1887

Abstract

The amount of major proteins per unit of surface area in the outer membrane (OM) of LT2 remained constant during steady-state growth in different media. Between growth rates of 2·40 doublings h and 0·31 doublings h, the surface density of major OM proteins varied between 0·9 × 10 and 1·2 × 10 molecules per m, while surface area per cell more than halved. The accumulation of molecules of the major OM proteins was not affected by addition of cyclic AMP to the growth medium. When exponentially growing cells were subjected to shift-up transitions, cell dimensions began to increase after a lag period of 20 min. Accumulation of major OM proteins followed the same pattern as total protein; this created a transitory imbalance of major OM protein density in the shift from acetate minimal medium to LB medium, before the steady situation was reached. After shift-down transitions, cell dimensions began to decrease immediately, cells eventually becoming shorter than in steady-state conditions. No fluctuations in major OM protein density were observed during the shift-down, although final stable levels differed from those in steady-state conditions. All these results indicate that bacteria adapt the accumulation of major proteins into the OM according to the amount of surface. Thus, no large differences exist at different cell sizes, although transitions between media can lead to transitory or stable changes in the composition of the OM.

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1980-10-01
2021-05-07
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References

  1. Alderman E. M., Dills S. S., Melton T., Dobrogosz W. J. 1979; Cyclic adenosine 3′,5′- monophosphate regulation of the bacteriophage T6/colicin K receptor of Escherichia coli. . Journal of Bacteriology 140:369–376
    [Google Scholar]
  2. Alphen W.van, Lugtenberg B. 1977; Influence of osmolarity of the growth medium on the outer membrane protein pattern of Escherichia coli. . Journal of Bacteriology 131:623–630
    [Google Scholar]
  3. Ames G. F., Nikaido H. 1976; Two-dimensional gel electrophoresis of membrane proteins. Biochemistry 15:616–623
    [Google Scholar]
  4. Ames G. F., Spudich E. N., Nikaido H. 1974; Protein composition of the outer membrane of Salmonella typhimurium: effect of lipopoly- saccharide mutations. Journal of Bacteriology 117:406–416
    [Google Scholar]
  5. Aono R., Yamasaki M., Tamura G. 1978; Changes in composition of envelope proteins in adenylate cyclase- or cyclic AMP receptor protein-deficient mutants of Escherichia coli. . Journal of Bacteriology 136:812–814
    [Google Scholar]
  6. Bassford P. J. Jr Diedrich D. L., Schnaitman C. L., Reeves P. 1977; Outer membrane proteins of Escherichia coli. VI. Protein alteration in bacteriophage-resistant mutants. Journal of Bacteriology 131:608–622
    [Google Scholar]
  7. Boyd A., Holland I. B. 1979; Regulation of the synthesis of surface protein in the cell cycle of E. coli B/r. Cell 18:287–296
    [Google Scholar]
  8. Bremer H., Dennis P. P. 1975; Transition period following a nutritional shift-up in the bacterium Escherichia coli B/r: stable RNA and protein synthesis. Journal of Theoretical Biology 52:365–382
    [Google Scholar]
  9. Clark D. J., Maaløe O. 1967; DNA replication and the division cycle in Escherichia coli. . Journal of Molecular Biology 23:99–112
    [Google Scholar]
  10. Cronan J. E. Jr Vagelos P. R. 1972; Metabolism and function of the membrane phospholipids of Escherichia coli. . Biochimica et biophysica acta 265:25–60
    [Google Scholar]
  11. Datta D. B., Kramer C., Henning U. 1976; Diploidy for a structural gene specifying a major protein of the outer cell envelope membrane from Escherichia coli K-12. Journal of Bacteriology 128:834–841
