1887

Abstract

The coupling between chromosome replication and cell division includes temporal and spatial elements. In bacteria, these have globally been resolved during the last 40 years, but their full details and action mechanisms are still under intensive study. The physiology of growth and the cell cycle are reviewed in the light of an established dogma that has formed a framework for development of new ideas, as exemplified here, using the Cell Cycle Simulation (CCSim) program. CCSim, described here in detail for the first time, employs four parameters related to time (replication, division and inter-division) and size (cell mass at replication initiation) that together are sufficient to describe bacterial cells under various conditions and states, which can be manipulated environmentally and genetically. Testing the predictions of CCSim by analysis of time-lapse micrographs of during designed manipulations of the rate of DNA replication identified aspects of both coupling elements. Enhanced frequencies of cell division were observed following an interval of reduced DNA replication rate, consistent with the prediction of a minimum possible distance between successive replisomes (an eclipse). As a corollary, the notion that cell poles are not always inert was confirmed by observed placement of division planes at perpendicular planes in monstrous and cuboidal cells containing multiple, segregating nucleoids.

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2011-07-01
2021-07-31
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References

  1. Beacham I. R., Beacham K., Zaritsky A., Pritchard R. H. ( 1971). Intracellular thymidine triphosphate concentrations in wild type and in thymine requiring mutants of Escherichia coli 15 and K12. J Mol Biol 60:75–86 [View Article][PubMed]
    [Google Scholar]
  2. Bernhardt T. G., de Boer P. A. J. ( 2005). SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over chromosomes in E. coli . Mol Cell 18:555–564 [View Article][PubMed]
    [Google Scholar]
  3. Bipatnath M., Dennis P. P., Bremer H. ( 1998). Initiation and velocity of chromosome replication in Escherichia coli B/r and K-12. J Bacteriol 180:265–273[PubMed]
    [Google Scholar]
  4. Bleecken S. ( 1969). Duplication of the bacterial cell and its initiation. J Theor Biol 25:137–158 [View Article][PubMed]
    [Google Scholar]
  5. Chai N.-C., Lark K. G. ( 1970). 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 104:401–409[PubMed]
    [Google Scholar]
  6. Cho H., McManus H. R., Dove S. L., Bernhardt T. G. ( 2011). Nucleoid occlusion factor SlmA is a DNA-activated FtsZ polymerization antagonist. Proc Natl Acad Sci U S A 108:3773–3778 [View Article][PubMed]
    [Google Scholar]
  7. de Pedro M. A., Grünfelder C. G., Schwarz H. ( 2004). Restricted mobility of cell surface proteins in the polar regions of Escherichia coli . J Bacteriol 186:2594–2602 [View Article][PubMed]
    [Google Scholar]
  8. Dix D. E., Helmstetter C. E. ( 1973). Coupling between chromosome completion and cell division in Escherichia coli . J Bacteriol 115:786–795[PubMed]
    [Google Scholar]
  9. Donachie W. D. ( 1968). Relationship between cell size and time of initiation of DNA replication. Nature 219:1077–1079 [View Article][PubMed]
    [Google Scholar]
  10. Elmore S., Müller M., Vischer N. O. E., Odijk Th., Woldringh C. L. ( 2005). Single-particle tracking of oriC-GFP fluorescent spots during chromosome segregation in Escherichia coli . J Struct Biol 151:275–287 [View Article][PubMed]
    [Google Scholar]
  11. Ephrati-Elizur E., Borenstein S. ( 1971). Velocity of chromosome replication in thymine-requiring and independent strains of Bacillus subtilis . J Bacteriol 106:58–64[PubMed]
    [Google Scholar]
  12. Erickson H. P. ( 2009). Modeling the physics of FtsZ assembly and force generation. Proc Natl Acad Sci U S A 106:9238–9243 [View Article][PubMed]
    [Google Scholar]
  13. Felczak M. M., Kaguni J. M. ( 2009). DnaAcos hyperinitiates by circumventing regulatory pathways that control the frequency of initiation in Escherichia coli . Mol Microbiol 72:1348–1363 [View Article][PubMed]
    [Google Scholar]
  14. Fishov I., Zaritsky A., Grover N. B. ( 1995). On microbial states of growth. Mol Microbiol 15:789–794 [View Article][PubMed]
    [Google Scholar]
  15. Grigorian A. V., Lustig R. B., Guzmán E. C., Mahaffy J. M., Zyskind J. W. ( 2003). Escherichia coli cells with increased levels of DnaA and deficient in recombinational repair have decreased viability. J Bacteriol 185:630–644 [View Article][PubMed]
    [Google Scholar]
  16. Hanawalt P., Wax R. ( 1964). Transcription of repressed gene: evidence that it requires DNA replication. Science 145:1061–1063 [View Article][PubMed]
    [Google Scholar]
  17. Hansen F. G., Christensen B. B., Atlung T. ( 1991). The initiator titration model: computer simulation of chromosome and minichromosome control. Res Microbiol 142:161–167 [View Article][PubMed]
    [Google Scholar]
  18. Helmstetter C. E. ( 1996). Timing and synthetic activities in the cell cycle. Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology1627–1649 Neidhardt F. C. et al. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  19. Helmstetter C. E., Cummings D. J. ( 1964). An improved method for the selection of bacterial cells at division. Biochim Biophys Acta 82:608–610[PubMed] [CrossRef]
    [Google Scholar]
  20. Helmstetter C. E., Cooper S., Pierucci O., Revelas E. ( 1968). On the bacterial life sequence. Cold Spring Harb Symp Quant Biol 33:809–822[PubMed] [CrossRef]
    [Google Scholar]
  21. Huang K. C., Mukhopadhyay R., Wingreen N. S. ( 2006). A curvature-mediated mechanism for localization of lipids to bacterial poles. PLOS Comput Biol 2:e151 [View Article][PubMed]
    [Google Scholar]
  22. Huls P. G., Vischer N. O., Woldringh C. L. ( 1999). Delayed nucleoid segregation in Escherichia coli . Mol Microbiol 33:959–970 [View Article][PubMed]
    [Google Scholar]
  23. Jiménez-Sanchez A., Guzmán E. C. ( 1988). Direct procedure for the determination of the number of replication forks and the reinitiation fraction in bacteria. Comput Appl Biosci 4:431–433[PubMed]
    [Google Scholar]
  24. Jones N. C., Donachie W. D. ( 1973). Chromosome replication, transcription and control of cell division in Escherichia coli . Nat New Biol 243:100–103[PubMed] [CrossRef]
    [Google Scholar]
  25. Kjeldgaard N. O., Maaløe O., Schaechter M. ( 1958). The transition between different physiological states during balanced growth of Salmonella typhimurium . J Gen Microbiol 19:607–616[PubMed] [CrossRef]
    [Google Scholar]
  26. Koch A. L., Schaechter M. ( 1962). A model for statistics of the cell division process. J Gen Microbiol 29:435–454[PubMed] [CrossRef]
    [Google Scholar]
  27. Leonard A. C., Grimwade J. E. ( 2010). Initiation of DNA replication. EcoSal – Escherichia coli and Salmonella: Cellular and Molecular Biology Böck A. et al. Washington, DC: American Society for Microbiology; http://www.ecosal.org
    [Google Scholar]
  28. Maaløe O., Kjeldgaard N. O. ( 1966). Control of Macromolecular Synthesis New York: W.A. Benjamin;
    [Google Scholar]
  29. Manor H., Deutscher M. P., Littauer U. Z. ( 1971). Rates of DNA chain growth in Escherichia coli . J Mol Biol 61:503–524 [View Article][PubMed]
    [Google Scholar]
  30. Meacock P. A., Pritchard R. H. ( 1975). Relationship between chromosome replication and cell division in a thymineless mutant of Escherichia coli B/r. J Bacteriol 122:931–942[PubMed]
    [Google Scholar]
  31. Michelsen O., Teixeira de Mattos M. J., Jensen P. R., Hansen F. G. ( 2003). Precise determinations of C and D periods by flow cytometry in Escherichia coli K-12 and B/r. Microbiology 149:1001–1010 [View Article][PubMed]
    [Google Scholar]
  32. Nordman J., Skovgaard O., Wright A. ( 2007). A novel class of mutations that affect DNA replication in E. coli . Mol Microbiol 64:125–138 [View Article][PubMed]
    [Google Scholar]
  33. Norris V. ( 1995). Hypothesis: chromosome separation in Escherichia coli involves autocatalytic gene expression, transertion and membrane-domain formation. Mol Microbiol 16:1051–1057 [View Article][PubMed]
    [Google Scholar]
  34. Ohkawa T. ( 1979). Abnormal metabolism of thymidine nucleotides and phosphorylation of deoxycytidine in Escherichia coli C thy ura mutant. Eur J Biochem 100:165–173 [View Article][PubMed]
    [Google Scholar]
  35. Powell E. O. ( 1956). Growth rate and generation time of bacteria, with special reference to continuous culture. J Gen Microbiol 15:492–511[PubMed] [CrossRef]
    [Google Scholar]
  36. Pritchard R. H. ( 1974). Review lecture on the growth and form of a bacterial cell. Philos Trans R Soc Lond B Biol Sci 267:303–336 [View Article][PubMed]
    [Google Scholar]
  37. Pritchard R. H., Zaritsky A. ( 1970). Effect of thymine concentration on the replication velocity of DNA in a thymineless mutant of Escherichia coli . Nature 226:126–131 [View Article][PubMed]
    [Google Scholar]
  38. Pritchard R. H., Barth P. T., Collins J. ( 1969). Control of DNA synthesis in bacteria. Microbial growth. Symp Soc Gen Microbiol 19:263–297
    [Google Scholar]
  39. Rabinovitch A., Zaritsky A., Feingold M. ( 2003). DNA-membrane interactions can localize bacterial cell center. J Theor Biol 225:493–496 [View Article][PubMed]
    [Google Scholar]
  40. Reinhart K. V., Copeland J. C. ( 1973). Evidence that thymine is not a normal metabolite in wild-type Bacillus subtilis . Biochim Biophys Acta 294:1–7 [CrossRef]
    [Google Scholar]
  41. Reyes-Lamothe R., Wang X., Sherratt D. ( 2008a). Escherichia coli and its chromosome. Trends Microbiol 16:238–245 [View Article][PubMed]
    [Google Scholar]
  42. Reyes-Lamothe R., Possoz C., Danilova O., Sherratt D. J. ( 2008b). Independent positioning and action of Escherichia coli replisomes in live cells. Cell 133:90–102 [View Article][PubMed]
    [Google Scholar]
  43. Rudolph C. J., Upton A. L., Lloyd R. G. ( 2009). Replication fork collisions cause pathological chromosomal amplification in cells lacking RecG DNA translocase. Mol Microbiol 74:940–955 [View Article][PubMed]
    [Google Scholar]
  44. Schaechter M., Maaløe O., Kjeldgaard N. O. ( 1958). Dependency on medium and temperature of cell size and chemical composition during balanced grown of Salmonella typhimurium . J Gen Microbiol 19:592–606[PubMed] [CrossRef]
    [Google Scholar]
  45. Simmons L. A., Breier A. M., Cozzarelli N. R., Kaguni J. M. ( 2004). Hyperinitiation of DNA replication in Escherichia coli leads to replication fork collapse and inviability. Mol Microbiol 51:349–358 [View Article][PubMed]
