Responses of E. coli to osmotic stress: large changes in amounts of cytoplasmic solutes and water

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Abstract

Escherichia coli is capable of growing in environments ranging from very dilute aqueous solutions of essential nutrients to media containing molar concentrations of salts or nonelectrolyte solutes. Growth in environments with such a wide range (at least 100-fold) of osmolarities poses significant physiological challenges for cells. To meet these challenges, E. coli adjusts a wide range of cytoplasmic solution variables, including the cytoplasmic amounts both of water and of charged and uncharged solutes.

Section snippets

Characteristics of E. coli as an osmotic system

The E. coli cell, like cells of related (Gram-negative) bacteria, consists of two concentric internal compartments, the periplasm and the cytoplasm, separated by the cytoplasmic membrane and surrounded by the cell wall (which consists of the outer membrane and the attached peptidoglycan layer). The cell wall is porous and elastic[13]; the peptidoglycan layer stretches without bursting in response to a modest, outwardly directed osmotic pressure difference called the turgor pressure (Δ∏), which

The E. coli cytoplasm as a chemical system

The grey panels in Fig. 2 summarize the amounts of cytoplasmic water, osmolytes and nucleic acid and, based on these amounts, total concentrations of these solutes in the cytoplasm of log phase E. coli grown in a defined minimal medium at the osmolarity of most rapid growth (0.28 OsM; darker grey panels) and at a lower osmolarity (0.1 OsM; lighter grey panels). The lighter blue, darker blue, and green panels in Fig. 2 depict the changes in cytoplasmic water, nucleic acid phosphate and osmotically

Stepwise analysis of cytoplasmic responses of growing E. coli to an osmotic upshift

The last four panels (lighter grey, lighter blue, darker blue and green) of Fig. 2 display the sequential consequences of shifting E. coli growing at an external osmolarity of 0.1 OsM to 1.0 OsM.

Osmotic challenges and responses of cells at low and high external osmolarity

All cells, with or without cell walls, face the same fundamental challenge as E. coli does, upon an increase in the osmolarity of their environment: namely, the need to increase the amounts of osmotically significant cytoplasmic solutes sufficiently so that dehydration is avoided and growth can continue. A variety of solutes are utilized[6], most of which are uncharged or zwitterionic derivatives of sugars or amino acids, and hence are expected to perturb cell processes less than the salt used

Acknowledgements

Support from the NIH for both the research from the authors' laboratory (NIH grant GM47022) and the preparation of this review is gratefully acknowledged. H. J. G. was supported by an NRSA NIH Postdoctoral Fellowship. We thank Peter von Hippel for the initial invitation and subsequent encouragement to write this article, and thank him and Wolf Epstein for their comments and constructive criticisms on an earlier draft. We also thank Sheila Aiello for her assistance in preparation of the

References (37)

  • B. Richey

    J. Biol. Chem.

    (1987)
  • M.W. Capp

    J. Mol. Biol.

    (1996)
  • S. Cayley et al.

    J. Mol. Biol.

    (1991)
  • J.B. Stock et al.

    J. Biol. Chem.

    (1977)
  • J.L. Milner et al.

    J. Biol. Chem.

    (1988)
  • J.M. Lucht et al.

    FEMS Microbiol. Rev.

    (1994)
  • D. McLaggan et al.

    J. Biol. Chem.

    (1994)
  • P.G. Squire et al.

    Arch. Biochem. Biophys.

    (1979)
  • A. Goldberg

    J. Mol. Biol.

    (1966)
  • I.R. Booth et al.

    Microbiol. Rev.

    (1990)
  • A.L. Koch

    J. Theor. Biol.

    (1995)
  • Wyman, J. and Gill, S. J. (1990) in Binding and Linkage, Functional Chemistry of Biological Macromolecules, University...
  • M.T. Record et al.

    Adv. Protein Chem.

    (1998)
  • Record, M. T., Jr, Courtenay, E. S., Cayley, D. S. and Guttman, H. J. Trends Biochem. Sci. (in...
  • A. Kuhn et al.

    J. Bacteriol.

    (1985)
  • P.H. Yancey

    Science

    (1982)
  • W. Epstein et al.

    J. Gen. Physiol.

    (1965)
  • P.I. Larsen et al.

    Arch. Microbiol.

    (1987)
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