Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1980 Sep;143(3):1241–1252. doi: 10.1128/jb.143.3.1241-1252.1980

Correlation between size and age at different events in the cell division cycle of Escherichia coli.

L J Koppes, M Meyer, H B Oonk, M A de Jong, N Nanninga
PMCID: PMC294487  PMID: 6997267

Abstract

The variability of (i) the B period between birth and initiation of chromosome replication, (ii) the U period between initiation of chromosome replication and initiation of cell constriction, and (iii) the interdivision period (tau) have been estimated for slowly growing Escherichia coli B/r F. Cultures synchronized by the membrane elution technique were pulse-labeled with [3H]thymidine or continuously labeled with [3H]thymine. After fixation, the pattern of deoxyribonucleic acid replication was analyzed by electron microscopic radioautography. Cell length was found to increase exponentially with age at two different slow growth rates. The coefficient of variation of the B period was estimated to be 60%, that of the U period was 29%, and that of the interdivision period was 12%. From these values and the coefficient of variation of length at different cell cycle events were calculated a negative correlation between the B and U period (r = -0.9) and a positive correlation between length at birth and cell separation (r = 0.6). Initiation of chromosome replication and cell constriction were strictly correlated both with respect to age (r = 0.7) and length (r = 0.8). On the other hand, length at initiation of chromosome replication was distantly correlated with age (r = 0.1) or length at birth (r = 0.3). This low correlation excludes a model in which chromosome initiation is controlled by a random event in the B period. It favors a model in which chromosome initiation occurs at a particular distributed size independent of cell division.

