Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1974 Sep;119(3):1039–1056. doi: 10.1128/jb.119.3.1039-1056.1974

Electron Microscope Study of Septum Formation in Escherichia coli Strains B and B/r During Synchronous Growth

I D J Burdett a,1, R G E Murray a
PMCID: PMC245711  PMID: 4604418

Abstract

The formation of cell wall septa was monitored in Escherichia coli B and B/r during synchronous growth in glucose media at 37 C by means of electron microscopy. The visible events of septation comprised the following sequence, starting at about 30 min of incubation: (a) bleb formation of the outer membrane; (b) invagination of mucopeptide and cytoplasmic membrane (with associated mesosomes); the outer membrane is excluded from the septum; (c) formation of a cross-wall; (d) ingrowth of the outer membrane during cell separation. The septum is composed of a fold of cytoplasmic membrane plus mucopeptide, and the latter is a double structure, composed of two opposed lamellae separated by an electron-transparent gap. Experiments with chloramphenicol and nalidixic acid suggested that division could occur in the presence of these inhibitors once a round of deoxyribonucleic acid replication is completed. The initial stages of septation, as estimated by the potential of the cells to produce bulges in the presence of ampicillin, may involve the modification of mucopeptide by hydrolases at the end of the C period. Assembly of the septum may occur during the first half of the D period by means of precursors synthesized during the preceding C period.

Full text

PDF
1039

Images in this article

1043Image
on p.1043
1044Image
on p.1044
1046Image
on p.1046
1047Image
on p.1047
1048Image
on p.1048
1049Image
on p.1049
1052Image
on p.1052

