Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1994 Oct;176(19):6030–6038. doi: 10.1128/jb.176.19.6030-6038.1994

Nucleoid partitioning and the division plane in Escherichia coli.

C L Woldringh 1, A Zaritsky 1, N B Grover 1
PMCID: PMC196821  PMID: 7523361

Abstract

Escherichia coli nucleoids were visualized after the DNA of OsO4-fixed but hydrated cells was stained with the fluorochrome DAPI (4',6-diamidino-2-phenylindole dihydrochloride hydrate). In slowly growing cells, the nucleoids are rod shaped and seem to move along the major cell axis, whereas in rapidly growing, wider cells they consist of two- to four-lobed structures that often appear to advance along axes lying perpendicular or oblique to the major axis of the cell. To test the idea that the increase in cell diameter following nutritional shift-up is caused by the increased amount of DNA in the nucleoid, the cells were subjected to DNA synthesis inhibition. In the absence of DNA replication, the nucleoids continued to move in the growing filaments and were pulled apart into small domains along the length of the cell. When these cells were then transferred to a richer medium, their diameters increased, especially in the region enclosing the nucleoid. It thus appears that the nucleoid motive force does not depend on DNA synthesis and that cell diameter is determined not by the amount of DNA per chromosome but rather by the synthetic activity surrounding the nucleoid. Under the non-steady-state but balanced growth conditions induced by thymine limitation, nucleoids become separated into small lobules, often lying in asymmetric configurations along the cell periphery, and oblique and asymmetric division planes occur in more than half of the constricting cells. We suggest that such irregular DNA movement affects both the angle of the division plane and its position.

