing Escherichia coli cells by osmotic challenge. J Bacteriol 159:919–924

    Google Scholar 

  • Kutscher F, Ackermann D (1933) Über das Vorkommen von Betainen in der Archenmuschel. Hoppe-Seyler's Z Physiol Chem 221:33–39

    Google Scholar 

  • Laimins LA, Rhoads DB, Epstein W (1981) Osmotic control of kdp operon expression in Escherichia coli. Proc Natl Acad Sci USA 78:464–468

    Google Scholar 

  • Landfald B, Strøm AR (1986) Choline-glycine betaine pathway confers a high level of osmotic tolerance in Escherichia coli. J Bacteriol 165:849–855

    Google Scholar 

  • Lapp D, Patterson BW, Elbein AD (1971) Properties of a trehalose phosphate synthetase from Mycobacterium smegmatis. Activation of the enzyme by polynucleotides and other polyanions. J Biol Chem 246:4567–4579

    Google Scholar 

  • Le Rudulier D, Valentine RC (1982) Genetic engineering in agriculture: osmoregulation. Trends Biochem Sci 7:431–433

    Google Scholar 

  • Le Rudulier D, Bernard T, Goas G, Hamelin J (1984a) Osmoregulation in Klebsiella pneumoniae: enhancement of anaerobic growth and nitrogen fixation under stress by proline betaine, γ-butyrobetaine, and other related compounds. Can J Microbiol 30:299–305

    Google Scholar 

  • Le Rudulier D, Strøm AR, Dandekar AM, Smith LT, Valentine RC (1984b) Molecular biology of osmoregulation. Science 224: 1064–1068

    Google Scholar 

  • Mackay MA, Norton RS, Borowitzka LJ (1984) Organic osmoregulatory solutes in cyanobacteria. J Gen Microbiol 130:2177–2191

    Google Scholar 

  • Mandava N, Fodor G (1970) Stickstoff-Stereochemie quartärer Pyrrolidiniumsalze. Liebig's Ann Chem 741:167–180

    Google Scholar 

  • Maréchal LR (1984) Transport and metabolism of trehalose in Escherichia coli and Salmonella typhimurium. Arch Microbiol 137:70–73

    Google Scholar 

  • Martin MC, Diaz LA, Manzanal MB, Hardisson C (1986) Role of trehalose in the spores of Streptomyces. FEMS Microbiol Lett 35:49–54

    Google Scholar 

  • Menzies IS, Seakins JWT (1976) Sugars. In: Smith I, Seakins JWT (eds) Chromatographic and electrophoretic techniques, vol 1. Paper and thin layer chromatography, 4th edn. William Heinemann Medical Books Ltd, Bath, pp 183–217

    Google Scholar 

  • Miller JH (1972) Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, p 431

    Google Scholar 

  • Mitchell P (1953) Transport of phosphate across the surface of Micrococcus pyogenes: nature of the cell ‘inorganic phosphate’. J Gen Microbiol 9:273–287

    Google Scholar 

  • Perroud B, Le Rudulier D (1985) Glycine betaine transport in Escherichia coli: osmotic modulation. J Bacteriol 161:393–401

    Google Scholar 

  • Reed RH, Richardson DL, Warr SRC, Stewart WDP (1984) Carbohydrate accumulation and osmotic stress in cyanobacteria. J Gen Microbiol 130:1–4

    Google Scholar 

  • Reed RH, Borowitzka LJ, Mackay MA, Chudek JA, Forster R, Warr SRC, Moore DJ, Stewart WDP (1986) Organic solute accumulation in osmotically stressed cyanobacteria. FEMS Microbiol Rev 39:51–56

    Google Scholar 

  • Roller SD, Anagnostopoulos GD (1982) Accumulation of carbohydrate by Escherichia coli B/r/1 during growth at low water activity. J Appl Bacteriol 52:425–434

    Google Scholar 

  • Stewart WDP (1983) Natural environments — challenges to microbial success and survival. Symp Soc Gen Microbiol 34:1–35

    Google Scholar 

  • Stock JB, Rauch B, Roseman S (1977) Periplasmic space in Salmonella typhimurium and Escherichia coli. J Biol Chem 252:7850–7861

    Google Scholar 

  • Strøm AR, Falkenberg P, Landfald B (1986) Genetics of osmoregulation in Escherichia coli: uptake and biosynthesis of organic osmolytes. FEMS Microbiol Rev 39:79–86

    Google Scholar 

  • Styrvold OB, Falkenberg P, Landfald B, Eshoo MW, Bjørnsen T, Strøm AR (1986) Selection, mapping, and characterization of osmoregulatory mutants of Escherichia coli blocked in the choline-glycine betaine pathway. J Bacteriol 165:856–863

    Google Scholar 

  • Tempest DW, Meers JL, Brown CM (1970) Influence of enviroment on the content and composition of microbial free amino acid pools. J Gen Microbiol 64:171–185

    Google Scholar 

  • Voelter W, Breitmaier E, Jung G (1971) Impuls-Fourier-Transform-13C-NMR-Spectroskopie mutarotierender Zucker. Angew Chem 83:1011–1012

    Google Scholar 

  • Voelter W, Fuchs S, Seuffer RH, Zech K (1974) 13C-NMR-Studien von geschützten Aminosäuren. Monatsh Chem 105: 1110–1135

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Larsen, P.I., Sydnes, L.K., Landfald, B. et al. Osmoregulation in Escherichia coli by accumulation of organic osmolytes: betaines, glutamic acid, and trehalose. Arch. Microbiol. 147, 1–7 (1987). https://doi.org/10.1007/BF00492896

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00492896

Key words

Navigation