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Deformations in the Cytoplasmic Membrane of Escherichia coli Direct the Repair of Peptidoglycan

  • Vic Norris
  • Sean Sweeney
Part of the Federation of European Microbiological Societies Symposium Series book series (FEMS, volume 65)

Abstract

Turgor pressures of 3.5 Atmospheres in Gram negative bacteria (Stock et al., 1977) and up to 20 Atmospheres in Gram positive bacteria (Mitchell and Moyle, 1956) mean that the weakening of any region of the force-bearing element of the bacterial wall, peptidoglycan, may result in lysis. A repair mechanism to strengthen such regions preferentially may therefore exist. In this communication, a model is proposed in which this mechanism involves local changes in the structure and composition of the cytoplasmic membrane, the requirements of the model are listed and supporting evidence and predictions are discussed.

Keywords

Cytoplasmic Membrane Turgor Pressure Phospholipid Composition Micrococcus Luteus Amidase Activity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Amako, K., Murata, K. and Umeda, A. 1983 Structure of the envelope of Escherichia coli observed by rapid-freezing and substitution fixation method. Microbiol. Immunol. 27, 95–99.PubMedGoogle Scholar
  2. Ames, G.F. 1968 Lipids of Salmonella typhimurium and Escherichia coli: structure and metabolism. J.Bacteriol. 95, 833–843.PubMedGoogle Scholar
  3. Barbas, J. A., Diaz, J., Rodriguez-Tebar, A. and Vasquez, D. 1986 Specific location of penicillin-binding proteins within the cell envelope of Escherichia coli. J. Bacteriol. 165, 269–275.PubMedGoogle Scholar
  4. Bayer, M. H., Costello, G. P. and Bayer, M. E. 1982 Isolation and partial characterization of membrane vesicles carrying markers of the membrane adhesion sites. J. Bacteriol. 149, 758–767.PubMedGoogle Scholar
  5. Bayer, M. H., Keck, W. and Bayer, M. E. 1990 Localization of penicillin-binding protein lb in Escherichia coli: immunoelectron microscopy and immunotransfer studies. J. Bacteriol. 172, 125–135.PubMedGoogle Scholar
  6. Braun, V., Gnirke. H., Henning, U. and Rehn, K. 1973 Model for the structure of the shape-maintaining layer of the Escherichia coli envelope. J. Bacteriol. 114, 1264–1270.PubMedGoogle Scholar
  7. Burdett, I.D.J. and Murray, R.G.E. 1974 Electron microscope study of septum formation in Escherichia coli strains B and B/r during synchronous growth. J. Bacteriol. 119, 1039–1056.PubMedGoogle Scholar
  8. Burman, L.G. and Park, J.T. 1984 Molecular model for elongation of the murein sacculus of Escherichia coli. Proc. Natl. Acad. Sci. USA 81, 1844–1848.PubMedCrossRefGoogle Scholar
  9. Cooper, S. (1991) Synthesis of the cell surface during the division cycle of rod-shaped, gram-negative bacteria. Microbiol. Rev. 55, 649–674.PubMedGoogle Scholar
  10. Cooper, S., Hsieh, M.-L. and Guenther, B. 1988 Mode of peptidoglycan synthesis in Salmonella typhimurium: single-strand insertion. J. Bacteriol. 170, 3509–3512.PubMedGoogle Scholar
  11. Cronan, J.E. and Vagelos, P.R. 1972 Metabolism and function of the membrane phospholipids of Escherichia coli. Biochim. Biophys. Acta 265, 25–60.PubMedCrossRefGoogle Scholar
  12. Cullis, P.R. and de Kruijff, B. 1979 Lipid polymorphism and the functional roles of lipids in biological membranes. Biochim. Biophys. Acta 559, 399–420.PubMedCrossRefGoogle Scholar
  13. De Jonge, B.L.M., Wientjes, F.B., Jurida, I., Driehuis, F., Wouters, J.T.M. and Nanninga, N. 1989 Peptidoglycan synthesis during the cell cycle of Escherichia coli: composition and mode of insertion. J. Bacteriol. 171, 5783–5794.PubMedGoogle Scholar
  14. Dubochet, J., McDowall, A.W., Menge, B., Schmid, E.N. and Lickfeld, K.G. 1983 Electron microscopy of frozen-hydrated bacteria. J. Bacteriol. 155, 381–390.PubMedGoogle Scholar
  15. Edidin, M. 1987 Rotational and lateral diffusion of membrane proteins and lipids: phenomena and function. Curr. Top. Membr. Trans. 29, 91–127.CrossRefGoogle Scholar
  16. Geis, A. and Plapp, R. 1978 Phospho-iV-Acetylmuramoyl-pentapeptide-tranferase of Escherichia coli K12: properties of the membrane-bound and the extracted and partially purified enzyme. Biochim. Biophys. Acta 527, 414–424.PubMedCrossRefGoogle Scholar