Full text

PDF
6035

Images in this article

6031Image
on p.6031
6033Image
on p.6033
6035Image
on p.6035
6036Image
on p.6036

Selected References

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

  1. Akerlund T., Nordström K., Bernander R. Branched Escherichia coli cells. Mol Microbiol. 1993 Nov;10(4):849–858. doi: 10.1111/j.1365-2958.1993.tb00955.x. [DOI] [PubMed] [Google Scholar]
  2. Begg K. J., Donachie W. D. Experiments on chromosome separation and positioning in Escherichia coli. New Biol. 1991 May;3(5):475–486. [PubMed] [Google Scholar]
  3. Bi E. F., Lutkenhaus J. FtsZ ring structure associated with division in Escherichia coli. Nature. 1991 Nov 14;354(6349):161–164. doi: 10.1038/354161a0. [DOI] [PubMed] [Google Scholar]
  4. Bi E., Lutkenhaus J. Isolation and characterization of ftsZ alleles that affect septal morphology. J Bacteriol. 1992 Aug;174(16):5414–5423. doi: 10.1128/jb.174.16.5414-5423.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bohrmann B., Villiger W., Johansen R., Kellenberger E. Coralline shape of the bacterial nucleoid after cryofixation. J Bacteriol. 1991 May;173(10):3149–3158. doi: 10.1128/jb.173.10.3149-3158.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cavalier-Smith T. Bacterial DNA segregation: its motors and positional control. J Theor Biol. 1987 Aug 7;127(3):361–372. doi: 10.1016/s0022-5193(87)80112-1. [DOI] [PubMed] [Google Scholar]
  7. Chai N. C., Lark K. G. Cytological studies of deoxyribonucleic acid replication in Escherichia coli 15T-: replication at slow growth rates and after a shift-up into rich medium. J Bacteriol. 1970 Oct;104(1):401–409. doi: 10.1128/jb.104.1.401-409.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cohen S. S., Barner H. D. STUDIES ON UNBALANCED GROWTH IN ESCHERICHIA COLI. Proc Natl Acad Sci U S A. 1954 Oct;40(10):885–893. doi: 10.1073/pnas.40.10.885. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Cooper S., Weusthoff G. Comment on the use of chloramphenicol to study the initiation of deoxyribonucleic acid synthesis. J Bacteriol. 1971 May;106(2):709–711. doi: 10.1128/jb.106.2.709-711.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dingman C. W. Bidirectional chromosome replication: some topological considerations. J Theor Biol. 1974 Jan;43(1):187–195. doi: 10.1016/s0022-5193(74)80052-4. [DOI] [PubMed] [Google Scholar]
  12. Donachie W. D., Begg K. J. Chromosome partition in Escherichia coli requires postreplication protein synthesis. J Bacteriol. 1989 Oct;171(10):5405–5409. doi: 10.1128/jb.171.10.5405-5409.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dürrenberger M., Bjornsti M. A., Uetz T., Hobot J. A., Kellenberger E. Intracellular location of the histonelike protein HU in Escherichia coli. J Bacteriol. 1988 Oct;170(10):4757–4768. doi: 10.1128/jb.170.10.4757-4768.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gayda R. C., Henk M. C., Leong D. C-shaped cells caused by expression of an ftsA mutation in Escherichia coli. J Bacteriol. 1992 Aug;174(16):5362–5370. doi: 10.1128/jb.174.16.5362-5370.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Higgins C. F., Dorman C. J., Stirling D. A., Waddell L., Booth I. R., May G., Bremer E. A physiological role for DNA supercoiling in the osmotic regulation of gene expression in S. typhimurium and E. coli. Cell. 1988 Feb 26;52(4):569–584. doi: 10.1016/0092-8674(88)90470-9. [DOI] [PubMed] [Google Scholar]
  16. Hiraga S. Chromosome and plasmid partition in Escherichia coli. Annu Rev Biochem. 1992;61:283–306. doi: 10.1146/annurev.bi.61.070192.001435. [DOI] [PubMed] [Google Scholar]
  17. Hiraga S., Ogura T., Niki H., Ichinose C., Mori H. Positioning of replicated chromosomes in Escherichia coli. J Bacteriol. 1990 Jan;172(1):31–39. doi: 10.1128/jb.172.1.31-39.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Koch A. L. How bacteria grow and divide in spite of internal hydrostatic pressure. Can J Microbiol. 1985 Dec;31(12):1071–1084. doi: 10.1139/m85-204. [DOI] [PubMed] [Google Scholar]
  19. Løbner-Olesen A., Kuempel P. L. Chromosome partitioning in Escherichia coli. J Bacteriol. 1992 Dec;174(24):7883–7889. doi: 10.1128/jb.174.24.7883-7889.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. MASON D. J., POWELSON D. M. Nuclear division as observed in live bacteria by a new technique. J Bacteriol. 1956 Apr;71(4):474–479. doi: 10.1128/jb.71.4.474-479.1956. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Marr A. G., Harvey R. J., Trentini W. C. Growth and division of Escherichia coli. J Bacteriol. 1966 Jun;91(6):2388–2389. doi: 10.1128/jb.91.6.2388-2389.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mulder E., Woldringh C. L. Actively replicating nucleoids influence positioning of division sites in Escherichia coli filaments forming cells lacking DNA. J Bacteriol. 1989 Aug;171(8):4303–4314. doi: 10.1128/jb.171.8.4303-4314.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. Ogden G. B., Pratt M. J., Schaechter M. The replicative origin of the E. coli chromosome binds to cell membranes only when hemimethylated. Cell. 1988 Jul 1;54(1):127–135. doi: 10.1016/0092-8674(88)90186-9. [DOI] [PubMed] [Google Scholar]
