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. 1997 May;179(9):2823–2834. doi: 10.1128/jb.179.9.2823-2834.1997

Murein segregation in Escherichia coli.

M A de Pedro 1, J C Quintela 1, J V Höltje 1, H Schwarz 1
PMCID: PMC179041  PMID: 9139895

Abstract

Peptidoglycan (murein) segregation has been studied by means of a new labeling method. The method relies on the ability of Escherichia coli cells to incorporate D-Cys into macromolecular murein. The incorporation depends on a periplasmic amino acid exchange reaction. At low concentrations, D-Cys is innocuous to the cell. The distribution of modified murein in purified sacculi can be traced and visualized by immunodetection of the -SH groups by fluorescence and electron microscopy techniques. Analysis of murein segregation in wild-type and cell division mutant strains revealed that murein in polar caps is metabolically inert and is segregated in a conservative fashion. Elongation of the sacculus apparently occurs by diffuse insertion of precursors over the cylindrical part of the cell surface. At the initiation of cell division, there is a FtsZ-dependent localized activation of murein synthesis at the potential division sites. Penicillin-binding protein 3 and the products of the division genes ftsA and ftsQ are dispensable for the activation of division sites. As a consequence, under restrictive conditions ftsA,ftsI,or ftsQ mutants generate filamentous sacculi with rings of all-new murein at the positions where septa would otherwise develop.