    [Google Scholar]
  12. Decad G. M., Nikaido H. 1976; Outer membrane of gram-negative bacteria. XII. Molecular sieving function of cell wall. Journal of Bacteriology 128:325–336
    [Google Scholar]
  13. Dennis P. P., Bremer H. 1974; Macromolecular composition during steady-state growth of Escherichia coli B/r. Journal of Bacteriology 119:270–281
    [Google Scholar]
  14. Dirienzo J. M., Nakamura K., Inouye M. 1978; The outer membrane proteins of gramnegative bacteria: biosynthesis, assembly and functions. Annual Review of Biochemistry 47:481–532
    [Google Scholar]
  15. Donachie W. D., Begg K. J., Vicente M. 1976; Cell length, cell growth and cell division. Nature London: 264:328–333
    [Google Scholar]
  16. Filip C., Fletcher G., Wulff J. L., Earhart C. F. 1973; Solubilization of the cytoplasmic membrane of Escherichia coli by the ionic detergent sodium lauryl sarcosinate. Journal of Bacteriology 115:717–722
    [Google Scholar]
  17. Gmeiner J., Schlecht S. 1979; Molecular organization of the outer membrane of Salmonella typhimurium. . European Journal of Biochemistry 93:609–620
    [Google Scholar]
  18. Grover N. B., Woldringh C. L., Zaritsky A., Rosenberger R. F. 1977; Elongation of rodshaped bacteria. Journal of Theoretical Biology 67:181–193
    [Google Scholar]
  19. Henning U., Hindennach I., Haller I. 1976; The major proteins of the Escherichia coli outer cell envelope membrane: evidence for the structural gene of protein II*. FEBS Letters 61:46–48
    [Google Scholar]
  20. Henning U., Schmidmayr W., Hindennach I. 1977; Major proteins of the outer cell envelope of Escherichia coli K-12: multiple species of protein I. Molecular and General Genetics 154:293–298
    [Google Scholar]
  21. Kamio Y., Nikaido H. 1977; Outer membrane of Salmonella typhimurium: identification of proteins exposed on cell surface. Biochimica et biophysica acta 464:589–601
    [Google Scholar]
  22. Kubitschek H. E. 1974; Constancy in the ratio of DNA to cell volume in steady state growth of E. coli B/r. Biophysical Journal 14:119–123
    [Google Scholar]
  23. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature London: 227:680–685
    [Google Scholar]
  24. Lee D. R., Schnaitman C. A., Pugsley A. P. 1979; Chemical heterogeneity of major outer membrane pore proteins of Escherichia coli. . Journal of Bacteriology 138:861–870
    [Google Scholar]
  25. Loeb A., McGrath B. E., Navre J. M., Pierucci O. 1978; Cell division during nutritional upshifts of Escherichia coli. . Journal of Bacteriology 136:631–637
    [Google Scholar]
  26. Lugtenberg B., Meijers J., Peters R., Hoek P.Van Der, Alphen L. van. 1975; Electrophoretic resolution of the “major outer membrane protein” of Escherichia coii K12 into four bands. FEBS Letters 58:254–258
    [Google Scholar]
  27. Lugtenberg B., Peters R., Bernheimer H., Berendsen W. 1976; Influence of cultural conditions and mutations on the composition of the outer membrane proteins of Escherichia coli. . Molecular and General Genetics 147:251–262
    [Google Scholar]
  28. Maaløe O., Kjeldgaard N. O. 1966 Control of Macromolecular Synthesis. New York:: Benjamin.;
    [Google Scholar]
  29. Manning P. A., Puspurs A., Reeves P. 1976; Outer membrane of Escherichia coli K-12: isolation of mutants with altered protein 3A by using host range mutants of bacteriophage K3. Journal of Bacteriology 127:1080–1084
    [Google Scholar]
  30. Muhlradt P. F., Menzel J., Goleck J. R., Speth V. 1974; Lateral mobility and surface density of lipopolysaccharide in the outer membrane of Salmonella typhimurium. . European Journal of Biochemistry 43:533–539
    [Google Scholar]
  31. Nakae T. 1976; Outer membrane of Salmonella.Isolation of protein complex that produces transmembrane channels. Journal of Biological Chemistry 251:2176–2178