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ahmed N., Smith D. G., Rowbury R. J. Effect of growth medium on the division of a filament-forming mutant of Salmonella typhimurium. Microbios. 1973 Apr-May;7(28):221–230. [PubMed] [Google Scholar]
  2. Braun V., Gnirke H., Henning U., Rehn K. Model for the structure of the shape-maintaining layer of the Escherichia coli cell envelope. J Bacteriol. 1973 Jun;114(3):1264–1270. doi: 10.1128/jb.114.3.1264-1270.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Braun V., Rehn K. Chemical characterization, spatial distribution and function of a lipoprotein (murein-lipoprotein) of the E. coli cell wall. The specific effect of trypsin on the membrane structure. Eur J Biochem. 1969 Oct;10(3):426–438. doi: 10.1111/j.1432-1033.1969.tb00707.x. [DOI] [PubMed] [Google Scholar]
  4. Burdett I. D. Bacterial mesosomes. Sci Prog. 1972 Winter;60(240):527–546. [PubMed] [Google Scholar]
  5. Burdett I. D., Murray R. G. Septum formation in Escherichia coli: characterization of septal structure and the effects of antibiotics on cell division. J Bacteriol. 1974 Jul;119(1):303–324. doi: 10.1128/jb.119.1.303-324.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Burdett I. D., Rogers H. J. The structure and development of mesosomes studied in Bacillus licheniformis strain 6346. J Ultrastruct Res. 1972 Jan;38(1):113–133. doi: 10.1016/s0022-5320(72)90087-1. [DOI] [PubMed] [Google Scholar]
  7. Clark D. J. The regulation of DNA replication and cell division in E. coli B-r. Cold Spring Harb Symp Quant Biol. 1968;33:823–838. doi: 10.1101/sqb.1968.033.01.094. [DOI] [PubMed] [Google Scholar]
  8. Cooper S., Helmstetter C. E. Chromosome replication and the division cycle of Escherichia coli B/r. J Mol Biol. 1968 Feb 14;31(3):519–540. doi: 10.1016/0022-2836(68)90425-7. [DOI] [PubMed] [Google Scholar]
  9. Daniels M. J. Lipid synthesis in relation to the cell cycle of Bacillus megaterium KM and Escherichia coli. Biochem J. 1969 Dec;115(4):697–701. doi: 10.1042/bj1150697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. De Petris S. Ultrastructure of the cell wall of Escherichia coli and chemical nature of its constituent layers. J Ultrastruct Res. 1967 Jul;19(1):45–83. doi: 10.1016/s0022-5320(67)80059-5. [DOI] [PubMed] [Google Scholar]
  11. Dix D. E., Helmstetter C. E. Coupling between chromosome completion and cell division in Escherichia coli. J Bacteriol. 1973 Sep;115(3):786–795. doi: 10.1128/jb.115.3.786-795.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ellar D. J., Lundgren D. G., Slepecky R. A. Fine structure of Bacillus megaterium during synchronous growth. J Bacteriol. 1967 Oct;94(4):1189–1205. doi: 10.1128/jb.94.4.1189-1205.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Glauert A. M., Thornley M. J. The topography of the bacterial cell wall. Annu Rev Microbiol. 1969;23:159–198. doi: 10.1146/annurev.mi.23.100169.001111. [DOI] [PubMed] [Google Scholar]
  14. HELMSTETTER C. E., CUMMINGS D. J. AN IMPROVED METHOD FOR THE SELECTION OF BACTERIAL CELLS AT DIVISION. Biochim Biophys Acta. 1964 Mar 16;82:608–610. doi: 10.1016/0304-4165(64)90453-2. [DOI] [PubMed] [Google Scholar]
  15. HOFFMAN H., FRANK M. E. TIME-LAPSE PHOTOMICROGRAPHY OF CELL GROWTH AND DIVISION IN ESCHERICHIA COLI. J Bacteriol. 1965 Jan;89:212–216. doi: 10.1128/jb.89.1.212-216.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hartmann R., Höltje J. V., Schwarz U. Targets of penicillin action in Escherichia coli. Nature. 1972 Feb 25;235(5339):426–429. doi: 10.1038/235426a0. [DOI] [PubMed] [Google Scholar]
  17. Helmstetter C. E. DNA synthesis during the division cycle of rapidly growing Escherichia coli B/r. J Mol Biol. 1968 Feb 14;31(3):507–518. doi: 10.1016/0022-2836(68)90424-5. [DOI] [PubMed] [Google Scholar]
  18. Helmstetter C. E., Pierucci O. Cell division during inhibition of deoxyribonucleic acid synthesis in Escherichia coli. J Bacteriol. 1968 May;95(5):1627–1633. doi: 10.1128/jb.95.5.1627-1633.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Helmstetter C., Cooper S., Pierucci O., Revelas E. On the bacterial life sequence. Cold Spring Harb Symp Quant Biol. 1968;33:809–822. doi: 10.1101/sqb.1968.033.01.093. [DOI] [PubMed] [Google Scholar]
  20. Higgins M. L., Shockman G. D. Procaryotic cell division with respect to wall and membranes. CRC Crit Rev Microbiol. 1971 May;1(1):29–72. doi: 10.3109/10408417109104477. [DOI] [PubMed] [Google Scholar]
  21. Hoffmann B., Messer W., Schwarz U. Regulation of polar cap formation in the life cycle of Escherichia coli. J Supramol Struct. 1972;1(1):29–37. doi: 10.1002/jss.400010105. [DOI] [PubMed] [Google Scholar]