Full text

PDF
1241

Selected References

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

  1. BLUMENTHAL L. K., ZAHLER S. A. Index for measurement of synchronization of cell populations. Science. 1962 Mar 2;135(3505):724–724. doi: 10.1126/science.135.3505.724. [DOI] [PubMed] [Google Scholar]
  2. Bleecken S. "Replisome"-controlled initiation of DNA replication. J Theor Biol. 1971 Jul;32(1):81–92. doi: 10.1016/0022-5193(71)90137-8. [DOI] [PubMed] [Google Scholar]
  3. COLLINS J. F., RICHMOND M. H. Rate of growth of Bacillus cereus between divisions. J Gen Microbiol. 1962 Apr;28:15–33. doi: 10.1099/00221287-28-1-15. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. 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]
  6. ERRINGTON F. P., POWELL E. O., THOMPSON N. GROWTH CHARACTERISITICS OF SOME GRAM-NEGATIVE BACTERIA. J Gen Microbiol. 1965 Apr;39:109–123. doi: 10.1099/00221287-39-1-109. [DOI] [PubMed] [Google Scholar]
  7. Fantes P. A. Control of cell size and cycle time in Schizosaccharomyces pombe. J Cell Sci. 1977 Apr;24:51–67. doi: 10.1242/jcs.24.1.51. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Harvey J. D. Parameters of the generation time distribution of Escherichia coli B-r. J Gen Microbiol. 1972 Apr;70(1):109–114. doi: 10.1099/00221287-70-1-109. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Helmstetter C. E., Pierucci O. DNA synthesis during the division cycle of three substrains of Escherichia coli B/r. J Mol Biol. 1976 Apr 15;102(3):477–486. doi: 10.1016/0022-2836(76)90329-6. [DOI] [PubMed] [Google Scholar]
  12. KOCH A. L., SCHAECHTER M. A model for statistics of the cell division process. J Gen Microbiol. 1962 Nov;29:435–454. doi: 10.1099/00221287-29-3-435. [DOI] [PubMed] [Google Scholar]
  13. Killander D., Zetterberg A. A quantitative cytochemical investigation of the relationship between cell mass and initiation of DNA synthesis in mouse fibroblasts in vitro. Exp Cell Res. 1965 Oct;40(1):12–20. doi: 10.1016/0014-4827(65)90285-5. [DOI] [PubMed] [Google Scholar]
  14. Koch A. L. Does the initiation of chromosome replication regulate cell division? Adv Microb Physiol. 1977;16:49–98. doi: 10.1016/s0065-2911(08)60047-8. [DOI] [PubMed] [Google Scholar]
  15. Koppes L. H., Woldringh C. L., Nanninga N. Size variations and correlation of different cell cycle events in slow-growing Escherichia coli. J Bacteriol. 1978 May;134(2):423–433. doi: 10.1128/jb.134.2.423-433.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Koppes L. J., Nanninga N. Positive correlation between size at initiation of chromosome replication in Escherichia coli and size at initiation of cell constriction. J Bacteriol. 1980 Jul;143(1):89–99. doi: 10.1128/jb.143.1.89-99.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Koppes L. J., Overbeeke N., Nanninga N. DNA replication pattern and cell wall growth in Escherichia coli PAT 84. J Bacteriol. 1978 Mar;133(3):1053–1061. doi: 10.1128/jb.133.3.1053-1061.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kubitschek H. E. Generation times: ancestral dependence and dependence upon cell size. Exp Cell Res. 1966 Aug;43(1):30–38. doi: 10.1016/0014-4827(66)90374-0. [DOI] [PubMed] [Google Scholar]
  19. LaBella F. S., Sanwal M. Isolation of nerve endings from the posterior pituitary gland. Electron microscopy of fractions obtained by centrifugation. J Cell Biol. 1965 Jun;25(3 Suppl):179–193. doi: 10.1083/jcb.25.3.179. [DOI] [PubMed] [Google Scholar]
  20. Meyer M., De Jong M. A., Demets R., Nanninga N. Length growth of two Escherichia coli B/r substrains. J Bacteriol. 1979 Apr;138(1):17–23. doi: 10.1128/jb.138.1.17-23.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nasmyth K., Nurse P., Fraser R. S. The effect of cell mass on the cell cycle timing and duration of S-phase in fission yeast. J Cell Sci. 1979 Oct;39:215–233. doi: 10.1242/jcs.39.1.215. [DOI] [PubMed] [Google Scholar]
  22. Newman C. N., Kubitschek H. E. Variation in periodic replication of the chromosome in Escherichia coli B/rTT. J Mol Biol. 1978 Jun 5;121(4):461–471. doi: 10.1016/0022-2836(78)90394-7. [DOI] [PubMed] [Google Scholar]
  23. POWELL E. O. A NOTE ON KOCH AND SCHAECHTER'S HYPOTHESIS ABOUT GROWTH AND FISSION OF BACTERIA. J Gen Microbiol. 1964 Nov;37:231–249. doi: 10.1099/00221287-37-2-231. [DOI] [PubMed] [Google Scholar]
  24. POWELL E. O. An outline of the pattern of bacterial generation times. J Gen Microbiol. 1958 Apr;18(2):382–417. doi: 10.1099/00221287-18-2-382. [DOI] [PubMed] [Google Scholar]
  25. POWELL E. O., ERRINGTON F. P. Generation times of individual bacteria: some corroborative measurements. J Gen Microbiol. 1963 May;31:315–327. doi: 10.1099/00221287-31-2-315. [DOI] [PubMed] [Google Scholar]
  26. Painter P. R., Marr A. G. Mathematics of microbial populations. Annu Rev Microbiol. 1968;22:519–548. doi: 10.1146/annurev.mi.22.100168.002511. [DOI] [PubMed] [Google Scholar]
  27. Prescott D. M. The cell cycle and the control of cellular reproduction. Adv Genet. 1976;18:99–177. doi: 10.1016/s0065-2660(08)60438-1. [DOI] [PubMed] [Google Scholar]
  28. STANNERS C. P., TILL J. E. DNA synthesis in individual L-strain mouse cells. Biochim Biophys Acta. 1960 Jan 29;37:406–419. doi: 10.1016/0006-3002(60)90496-0. [DOI] [PubMed] [Google Scholar]
  29. Sompayrac L., Maaloe O. Autorepressor model for control of DNA replication. Nat New Biol. 1973 Jan 31;241(109):133–135. doi: 10.1038/newbio241133a0. [DOI] [PubMed] [Google Scholar]
  30. Tyson C. B., Lord P. G., Wheals A. E. Dependency of size of Saccharomyces cerevisiae cells on growth rate. J Bacteriol. 1979 Apr;138(1):92–98. doi: 10.1128/jb.138.1.92-98.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]
  32. Yen A., Fried J., Kitahara T., Stride A., Clarkson B. D. The kinetic significance of cell size, I. Variation of cell cycle parameters with size measured at mitosis. Exp Cell Res. 1975 Oct 15;95(2):295–302. doi: 10.1016/0014-4827(75)90554-6. [DOI] [PubMed] [Google Scholar]

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

RESOURCES