    [Google Scholar]
  32. Nikaido H., Nakae T. 1979; The outer membrane of gram-negative bacteria. Advances in Microbial Physiology 20:164–250
    [Google Scholar]
  33. Palva E. T. 1979; Protein interactions in the outer membrane of Escherichia coli. . European Journal of Biochemistry 93:495–503
    [Google Scholar]
  34. Pedersen S., Bloch P. L., Reeh S., Neidhardt F. 1978; Patterns of protein synthesis in Escherichia coli: a catalogue of the amount of 140 individual proteins at different growth rates. Cell 14:179–190
    [Google Scholar]
  35. Pierucci O. 1978; Dimensions of Escherichia coliat various growth rates: model for envelope growth. Journal of Bacteriology 135:559–574
    [Google Scholar]
  36. Pritchard R. H. 1974; On the growth and form of a bacterial cell. Philosophical Transactions of the Royal Society B267:303–336
    [Google Scholar]
  37. Rosenberger R. F., Grover N. B., Zaritsky A., Woldringh C. L. 1978; Control of microbial surface by density. Nature London: 271:244–245
    [Google Scholar]
  38. Rosenbusch J. P. 1974; Characterization of the major envelope protein from Escherichia coli.Regular arrangement on the peptidoglycan and unusual dodecyl sulphate binding. Journal of Biological Chemistry 249:8019–8029
    [Google Scholar]
  39. Sato T., Yura T. 1979; Chromosomal location and expression of the structural gene for major outer membrane proteins la of Escherichia coliK-12 and of the homologous gene of Salmonella typhimurium. . Journal of Bacteriology 139:468–477
    [Google Scholar]
  40. Schaechter M., Maaløe O., Kjeldgaard N. O. 1958; Dependency on medium and temperature of cell size and chemical composition during balanced growth of Salmonella typhimurium. . Journal of General Microbiology 19:592–606
    [Google Scholar]
  41. Schmitges C. J., Henning U. 1976; The major proteins of the Escherichia coli outer cell-envelope membrane. Heterogeneity of protein I. European Journal of Biochemistry 63:47–52
    [Google Scholar]
  42. Schnaitman C. 1970; Protein composition of the cell wall and cytoplasmic membrane of Escherichia coli. . Journal of Bacteriology 104:890–901
    [Google Scholar]
  43. Sekizawa J., Inouye S., Halegoua S., Inouye M. 1977; Precursors of major outer membrane proteins of Escherichia coli. . Biochemical and Biophysical Research Communications 77:1126–1133
    [Google Scholar]
  44. Shen V., Bremer H. 1977; Chloramphenicol- induced changes in the synthesis of ribosomal, transfer and messenger ribonucleic acids in Escherichia coli B/r. Journal of Bacteriology 130:1098–1108
    [Google Scholar]
  45. Sloan J. B., Urban J. E. 1976; Growth response of Escherichia coli to nutritional shift-up: immediate division stimulation in slow-growing cells. Journal of Bacteriology 128:302–308
    [Google Scholar]
  46. Smit J., Kamio Y., Nikaido H. 1975; Outer membrane of Salmonella typhimurium: chemical analysis and freeze-fracture studies with lipopoly- saccharide mutants. Journal of Bacteriology 124:942–958
    [Google Scholar]
  47. Steven A. C., Ten Heggeler B., Muller R., Kistler J., Rosenbusch J. P. 1977; Ultrastructure of a periodic protein layer in the outer membrane of Escherichia coli. . Journal of Cell Biology 72:292–301
    [Google Scholar]
  48. Verhoeff C., Lugtenberg B., Boxtel R. van, de Graff P., Verheij J. 1979; Genetics and biochemistry of the peptidoglycan-associated proteins b and c of Escherichia coli K12. Molecular and General Genetics 169:137–146
    [Google Scholar]
  49. Zaritsky A., Woldringh C. L., Mirelman D. 1979; Constant peptidoglycan density in the sacculus of Escherichia coli B/r growing at different rates. FEBS Letters 98:29–32
    [Google Scholar]
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