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Selected References

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  1. Begg K. J., Donachie W. D. Cell shape and division in Escherichia coli: experiments with shape and division mutants. J Bacteriol. 1985 Aug;163(2):615–622. doi: 10.1128/jb.163.2.615-622.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bi E., Lutkenhaus J. FtsZ regulates frequency of cell division in Escherichia coli. J Bacteriol. 1990 May;172(5):2765–2768. doi: 10.1128/jb.172.5.2765-2768.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Burman L. G., Park J. T. Molecular model for elongation of the murein sacculus of Escherichia coli. Proc Natl Acad Sci U S A. 1984 Mar;81(6):1844–1848. doi: 10.1073/pnas.81.6.1844. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Burman L. G., Raichler J., Park J. T. Evidence for diffuse growth of the cylindrical portion of the Escherichia coli murein sacculus. J Bacteriol. 1983 Sep;155(3):983–988. doi: 10.1128/jb.155.3.983-988.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Caparrós M., Arán V., de Pedro M. A. Incorporation of S-[3H]methyl-D-cysteine into the peptidoglycan of ether-treated cells of Escherichia coli. FEMS Microbiol Lett. 1992 Jun 1;72(2):139–146. doi: 10.1016/0378-1097(92)90519-t. [DOI] [PubMed] [Google Scholar]
  6. Caparrós M., Pisabarro A. G., de Pedro M. A. Effect of D-amino acids on structure and synthesis of peptidoglycan in Escherichia coli. J Bacteriol. 1992 Sep;174(17):5549–5559. doi: 10.1128/jb.174.17.5549-5559.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Caparrós M., Torrecuadrada J. L., de Pedro M. A. Effect of D-amino acids on Escherichia coli strains with impaired penicillin-binding proteins. Res Microbiol. 1991 Feb-Apr;142(2-3):345–350. doi: 10.1016/0923-2508(91)90050-k. [DOI] [PubMed] [Google Scholar]
  8. Cook W. R., Rothfield L. I. Early stages in development of the Escherichia coli cell-division site. Mol Microbiol. 1994 Nov;14(3):485–495. doi: 10.1111/j.1365-2958.1994.tb02183.x. [DOI] [PubMed] [Google Scholar]
  9. Dai K., Lutkenhaus J. The proper ratio of FtsZ to FtsA is required for cell division to occur in Escherichia coli. J Bacteriol. 1992 Oct;174(19):6145–6151. doi: 10.1128/jb.174.19.6145-6151.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Donachie W. D., Begg K. J., Vicente M. Cell length, cell growth and cell division. Nature. 1976 Nov 25;264(5584):328–333. doi: 10.1038/264328a0. [DOI] [PubMed] [Google Scholar]
  11. Donachie W. D. Relationship between cell size and time of initiation of DNA replication. Nature. 1968 Sep 7;219(5158):1077–1079. doi: 10.1038/2191077a0. [DOI] [PubMed] [Google Scholar]
  12. García del Portillo F., de Pedro M. A. Differential effect of mutational impairment of penicillin-binding proteins 1A and 1B on Escherichia coli strains harboring thermosensitive mutations in the cell division genes ftsA, ftsQ, ftsZ, and pbpB. J Bacteriol. 1990 Oct;172(10):5863–5870. doi: 10.1128/jb.172.10.5863-5870.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Georgopapadakou N. H., Smith S. A., Sykes R. B. Mode of action of azthreonam. Antimicrob Agents Chemother. 1982 Jun;21(6):950–956. doi: 10.1128/aac.21.6.950. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Glauner B., Höltje J. V. Growth pattern of the murein sacculus of Escherichia coli. J Biol Chem. 1990 Nov 5;265(31):18988–18996. [PubMed] [Google Scholar]
  15. Goodell E. W. Recycling of murein by Escherichia coli. J Bacteriol. 1985 Jul;163(1):305–310. doi: 10.1128/jb.163.1.305-310.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Goodell E. W., Schwarz U. Cleavage and resynthesis of peptide cross bridges in Escherichia coli murein. J Bacteriol. 1983 Oct;156(1):136–140. doi: 10.1128/jb.156.1.136-140.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hooper D. C. Quinolone mode of action. Drugs. 1995;49 (Suppl 2):10–15. doi: 10.2165/00003495-199500492-00004. [DOI] [PubMed] [Google Scholar]
  18. Höltje J. V., Glauner B. Structure and metabolism of the murein sacculus. Res Microbiol. 1990 Jan;141(1):75–89. doi: 10.1016/0923-2508(90)90100-5. [DOI] [PubMed] [Google Scholar]
  19. Jacobs C., Huang L. J., Bartowsky E., Normark S., Park J. T. Bacterial cell wall recycling provides cytosolic muropeptides as effectors for beta-lactamase induction. EMBO J. 1994 Oct 3;13(19):4684–4694. doi: 10.1002/j.1460-2075.1994.tb06792.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Koch A. L. Biophysics of bacterial walls viewed as stress-bearing fabric. Microbiol Rev. 1988 Sep;52(3):337–353. doi: 10.1128/mr.52.3.337-353.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. LENNOX E. S. Transduction of linked genetic characters of the host by bacteriophage P1. Virology. 1955 Jul;1(2):190–206. doi: 10.1016/0042-6822(55)90016-7. [DOI] [PubMed] [Google Scholar]