    [Google Scholar]
  46. Slater M., Schaechter M. ( 1974). Control of cell division in bacteria. Bacteriol Rev 38:199–221[PubMed]
    [Google Scholar]
  47. Sueoka N., Yoshikawa H. ( 1965). The chromosome of Bacillus subtilis. I. Theory of marker frequency analysis. Genetics 52:747–757[PubMed]
    [Google Scholar]
  48. Tonthat N. K., Arold S. T., Pickering B. F., Van Dyke M. W., Liang S., Lu Y., Beuria T. K., Margolin W., Schumacher M. A. ( 2011). Molecular mechanism by which the nucleoid occlusion factor, SlmA, keeps cytokinesis in check. EMBO J 30:154–164 [View Article][PubMed]
    [Google Scholar]
  49. Toro E., Shapiro L. ( 2010). Bacterial chromosome organization and segregation. Cold Spring Harb Perspect Biol 2:a000349 [View Article][PubMed]
    [Google Scholar]
  50. Trueba F. J., Woldringh C. L. ( 1980). Changes in cell diameter during the division cycle of Escherichia coli . J Bacteriol 142:869–878[PubMed]
    [Google Scholar]
  51. von Freiesleben U., Krekling M. A., Hansen F. G., Løbner-Olesen A. ( 2000). The eclipse period of Escherichia coli . EMBO J 19:6240–6248 [View Article][PubMed]
    [Google Scholar]
  52. Wold S., Skarstad K., Steen H. B., Stokke T., Boye E. ( 1994). The initiation mass for DNA replication in Escherichia coli K-12 is dependent on growth rate. EMBO J 13:2097–2102[PubMed]
    [Google Scholar]
  53. Woldringh C. L. ( 2002). The role of co-transcriptional translation and protein translocation (transertion) in bacterial chromosome segregation. Mol Microbiol 45:17–29 [View Article][PubMed]
    [Google Scholar]
  54. Woldringh C. L., Jensen P. R., Westerhoff H. V. ( 1995). Structure and partitioning of bacterial DNA: determined by a balance of compaction and expansion forces?. FEMS Microbiol Lett 131:235–242 [View Article][PubMed]
    [Google Scholar]
  55. Zaritsky A. ( 1975). Rate stimulation of deoxyribonucleic acid synthesis after inhibition. J Bacteriol 122:841–846[PubMed]
    [Google Scholar]
  56. Zaritsky A., Pritchard R. H. ( 1973). Changes in cell size and shape associated with changes in the replication time of the chromosome of Escherichia coli . J Bacteriol 114:824–837[PubMed]
    [Google Scholar]
  57. Zaritsky A., Woldringh C. L. ( 1978). Chromosome replication rate and cell shape in Escherichia coli: lack of coupling. J Bacteriol 135:581–587[PubMed]
    [Google Scholar]
  58. Zaritsky A., Woldringh C. L. ( 2003). Localizing cell division in spherical Escherichia coli by nucleoid occlusion. FEMS Microbiol Lett 226:209–214 [View Article][PubMed]
    [Google Scholar]
  59. Zaritsky A., Zabrovitz S. ( 1981). DNA synthesis in Escherichia coli during a nutritional shift-up. Mol Gen Genet 181:564–566 [View Article][PubMed]
    [Google Scholar]
  60. Zaritsky A., Woldringh C. L., Fishov I., Vischer N. O. E., Einav M. ( 1999). Varying division planes of secondary constrictions in spheroidal Escherichia coli cells. Microbiology 145:1015–1022 [View Article][PubMed]
    [Google Scholar]
  61. Zaritsky A., Woldringh C. L., Einav M., Alexeeva S. ( 2006). Use of thymine limitation and thymine starvation to study bacterial physiology and cytology. J Bacteriol 188:1667–1679 [View Article][PubMed]
    [Google Scholar]
  62. Zaritsky A., Vischer N., Rabinovitch A. ( 2007). Changes of initiation mass and cell dimensions by the ‘eclipse’. Mol Microbiol 63:15–21 [View Article][PubMed]
    [Google Scholar]
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