Biophysical characterization of changes in amounts and activity of Escherichia coli cell and compartment water and turgor pressure in response to osmotic stress

Biophysical Journal

Volumn 78, Issue 4, 2000, Pages 1748-1764

  Cayley, D Scott ^a   Guttman, Harry J ^a,b   Record Jr , M Thomas ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL COMPARTMENTALIZATION; CELL GROWTH; CYTOPLASM; ESCHERICHIA COLI; MACROMOLECULE; NONHUMAN; OSMOLALITY; OSMOREGULATION; OSMOTIC STRESS; PLASMOLYSIS; PRESSURE;

ESCHERICHIA COLI; NEGIBACTERIA;

EID: 0034028431     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/s0006-3495(00)76726-9     Document Type: Article

References (59)

1. Alemohammad, M. M., and C. J. Knowles. 1974. Osmotically induced volume and turbidity changes of Escherichia coli due to salts, sucrose and glycerol. J. Gen. Microbiol. 82:125-142.
2. Ames, G. F. L., C. Brody, and S. Kustu. 1984. Simple, rapid and quantitative release of periplasmic proteins by chloroform. J. Bacteriol. 160: 1181-1183.
3. Baldwin, W. W., R. Meyer, T. King, E. Anderson, and A. L. Koch. 1995. Growth and buoyant density of Escherichia coli at very low osmolarities. J. Bacteriol. 177:235-237.
4. Brass, J. M., C. F. Higgins, M. Foley, P. A. Rugman, J. Birmingham, and P. B. Garland. 1986. Lateral diffusion of proteins in the periplasm of Escherichia coli. J. Bacteriol. 165:787-794.
5. Bremer, H., and P. P. Dennis. 1996. Modulation of chemical composition and other parameters of the cell by growth rate. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd ed. F. C. Neidhardt, R. Curtis, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaecter, and H. E. Umbarger, editors. American Society for Microbiology. Washington, DC. 1553-1569.
6. Broyer, T. C. 1952. On volume enlargement and work expenditure by an osmotic system in plants. Physiol. Plant. 5:459-469.
7. + concentrations on lac repressor-lac operator binding: in vitro thermodynamic analysis and in vivo relevance. J. Mol. Biol 258:5-36.
8. Cayley, S., B. A. Lewis, and M. T. Record, Jr. 1989. Accumulation of 3-[N-morpholino]propanesulfonate by osmotically stressed Escherichia coli K12. J. Bacteriol. 171:3597-3602.
9. Cayley, S., B. A. Lewis, H. J. Guttman, and M. T. Record, Jr. 1991. Characterization of the cytoplasm of Escherichia coli K-12 as a function of external osmolarity: implications for protein-DNA interactions in vivo. J. Mol. Biol. 222:281-300.
10. Cayley, S., B. A. Lewis, and M. T. Record, Jr. 1992. Origins of the osmoprotective properties of betaine and proline in Escherichia coli K-12. J. Bacteriol. 174:1586-1595.
11. Cosgrove, D. J. 1988. In defense of the volumetric elastic modulus. Plant Cell Environ. 11:67-69.
12. Cosgrove, D. J. 1993. Tansley Review No. 46, Wall extensibility: its nature, measurement and relationship to plant cell growth. New Phytol. 124:1-23.
13. Csonka, L. N., and W. Epstein. 1996. Osmoregulation. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology. F. C. Neidhardt, R. Curtis, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaecter, and H. E. Umbarger, editors. 2nd ed. ASM Press, Washington, DC. 1210-1223.
14. Cronan, J. E., Jr., R. B. Gennis, and S. R. Maloy. 1987. Cytoplasmic membrane. In Escherichia coli and Salmonella typhimurium Cellular and Molecular Biology. F. C. Neidhardt, S. L. Ingraham, K. B. Low, B. Magasanik, M. Schaecter, and H. E. Umbarger, editors. American Society for Microbiology, Washington, DC. 31-55.
15. Doyle, R. J., and R. E. Marquis. 1994. Elastic, flexible peptidoglycan and bacterial cell wall properties. Trends Microbiol. 2:57-60.
16. Epstein, W., and S. G. Schultz. 1965. Cation transport in Escherichia coli. V. Regulation of cation content. J. Gen. Phys. 49:221-234.