  22. Hoffmann H. P., Geftic S. G., Heymann H., Adair F. W. Mesosomes in Pseudomonas aeruginosa. J Bacteriol. 1973 Apr;114(1):434–438. doi: 10.1128/jb.114.1.434-438.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Izaki K., Matsuhashi M., Strominger J. L. Biosynthesis of the peptidoglycan of bacterial cell walls. 8. Peptidoglycan transpeptidase and D-alanine carboxypeptidase: penicillin-sensitive enzymatic reaction in strains of Escherichia coli. J Biol Chem. 1968 Jun 10;243(11):3180–3192. [PubMed] [Google Scholar]
  24. Jones N. C., Donachie W. D. Chromosome replication, transcription and control of cell division in Escherichia coli. Nat New Biol. 1973 May 23;243(125):100–103. [PubMed] [Google Scholar]
  25. MURRAY R. G., STEED P., ELSON H. E. THE LOCATION OF THE MUCOPEPTIDE IN SECTIONS OF THE CELL WALL OF ESCHERICHIA COLI AND OTHER GRAM-NEGATIVE BACTERIA. Can J Microbiol. 1965 Jun;11:547–560. doi: 10.1139/m65-072. [DOI] [PubMed] [Google Scholar]
  26. Maier S., Murray R. G. The fine structure of Thioploca ingrica and a comparison with Beggiatoa. Can J Microbiol. 1965 Aug;11(4):645–655. doi: 10.1139/m65-087. [DOI] [PubMed] [Google Scholar]
  27. Martin H. H., Heilmann H. D., Preusser H. J. State of the rigid-layer in celll walls of some gram-negative Bacteria. Arch Mikrobiol. 1972;83(4):332–346. doi: 10.1007/BF00425246. [DOI] [PubMed] [Google Scholar]
  28. NAGATA T. The molecular synchrony and sequential replication of DNA in Escherichia coli. Proc Natl Acad Sci U S A. 1963 Apr;49:551–559. doi: 10.1073/pnas.49.4.551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Pato M. L. Regulation of chromosome replication and the bacterial cell cycle. Annu Rev Microbiol. 1972;26:347–368. doi: 10.1146/annurev.mi.26.100172.002023. [DOI] [PubMed] [Google Scholar]
  30. Pierucci O., Helmstetter C. E. Chromosome replication, protein synthesis and cell division in Escherichia coli. Fed Proc. 1969 Nov-Dec;28(6):1755–1760. [PubMed] [Google Scholar]
  31. Pontefract R. D., Bergeron G., Thatcher F. S. Mesosomes in Escherichia coli. J Bacteriol. 1969 Jan;97(1):367–375. doi: 10.1128/jb.97.1.367-375.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. RYTER A., KELLENBERGER E., BIRCHANDERSEN A., MAALOE O. Etude au microscope électronique de plasmas contenant de l'acide désoxyribonucliéique. I. Les nucléoides des bactéries en croissance active. Z Naturforsch B. 1958 Sep;13B(9):597–605. [PubMed] [Google Scholar]
  33. Reeve J. N., Groves D. J., Clark D. J. Regulation of Cell Division in Escherichia coli: Characterization of Temperature-Sensitive Division Mutants. J Bacteriol. 1970 Dec;104(3):1052–1064. doi: 10.1128/jb.104.3.1052-1064.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Reyn A., Birch-Andersen A., Berger U. Fine structure and taxonomic position of Neisseria haemolysans (Thjotta and Boe 1938) or Gemella haemolysans (Berger 1960). Acta Pathol Microbiol Scand B Microbiol Immunol. 1970;78(3):375–389. doi: 10.1111/j.1699-0463.1970.tb04317.x. [DOI] [PubMed] [Google Scholar]
  35. Rode L. J. Bacterial spore appendages. CRC Crit Rev Microbiol. 1971 May;1(1):1–27. doi: 10.3109/10408417109104476. [DOI] [PubMed] [Google Scholar]
  36. Rogers H. J. Bacterial growth and the cell envelope. Bacteriol Rev. 1970 Jun;34(2):194–214. doi: 10.1128/br.34.2.194-214.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Rowbury R. J. Bacterial cell division: its regulation and relation to DNA synthesis. Sci Prog. 1972 Summer;60(238):169–188. [PubMed] [Google Scholar]
  38. Ryter A., Hirota Y., Schwarz U. Process of cellular division in Escherichia coli growth pattern of E. coli murein. J Mol Biol. 1973 Jun 25;78(1):185–195. doi: 10.1016/0022-2836(73)90437-3. [DOI] [PubMed] [Google Scholar]
  39. Ryter A., Jacob F. Etude morphologique de la liaison du noyau à la membrane chez E. coli et chez les protoplastes de B. subtilis. Ann Inst Pasteur (Paris) 1966 Jun;110(6):801–812. [PubMed] [Google Scholar]
  40. Schwarz U., Asmus A., Frank H. Autolytic enzymes and cell division of Escherichia coli. J Mol Biol. 1969 May 14;41(3):419–429. doi: 10.1016/0022-2836(69)90285-x. [DOI] [PubMed] [Google Scholar]
  41. Steed P., Murray R. G. The cell wall and cell division of gram-negative bacteria. Can J Microbiol. 1966 Apr;12(2):263–270. doi: 10.1139/m66-036. [DOI] [PubMed] [Google Scholar]
  42. Wu P. C., Pardee A. B. Cell division of Escherichia coli: control by membrane organization. J Bacteriol. 1973 May;114(2):603–611. doi: 10.1128/jb.114.2.603-611.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Zaritsky A., Pritchard R. H. Changes in cell size and shape associated with changes in the replication time of the chromosome of Escherichia coli. J Bacteriol. 1973 May;114(2):824–837. doi: 10.1128/jb.114.2.824-837.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES