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. 1986 Jul;167(1):219–230. doi: 10.1128/jb.167.1.219-230.1986

Growth kinetics of individual Bacillus subtilis cells and correlation with nucleoid extension.

I D Burdett, T B Kirkwood, J B Whalley
PMCID: PMC212864  PMID: 3087953

Abstract

The growth rate of individual cells of Bacillus subtilis (doubling time, 120 min) has been calculated by using a modification of the Collins-Richmond principle which allows the growth rate of mononucleate, binucleate, and septate cells to be calculated separately. The standard Collins-Richmond equation represents a weighted average of the growth rate calculated from these three major classes. Both approaches strongly suggest that the rate of length extension is exponential. By preparing critical-point-dried cells, in which major features of the cell such as nucleoids and cross-walls can be seen, it has also been possible to examine whether nucleoid extension is coupled to length extension. Growth rates for nucleoid movement are parallel to those of total length extension, except possibly in the case of septate cells. Furthermore, by calculating the growth rate of various portions of the cell surface, it appears likely that the limits of the site of cylindrical envelope assembly lie between the distal tips of the nucleoid; the old poles show zero growth rate. Coupling of nucleoid extension with increase of cell length is envisaged as occurring through an exponentially increasing number of DNA-surface attachment sites occupying most of the available surface.