17. Guttman, H. J., C. F. Anderson, and M. T. Record, Jr. 1995. Analyses of thermodynamic data for concentrated hemoglobin solutions using scaled particle theory: implications for a simple two-state model of water in thermodynamic analyses of crowding in vitro and in vivo. Biophys. J. 68:835-846.
18. Hengge-Aronis, R., W. Klein, R. Lange, M. Rimmele, and W. Boos. 1991. 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. 173:7918-7924.
19. Höltje, J.-V. 1998. Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol. Molec. Biol. Rev. 62: 181-203.
20. Jacobson, K., and J. Wojcieszyn. 1984. The translational mobility of substances within the cytoplasmic matrix. Proc. Natl. Acad. Sci. USA. 81:6747-6751.
21. Johnson, M. L., and S. G. Frasier. 1985. Nonlinear least-squares analysis. Methods Enzymol. 117:301-342.
22. Kennedy, E. P. 1996. Membrane-derived oligosaccharides (periplasmic beta-D-glucans) of Escherichia coli. In Escherichia coli and Salmonella Cellular and Molecular Biology. F. C. Neidhardt, R. Curtis, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaecter, and H. E. Umbarger, editors. 2nd Ed. ASM Press, Washington, DC. 1064-1071.
23. Kennedy, E. P. 1982. Osmotic regulation and the biosynthesis of membrane-derived oligosaccharide in Escherichia coli. Proc. Natl. Acad. Sci. USA. 79:1092-1095.
24. Kennedy, E. P., and M. K. Rumley. 1988. Osmotic regulation of biosynthesis of membrane-derived oligosaccharides in Escherichia coli. J. Bacteriol. 170:2457-2461.
25. Kinsman, R., B. W. Ibelings, and A. E. Walsby. 1991. Gas vesicle collapse by turgor pressure and its role in buoyancy regulation by Anabaena flos-aquae. J. Gen. Microbiol. 137:1171-1178.
26. Koch, A. L. 1995. The geometry and osmotic relation of plasmolysis spaces in bacteria and the role of endocytosis, tubular structures and Scheie structures in their formation. J. Theor. Biol. 176:471-492.
27. Koch, A. L. 1998. The biophysics of the gram-negative periplasmic space. Crit. Rev. Microbiol. 24:23-59.
28. Koch, A. L., and M. F. S. Pinette. 1987. Nephelometric determination of turgor pressure in growing gram-negative bacteria. J. Bacteriol. 169: 3654-3663.
29. Koch, A. L., and S. Woeste. 1992. Elasticity of the sacculus of Escherichia coli. J. Bacteriol. 174:4811-4819.
30. Labischinski, H., and H. Maidhof, 1994. Bacterial peptidoglycan: overview and evolving concepts. In Bacterial Cell Wall. J.-M. Ghuysen and R. Hakenbech, editors. Elsevier Science, Amsterdam. 23-38.
31. Lacroix, J.-M., M. Tempete, B. Menichi, and J.-P. Bohin. 1989. Molecular cloning and expression of a locus (mdoA) implicated in the biosynthesis of membrane-derived oligosaccharides in Escherichia coli. Mol. Microbiol. 3:1173-1182.
32. Laimins, L. A., D. B. Rhodes, and W. Epstein. 1981. Osmotic control of kdp operon expression in Escherichia coli. Proc. Natl. Acad. Sci. USA. 78:464-468.
33. Larsen, P. I., L. K. Sydnes, B. Landfald, and A. R. Strøm. 1987. Osmoregulation in Escherichia coli by accumulation of organic osmolytes: betaines, glutamic acid, and trehalose. Arch. Microbiol. 147:1-7.
34. Li, N., and M. C. Cannon. 1998. Gas vesicle genes identified in Bacillus megaterium and functional expression in Escherichia coli. J. Bacteriol. 180:2450-2458.
35. Lowry, O. H., N. J. Rosebrough, A. L. Farr, and R. J. Randall. 1951. Protein measurements with the Folin phenol reagent. J. Biol. Chem. 193:265-275.
36. Malli, R., and W. Epstein. 1998. Expression of the Kdp ATPase is consistent with regulation by turgor pressure. J. Bacteriol. 180:5102-5108.
37. McLaggan, D., and W. Epstein. 1991. Escherichia coli accumulates the eukaryotic osmolyte taurine at high osmolality. FEMS Microbiol. Lett. 81:209-214.