  25. Pritchard R. H., Zaritsky A. Effect of thymine concentration on the replication velocity of DNA in a thymineless mutant of Escherichia coli. Nature. 1970 Apr 11;226(5241):126–131. doi: 10.1038/226126a0. [DOI] [PubMed] [Google Scholar]
  26. Ryter A., Chang A. Localization of transcribing genes in the bacterial cell by means of high resolution autoradiography. J Mol Biol. 1975 Nov 15;98(4):797–810. doi: 10.1016/s0022-2836(75)80011-8. [DOI] [PubMed] [Google Scholar]
  27. SCHAECHTER M., MAALOE O., KJELDGAARD N. O. Dependency on medium and temperature of cell size and chemical composition during balanced grown of Salmonella typhimurium. J Gen Microbiol. 1958 Dec;19(3):592–606. doi: 10.1099/00221287-19-3-592. [DOI] [PubMed] [Google Scholar]
  28. Schmid M. B. A locus affecting nucleoid segregation in Salmonella typhimurium. J Bacteriol. 1990 Sep;172(9):5416–5424. doi: 10.1128/jb.172.9.5416-5424.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Taschner P. E., Verest J. G., Woldringh C. L. Genetic and morphological characterization of ftsB and nrdB mutants of Escherichia coli. J Bacteriol. 1987 Jan;169(1):19–25. doi: 10.1128/jb.169.1.19-25.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Trueba F. J., Woldringh C. L. Changes in cell diameter during the division cycle of Escherichia coli. J Bacteriol. 1980 Jun;142(3):869–878. doi: 10.1128/jb.142.3.869-878.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Valkenburg J. A., Woldringh C. L., Brakenhoff G. J., van der Voort H. T., Nanninga N. Confocal scanning light microscopy of the Escherichia coli nucleoid: comparison with phase-contrast and electron microscope images. J Bacteriol. 1985 Feb;161(2):478–483. doi: 10.1128/jb.161.2.478-483.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Valkenburg J. A., Woldringh C. L. Phase separation between nucleoid and cytoplasm in Escherichia coli as defined by immersive refractometry. J Bacteriol. 1984 Dec;160(3):1151–1157. doi: 10.1128/jb.160.3.1151-1157.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Woldringh C. L., Grover N. B., Rosenberger R. F., Zaritsky A. Dimensional rearrangement of rod-shaped bacteria following nutritional shift-up. II. Experiments with Escherichia coli B/r. J Theor Biol. 1980 Oct 7;86(3):441–454. doi: 10.1016/0022-5193(80)90344-6. [DOI] [PubMed] [Google Scholar]
  34. Woldringh C. L. Morphological analysis of nuclear separation and cell division during the life cycle of Escherichia coli. J Bacteriol. 1976 Jan;125(1):248–257. doi: 10.1128/jb.125.1.248-257.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Woldringh C. L., Mulder E., Huls P. G., Vischer N. Toporegulation of bacterial division according to the nucleoid occlusion model. Res Microbiol. 1991 Feb-Apr;142(2-3):309–320. doi: 10.1016/0923-2508(91)90046-d. [DOI] [PubMed] [Google Scholar]
  36. Woldringh C. L., Mulder E., Valkenburg J. A., Wientjes F. B., Zaritsky A., Nanninga N. Role of the nucleoid in the toporegulation of division. Res Microbiol. 1990 Jan;141(1):39–49. doi: 10.1016/0923-2508(90)90096-9. [DOI] [PubMed] [Google Scholar]
  37. Woldringh C. L., de Jong M. A., van den Berg W., Koppes L. Morphological analysis of the division cycle of two Escherichia coli substrains during slow growth. J Bacteriol. 1977 Jul;131(1):270–279. doi: 10.1128/jb.131.1.270-279.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Zaritsky A., Helmstetter C. E. Rate maintenance of cell division in Escherichia coli B/r: analysis of a simple nutritional shift-down. J Bacteriol. 1992 Dec;174(24):8152–8155. doi: 10.1128/jb.174.24.8152-8155.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Zaritsky A. On dimensional determination of rod-shaped bacteria. J Theor Biol. 1975 Oct;54(2):243–248. doi: 10.1016/s0022-5193(75)80129-9. [DOI] [PubMed] [Google Scholar]
  40. 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]
  41. Zaritsky A., Woldringh C. L. Chromosome replication rate and cell shape in Escherichia coli: lack of coupling. J Bacteriol. 1978 Aug;135(2):581–587. doi: 10.1128/jb.135.2.581-587.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Zyskind J. W., Svitil A. L., Stine W. B., Biery M. C., Smith D. W. RecA protein of Escherichia coli and chromosome partitioning. Mol Microbiol. 1992 Sep;6(17):2525–2537. doi: 10.1111/j.1365-2958.1992.tb01429.x. [DOI] [PubMed] [Google Scholar]
  43. van Helvoort J. M., Woldringh C. L. Nucleoid partitioning in Escherichia coli during steady-state growth and upon recovery from chloramphenicol treatment. Mol Microbiol. 1994 Aug;13(4):577–583. doi: 10.1111/j.1365-2958.1994.tb00452.x. [DOI] [PubMed] [Google Scholar]

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

RESOURCES