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Selected References

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  1. Archibald A. R., Coapes H. E. Bacteriophage SP50 as a marker for cell wall growth in Bacillus subtilis. J Bacteriol. 1976 Mar;125(3):1195–1206. doi: 10.1128/jb.125.3.1195-1206.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Burdett I. D. Electron microscope study of the rod-to-coccus shape change in a temperature-sensitive rod- mutant of Bacillus subtilis. J Bacteriol. 1979 Mar;137(3):1395–1405. doi: 10.1128/jb.137.3.1395-1405.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Burdett I. D., Higgins M. L. Study of pole assembly in Bacillus subtilis by computer reconstruction of septal growth zones seen in central, longitudinal thin sections of cells. J Bacteriol. 1978 Feb;133(2):959–971. doi: 10.1128/jb.133.2.959-971.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Burdett I. D., Kirkwood T. B. How does a bacterium grow during its cell cycle? J Theor Biol. 1983 Jul 7;103(1):11–20. doi: 10.1016/0022-5193(83)90195-9. [DOI] [PubMed] [Google Scholar]
  5. Burdett I. D. Quantitative studies of rod--coccus morphogenesis in a temperature-sensitive rod- mutant of Bacillus subtilis. J Gen Microbiol. 1980 Nov;121(1):93–103. doi: 10.1099/00221287-121-1-93. [DOI] [PubMed] [Google Scholar]
  6. CHUNG K. L., HAWIRKO R. Z., ISAAC P. K. CELL WALL REPLICATION. I. CELL WALL GROWTH OF BACILLUS CEREUS AND BACILLUS MEGATERIUM. Can J Microbiol. 1964 Feb;10:43–48. doi: 10.1139/m64-007. [DOI] [PubMed] [Google Scholar]
  7. 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]
  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. Doyle R. J., Koch A. L., Carstens P. H. Cell wall-DNA association in Bacillus subtilis. J Bacteriol. 1983 Mar;153(3):1521–1527. doi: 10.1128/jb.153.3.1521-1527.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Ephrati-Elizur E., Borenstein S. Velocity of chromosome replication in thymine-requiring and independent strains of Bacillus subtilis. J Bacteriol. 1971 Apr;106(1):58–64. doi: 10.1128/jb.106.1.58-64.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gibson C. W., Daneo-Moore L., Higgins M. L. Initiation of wall assembly sites in Streptococcus faecium. J Bacteriol. 1983 May;154(2):573–579. doi: 10.1128/jb.154.2.573-579.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hariharan I. K., Czolij R., Wake R. G. Conformation and segregation of nucleoids accompanying cell length extension after completion of a single round of DNA replication in germinated and outgrowing Bacillus subtilis spores. J Bacteriol. 1982 May;150(2):861–869. doi: 10.1128/jb.150.2.861-869.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Harvey R. J., Marr A. G., Painter P. R. Kinetics of growth of individual cells of Escherichia coli and Azotobacter agilis. J Bacteriol. 1967 Feb;93(2):605–617. doi: 10.1128/jb.93.2.605-617.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Higgins M. L., Shockman G. D. Study of cycle of cell wall assembly in Streptococcus faecalis by three-dimensional reconstructions of thin sections of cells. J Bacteriol. 1976 Sep;127(3):1346–1358. doi: 10.1128/jb.127.3.1346-1358.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Highton P. J. An electron microscopic study of mesosomes in Bacillus subtilis. J Ultrastruct Res. 1970 May;31(3):260–271. doi: 10.1016/s0022-5320(70)90130-9. [DOI] [PubMed] [Google Scholar]
  17. Hughes R. C., Stokes E. Cell wall growth in Bacillus licheniformis followed by immunofluorescence with mucopeptide-specific antiserum. J Bacteriol. 1971 May;106(2):694–696. doi: 10.1128/jb.106.2.694-696.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. KELLENBERGER E., RYTER A., SECHAUD J. Electron microscope study of DNA-containing plasms. II. Vegetative and mature phage DNA as compared with normal bacterial nucleoids in different physiological states. J Biophys Biochem Cytol. 1958 Nov 25;4(6):671–678. doi: 10.1083/jcb.4.6.671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. Koch A. L., Blumberg G. Distribution of bacteria in the velocity gradient centrifuge. Biophys J. 1976 May;16(5):389–405. doi: 10.1016/S0006-3495(76)85696-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Koch A. L., Higgins M. L. Cell cycle dynamics inferred from the static properties of cells in balanced growth. J Gen Microbiol. 1982 Dec;128(12):2877–2892. doi: 10.1099/00221287-128-12-2877. [DOI] [PubMed] [Google Scholar]