  17. Gennis, R.B. and Strominger, J.L. 1976. Activation of C55-isoprenoid alcohol phosphokinase from Staphylococcus aureus. J. Biol. Chem. 251, 1264–1269.PubMedGoogle Scholar
  18. Glauner, B., Holtje, J.-V. and Schwartz, U. 1988 The composition of the murein of Escherichia coli. J. Biol. Chem. 263, 10088–10095.PubMedGoogle Scholar
  19. Goldfine, H. 1982. Lipids of prokaryotes — structure and distribution. In Curr. Top. Membr. Trans. Razin, S. and Rottem, S., editors. Academic Press, 1-43.Google Scholar
  20. Grüner, S.M. 1985. Intrinsic curvature hypothesis for biomembrane lipid composition: a role for nonbilayer lipids. Proc. Nat. Acad. Sci. USA 82, 3665–3669.PubMedCrossRefGoogle Scholar
  21. Haverstick, D.M. and Glaser, M. 1989 Influence of proteins on the reorganization of phospholipid bilayers into large domains. Biophys. J. 55, 677–682.PubMedCrossRefGoogle Scholar
  22. Higashi, Y. and Strominger, J.L. 1970 Biosynthesis of the peptidoglycan of bacterial cell walls: identification of phosphatidylglycerol and cardiolipin as cofactors for isoprenoid alcohol phosphokinase. J. Biol. Chem. 245, 3691–3696.PubMedGoogle Scholar
  23. Hobot, J.A., Carlemalm. E., Villiger, W. and Kellenberger, E. 1984 Periplasmic gel: new concept resulting from the reinvestigation of bacterial cell envelope ultrastructure by new methods. J. Bacteriol. 160, 143–152.PubMedGoogle Scholar
  24. Holtje, J.-V. and Glauner, B. 1990 Structure and metabolism of the murein sacculus. Res. Microbiol. 141, 75–89.PubMedCrossRefGoogle Scholar
  25. Israelachvili, J.N., Marcelja, S. and Horn, R.G. 1980 Physical principles of membrane organization. Quart. Rev. Biophys. 13, 121–200.CrossRefGoogle Scholar
  26. Kellenberger, E. 1990 The “Bayer bridges” confronted with results from improved electron microscopy methods. Mol. Microbiol. 4, 697–705.PubMedCrossRefGoogle Scholar
  27. Kennedy, E.P. 1982 Osmotic regulation and the biosynthesis of membrane-derived oligosacchides in Escherichia coli. Proc. Natl. Acad. Sci. USA 79, 1092–1095.PubMedCrossRefGoogle Scholar
  28. Koch, A.L. 1983 The surface stress theory of microbial morphogenesis. Advances Microbiol. Physiol. 24, 301–366.CrossRefGoogle Scholar
  29. Koch, A. L. 1990 Additional arguments for the key role of “smart” autolysins in the enlargement of the wall of Gram-negative bacteria. Res. Microbiol. 141, 529–541.PubMedCrossRefGoogle Scholar
  30. Labischinski, H. Goodell, E.W., Goodell, A. and Hochberg, M.L. 1991 Direct proof of a “more-than-single-layered” peptidoglycan architecture of Escherichia coli W7: a neutron small-angle scattering study. J. Bacteriol. 173, 751–756.PubMedGoogle Scholar
  31. Leduc, M., Frehel, C. and van Heijenoort, J. 1985 Correlation between degradation and ultrastructure of peptidoglycan during autolysis of Escherichia coli. J. Bacteriol. 161, 627–635.PubMedGoogle Scholar
  32. Lee, P.P., Weppner, W.A. and Neuhaus, F.C. 1980 Initial membrane reaction in peptidoglycan synthesis: perturbation of lipid-phospho-Af-acetylmuramyl-pentapeptide translocase interactions by n-butanol. Biochim. Biophys. Acta 597, 603–613.PubMedCrossRefGoogle Scholar
  33. Leidenix, M. J., Jacoby, G. H., Henderson, T. A. and Young, K. D. 1989 Separation of Escherichia coli penicillin-binding proteins into different membrane vesicles by agarose electrophoresis and sizing chromatography. J. Bacteriol. 171, 5680–5686.PubMedGoogle Scholar
  34. Lindblom, G. and Rifors, L. 1989 Cubic phases and isotropic structures formed by membrane lipids — possible biological relevance. Biochim. Biophys. Acta 988, 221–256.CrossRefGoogle Scholar
  35. Matsuhashi, M. Dietrich, C.P. and Strominger, J.L. 1967 Biosynthesis of the peptidoglycan of bacterial cell walls: III the role of soluble ribonucleic acid and of lipid intermediates in glycine incorporation in Staphylococcus aureus. J. Biol. Chem. 242, 3191–3206.Google Scholar
  36. Matsuhashi, M., Wachi, M. and Ishino, F. 1990 Machinery for cell growth and division: penicillin-binding proteins and other proteins. Res. Microbiol. 141, 89–103.PubMedCrossRefGoogle Scholar
  37. Mitchell, P. and Moyle, J. 1956 Osmotic structure and function in bacteria. Symp. Soc. Gen. Microbiol. 6, 150–180.Google Scholar