38. McLaggan, D., T. M. Logan, D. G. Lynn, and W. Epstein. 1990. Involvement of γ-glutamyl peptides in osmoadaptation of Escherichia coli. J. Bacteriol. 172:3631-3636.
39. Meury, J. 1994. Immediate and transient inhibition of the respiration of Escherichia coli under hyperosmotic shock. FEMS Microbiol. Lett. 121:281-286.
40. Mitchell, P., and J. Moyle. 1956. Osmotic function and structure in bacteria. In Bacterial Anatomy. Symposia of the Society for General Microbiology. Cambridge University Press, Cambridge, MA. 150-180.
41. Money, N. 1997. Wishful thinking of turgor revisited: the mechanics of fungal growth. Fungal Genet. Biol. 21:173-187.
42. Neidhardt, F. C., J. L. Ingraham, and M. Schaechter. 1990. Physiology of the Bacterial Cell: A Molecular Approach. Sinauer Associates, Inc., Sunderland, MA. 8.
43. Phillip, J. R. 1958. The osmotic cell, solute diffusibility, and the plant water economy. Plant. Physiol. 33:264-271.
44. Record, M. T., Jr., E. S. Courtenay, D. S. Cayley, and H. J. Guttman. 1998a. Responses of E. coli to osmotic stress: large changes in amounts of cytoplasmic solutes and water. Trends Biochem. Sci. 23:144-149.
45. Record, M. T., Jr., E. S. Courtenay, D. S. Cayley, and H. J. Guttman. 1998b. Biophysical compensation mechanisms buffering E. coli protein-nucleic acid interactions against changing environments. Trends Biochem. Sci. 23:190-194.
46. Reed, R. H., and A. E. Walsby. 1985. Changes in turgor pressure in response to increases in external NaCl concentration in the gas-vacuolate cyanobacterium Microcystis sp. Arch. Microbiol. 143:290-296.
47. Richey, B., D. S. Cayley, M. C. Mossing, C. Kolka, C. F. Anderson, T. C. Farrar, and M. T. Record, Jr. 1987. Variability of the intracellular ionic environment of Escherichia coli: differences between in vitro and in vivo effects of ion concentrations on protein-DNA interactions and gene expression. J. Biol. Chem. 262:7157-7164.
48. Robinson, R. A., and R. H. Stokes. 1959. Electrolyte Solutions. Academic Press, New York. 476.
49. Rumley, M. K., H. Therisod, A. C. Weissborn, and E. P. Kennedy. 1992. Mechanisms of regulation of the biosynthesis of membrane-derived oligosaccharides in Escherichia coli. J. Biol. Chem. 267:11806-11810.
50. Sen, K., J. Hellman, and H. Nikaido. 1988. Porin channels in intact cells of Escherichia coli are not affected by Donnan potentials across the outer membrane. J. Biol. Chem. 263:1182-1187.
51. Schwarz, H., and A. L. Koch. 1995. Phase and electron microscopic observations of osmotically induced wrinkling and the role of endocytotic vesicles in the plasmolysis of the Gram-negative cell wall. Microbiology. 141:3161-3170.
52. Stock, J. B., B. Rauch, and S. Roseman. 1977. Periplasmic space in Salmonella typhimurium and Escherichia coli. J. Biol. Chem. 252: 7850-7861.
53. Straume, M., S. G. Frasier-Cadoret, and M. L. Johnson. 1991. Least-squares analysis of fluorescence data. In Topics in Fluorescence Spectroscopy. R. J. Lakowicz, editor. Plenum Press, New York. 177-240.
54. Vinckier, A., and G. Semenza. 1998. Measuring elasticity of biological materials by atomic force microscopy. FEBS Lett. 430:12-16.
55. Walsby, A. E. 1980. The water relations of gas-vacuolate prokaryotes. Proc. K. Soc. Lond. B. 208:73-102.
56. Woldringh, C. L. 1994. Significance of plasmolysis spaces as markers for periseptal annuli and adhesion sites. Mol. Microbiol. 14:597-607.
57. Wood, J. M. 1999. Osmosensing by bacteria: signals and membrane-based sensors. Microbiol. Mol. Biol. Rev. 63:230-262.
58. Zhu, G. L., and J. S. Boyer. 1992. Enlargement in Chara studied with a turgor clamp. Plant Physiol. 100:2071-2080.
59. Zimmermann, U. 1978. Physics of turgor-and osmoregulation. Annu. Rev. Plant Physiol. 29:121-148.