  22. Koch A. L. The surface stress theory of microbial morphogenesis. Adv Microb Physiol. 1983;24:301–366. doi: 10.1016/s0065-2911(08)60388-4. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Kubitschek H. E., Baldwin W. W., Graetzer R. Buoyant density constancy during the cell cycle of Escherichia coli. J Bacteriol. 1983 Sep;155(3):1027–1032. doi: 10.1128/jb.155.3.1027-1032.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kubitschek H. E. Bilinear cell growth of Escherichia coli. J Bacteriol. 1981 Nov;148(2):730–733. doi: 10.1128/jb.148.2.730-733.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kubitschek H. E., Woldringh C. L. Cell elongation and division probability during the Escherichia coli growth cycle. J Bacteriol. 1983 Mar;153(3):1379–1387. doi: 10.1128/jb.153.3.1379-1387.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kusano T., Steinmetz D., Hendrickson W. G., Murchie J., King M., Benson A., Schaechter M. Direct evidence for specific binding of the replicative origin of the Escherichia coli chromosome to the membrane. J Bacteriol. 1984 Apr;158(1):313–316. doi: 10.1128/jb.158.1.313-316.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Leibowitz P. J., Schaechter M. The attachment of the bacterial chromosome to the cell membrane. Int Rev Cytol. 1975;41:1–28. doi: 10.1016/s0074-7696(08)60964-x. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Nanninga N., Koppes L. J., de Vries-Tijssen F. C. The cell cycle of Bacillus subtilis as studied by electron microscopy. Arch Microbiol. 1979 Nov;123(2):173–181. doi: 10.1007/BF00446817. [DOI] [PubMed] [Google Scholar]
  31. Nermut M. V. The 'cell monolayer technique' in membrane research. Eur J Cell Biol. 1982 Aug;28(1):160–172. [PubMed] [Google Scholar]
  32. Pierucci O. Dimensions of Escherichia coli at various growth rates: model for envelope growth. J Bacteriol. 1978 Aug;135(2):559–574. doi: 10.1128/jb.135.2.559-574.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Pooley H. M. Layered distribution, according to age, within the cell wall of bacillus subtilis. J Bacteriol. 1976 Mar;125(3):1139–1147. doi: 10.1128/jb.125.3.1139-1147.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Pooley H. M. Turnover and spreading of old wall during surface growth of Bacillus subtilis. J Bacteriol. 1976 Mar;125(3):1127–1138. doi: 10.1128/jb.125.3.1127-1138.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Previc E. P. Biochemical determination of bacterial morphology and the geometry of cell division. J Theor Biol. 1970 Jun;27(3):471–497. doi: 10.1016/s0022-5193(70)80010-8. [DOI] [PubMed] [Google Scholar]
  36. Pritchard R. H. Review lecture on the growth and form of a bacterial cell. Philos Trans R Soc Lond B Biol Sci. 1974 Feb 21;267(886):303–336. doi: 10.1098/rstb.1974.0003. [DOI] [PubMed] [Google Scholar]
  37. Reeve J. N., Mendelson N. H., Coyne S. I., Hallock L. L., Cole R. M. Minicells of Bacillus subtilis. J Bacteriol. 1973 May;114(2):860–873. doi: 10.1128/jb.114.2.860-873.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Sargent M. G., Bennett M. F., Burdett I. D. Identification of specific restriction fragments associated with a membrane subparticle from Bacillus subtilis. J Bacteriol. 1983 Jun;154(3):1389–1396. doi: 10.1128/jb.154.3.1389-1396.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Sargent M. G. Control of cell length in Bacillus subtilis. J Bacteriol. 1975 Jul;123(1):7–19. doi: 10.1128/jb.123.1.7-19.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Sargent M. G. Control of membrane protein synthesis in Bacillus subtilis. Biochim Biophys Acta. 1975 Nov 3;406(4):564–574. doi: 10.1016/0005-2736(75)90033-4. [DOI] [PubMed] [Google Scholar]
  41. Sargent M. G. Surface extension and the cell cycle in prokaryotes. Adv Microb Physiol. 1978;18:105–176. doi: 10.1016/s0065-2911(08)60416-6. [DOI] [PubMed] [Google Scholar]
  42. Schlaeppi J. M., Karamata D. Cosegregation of cell wall and DNA in Bacillus subtilis. J Bacteriol. 1982 Dec;152(3):1231–1240. doi: 10.1128/jb.152.3.1231-1240.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Schlaeppi J. M., Pooley H. M., Karamata D. Identification of cell wall subunits in bacillus subtilis and analysis of their segregation during growth. J Bacteriol. 1982 Jan;149(1):329–337. doi: 10.1128/jb.149.1.329-337.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Trueba F. J., Neijssel O. M., Woldringh C. L. Generality of the growth kinetics of the average individual cell in different bacterial populations. J Bacteriol. 1982 Jun;150(3):1048–1055. doi: 10.1128/jb.150.3.1048-1055.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. 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]
  46. Viret J. F., Rogers H. J., Karamata D. Morphological and cell wall alterations in thermosensitive DNA mutants of Bacillus subtilis. Ann Inst Pasteur Microbiol. 1985 Jan-Feb;136A(1):119–129. doi: 10.1016/s0769-2609(85)80032-6. [DOI] [PubMed] [Google Scholar]
  47. Woldringh C. L., Binnerts J. S., Mans A. Variation in Escherichia coli buoyant density measured in Percoll gradients. J Bacteriol. 1981 Oct;148(1):58–63. doi: 10.1128/jb.148.1.58-63.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. 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]
  49. 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]
  50. Zusman D., Gottlieb P., Rosenberg E. Division cycle of Myxococcus xanthus. 3. Kinetics of cell growth and protein synthesis. J Bacteriol. 1971 Mar;105(3):811–819. doi: 10.1128/jb.105.3.811-819.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. de Chastellier C., Hellio R., Ryter A. Study of cell wall growth in Bacillus megaterium by high-resolution autoradiography. J Bacteriol. 1975 Sep;123(3):1184–1196. doi: 10.1128/jb.123.3.1184-1196.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]

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