  38. Nords, V. 1989 Phospholipid flip-out controls the cell cycle of Escherichia coli. J. Theor. Biol. 139, 117–128.CrossRefGoogle Scholar
  39. Norris, V. 1990 DNA replication in Escherichia coli is initiated by membrane detachment of oriC. J. Mol. Biol. 215, 67–71.PubMedCrossRefGoogle Scholar
  40. Norris, V. 1992 Phospholipid domains determine the spatial organization of the E.coli cell cycle: the membrane tectonics model. J. Theor. Biol., 154, 91–107.PubMedCrossRefGoogle Scholar
  41. Park, J.T. 1987. Murein synthesis In Escherichia coli and Salmonella typhimurium. F.C. Neidhardt editor. ASM, Washington, D.C. 663–671.Google Scholar
  42. Pinette, M.F.S. and Koch, A.L. 1987 The stress in the Gram-negative wall is constant throughout the cell cycle of Ancyclobacter aquaticus. J. Bacteriol. 169, 4737–4742.PubMedGoogle Scholar
  43. Raetz, C.R.H. and Dowhan, W. 1990 Biosynthesis and function of phospholipids in Escherichia coli. J. Biol. Chem. 265, 1235–1238.PubMedGoogle Scholar
  44. Rand, R.P. and Parsegian, V.A. 1986 Mimicry and mechanism in phospholipid models of membrane fusion. Ann. Rev. Physiol. 48, 201–212.CrossRefGoogle Scholar
  45. Rodgers, W. and Glaser, M. 1991 Characterization of lipid domains in erythrocyte membranes. Proc. Natl. Acad. Sci. USA. 88, 1364–1368.PubMedCrossRefGoogle Scholar
  46. Rogers, H.J., Perkins, H.R. and Ward, J.B. 1980. Microbial cell walls and membranes. Chapman and Hall, London.CrossRefGoogle Scholar
  47. Spratt, B. G. 1975 Distinct penicillin binding proteins involved in the division, elongation, and shape of Escherichia coli K12. Proc. Natl. Acad. Sci. USA. 72, 2999–3003.PubMedCrossRefGoogle Scholar
  48. Stock, J.B., Rauch, B. and Roseman, S. 1977 Periplasmic space in Salmonella typhimurium and Escherichia coli. J. Biol. Chem. 252, 7850–7861.PubMedGoogle Scholar
  49. Taku, A. and Fan, D.P. 1976 Identification of an isolated protein essential for peptidoglycan synthesis as the Af-acetylglucosaminyltransferase. J. Biol. Chem. 251, 6154–6156.PubMedGoogle Scholar
  50. Tocanne, J.-F, Dupou-Cezanne, L., Lopez, A. and Tournier, J-F. 1989 Lipid lateral diffusion and membrane organization. FEBS Lett. 257, 10–16.PubMedCrossRefGoogle Scholar
  51. Umbreit, J.N. and Strominger, J.L. 1972a. Isolation of polyisoprenyl alcohols from Streptococcus faecalis. J. Bacteriol. 112, 1302–1305.PubMedGoogle Scholar
  52. Umbreit, J.N. and Strominger, J.L. 1972b. Complex lipid requirements for detergentsolubilized phosphoacetylmuramyl-pentapeptide translocase from Micrococcus luteus. Proc. Natl. Acad. Sci. USA. 69, 1972–1974.PubMedCrossRefGoogle Scholar
  53. Vanderwinkel, E. and de Vlieghere, M. 1985 Modulation of Escherichia coli N-acetylmuramyl-L-alanine amidase activity by phosphatidylglycerol. Biochim. Biophys. Acta 838, 54–59.PubMedCrossRefGoogle Scholar
  54. Vaz, W.L.C., Melo, E.C.C. and Thompson, T.E. 1989 Translational diffusion and fluid domain connectivity in a two-component, two-phase phospholipid bilayer. Biophys. J. 56, 869–876.PubMedCrossRefGoogle Scholar
  55. Walker, J. M., Homan, E. C. and Sando, J. J. 1990 Differential activation of protein kinase C isozymes by short chain phosphatidylserines and phosphatidylcholines J. Biol. Chem. 265, 8016–8021.Google Scholar
  56. Weppner, W.A. and Neuhaus, F.C. 1978 Biosynthesis of peptidoglycan: definition of the microenvironment of undecaprenyl diphosphate-V-acetylmuramyl-(5-dimethyl-amino-naphthalene-1-sulfonyl) pentapeptide by fluorescence spectroscopy. J. Biol. Chem. 253, 472–478.PubMedGoogle Scholar
  57. Weppner, W.A. and Neuhaus, F.C. 1979 Initial membrane reaction in peptidoglycan synthesis: interaction of lipid with phospho-N-acetylmuramyl-pentapeptide translocase. Biochim. Biophys. Acta 552, 418–427.PubMedCrossRefGoogle Scholar
  58. Zachowski, A. and Devaux, P.F. 1990 Transmembrane movements of lipids. Experientia 46, 645–656.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1993

Authors and Affiliations

  • Vic Norris
    • 1
  • Sean Sweeney
    • 1
  1. 1.Department of GeneticsUniversity of LeicesterLeicesterUK

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