  22. Lutkenhaus J. F. Coupling of DNA replication and cell division: sulB is an allele of ftsZ. J Bacteriol. 1983 Jun;154(3):1339–1346. doi: 10.1128/jb.154.3.1339-1346.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. MacAlister T. J., Cook W. R., Weigand R., Rothfield L. I. Membrane-murein attachment at the leading edge of the division septum: a second membrane-murein structure associated with morphogenesis of the gram-negative bacterial division septum. J Bacteriol. 1987 Sep;169(9):3945–3951. doi: 10.1128/jb.169.9.3945-3951.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Maguin E., Lutkenhaus J., D'Ari R. Reversibility of SOS-associated division inhibition in Escherichia coli. J Bacteriol. 1986 Jun;166(3):733–738. doi: 10.1128/jb.166.3.733-738.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Mobley H. L., Koch A. L., Doyle R. J., Streips U. N. Insertion and fate of the cell wall in Bacillus subtilis. J Bacteriol. 1984 Apr;158(1):169–179. doi: 10.1128/jb.158.1.169-179.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Mulder E., Woldringh C. L. Autoradiographic analysis of diaminopimelic acid incorporation in filamentous cells of Escherichia coli: repression of peptidoglycan synthesis around the nucleoid. J Bacteriol. 1991 Aug;173(15):4751–4756. doi: 10.1128/jb.173.15.4751-4756.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Mullin D. A., Woldringh C. L., Henson J. M., Walker J. R. Cloning of the Escherichia coli dnaZX region and identification of its products. Mol Gen Genet. 1983;192(1-2):73–79. doi: 10.1007/BF00327649. [DOI] [PubMed] [Google Scholar]
  28. Nanninga N. Cell division and peptidoglycan assembly in Escherichia coli. Mol Microbiol. 1991 Apr;5(4):791–795. doi: 10.1111/j.1365-2958.1991.tb00751.x. [DOI] [PubMed] [Google Scholar]
  29. Obermann W., Höltje J. V. Alterations of murein structure and of penicillin-binding proteins in minicells from Escherichia coli. Microbiology. 1994 Jan;140(Pt 1):79–87. doi: 10.1099/13500872-140-1-79. [DOI] [PubMed] [Google Scholar]
  30. Park J. T., Burman L. G. Elongation of the murein sacculus of Escherichia coli. Ann Inst Pasteur Microbiol. 1985 Jan-Feb;136A(1):51–58. doi: 10.1016/s0769-2609(85)80021-1. [DOI] [PubMed] [Google Scholar]
  31. Pisabarro A. G., de Pedro M. A., Vázquez D. Structural modifications in the peptidoglycan of Escherichia coli associated with changes in the state of growth of the culture. J Bacteriol. 1985 Jan;161(1):238–242. doi: 10.1128/jb.161.1.238-242.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Prats R., de Pedro M. A. Normal growth and division of Escherichia coli with a reduced amount of murein. J Bacteriol. 1989 Jul;171(7):3740–3745. doi: 10.1128/jb.171.7.3740-3745.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Rothfield L. I., DeBoer P., Cook W. R. Localization of septation sites. Res Microbiol. 1990 Jan;141(1):57–63. doi: 10.1016/0923-2508(90)90098-b. [DOI] [PubMed] [Google Scholar]
  34. Schleifer K. H., Kandler O. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev. 1972 Dec;36(4):407–477. doi: 10.1128/br.36.4.407-477.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Schwarz U., Ryter A., Rambach A., Hellio R., Hirota Y. Process of cellular division in Escherichia coli: differention of growth zones in the Sacculus. J Mol Biol. 1975 Nov 15;98(4):749–759. doi: 10.1016/s0022-2836(75)80008-8. [DOI] [PubMed] [Google Scholar]
  36. Tsuruoka T., Tamura A., Miyata A., Takei T., Iwamatsu K., Inouye S., Matsuhashi M. Penicillin-insensitive incorporation of D-amino acids into cell wall peptidoglycan influences the amount of bound lipoprotein in Escherichia coli. J Bacteriol. 1984 Dec;160(3):889–894. doi: 10.1128/jb.160.3.889-894.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Verwer R. W., Nanninga N., Keck W., Schwarz U. Arrangement of glycan chains in the sacculus of Escherichia coli. J Bacteriol. 1978 Nov;136(2):723–729. doi: 10.1128/jb.136.2.723-729.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Wientjes F. B., Nanninga N. Rate and topography of peptidoglycan synthesis during cell division in Escherichia coli: concept of a leading edge. J Bacteriol. 1989 Jun;171(6):3412–3419. doi: 10.1128/jb.171.6.3412-3419.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. de Boer P. A., Cook W. R., Rothfield L. I. Bacterial cell division. Annu Rev Genet. 1990;24:249–274. doi: 10.1146/annurev.ge.24.120190.001341. [DOI] [PubMed] [Google Scholar]
  40. de Pedro M. A., Schwarz U. Heterogeneity of newly inserted and preexisting murein in the sacculus of Escherichia coli. Proc Natl Acad Sci U S A. 1981 Sep;78(9):5856–5860. doi: 10.1073/pnas.78.9.5856. [DOI] [PMC free article] [PubMed] [Google Scholar]

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