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.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.049403-0
2011-07-01
2020-01-17
Loading full text...

Full text loading...

/deliver/fulltext/micro/157/7/1876.html?itemId=/content/journal/micro/10.1099/mic.0.049403-0&mimeType=html&fmt=ahah

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 Biol60:75–86 [CrossRef][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 Cell18:555–564 [CrossRef][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 Bacteriol180:265–273[PubMed]
    [Google Scholar]
  4. Bleecken S.. ( 1969;). Duplication of the bacterial cell and its initiation. J Theor Biol25:137–158 [CrossRef][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 Bacteriol104:401–409[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 A108:3773–3778 [CrossRef][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 Bacteriol186:2594–2602 [CrossRef][PubMed]
    [Google Scholar]
  8. Dix D. E., Helmstetter C. E.. ( 1973;). Coupling between chromosome completion and cell division in Escherichia coli . J Bacteriol115:786–795[PubMed]
    [Google Scholar]
  9. Donachie W. D.. ( 1968;). Relationship between cell size and time of initiation of DNA replication. Nature219:1077–1079 [CrossRef][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 Biol151:275–287 [CrossRef][PubMed]
    [Google Scholar]
  11. Ephrati-Elizur E., Borenstein S.. ( 1971;). Velocity of chromosome replication in thymine-requiring and independent strains of Bacillus subtilis . J Bacteriol106:58–64[PubMed]
    [Google Scholar]
  12. Erickson H. P.. ( 2009;). Modeling the physics of FtsZ assembly and force generation. Proc Natl Acad Sci U S A106:9238–9243 [CrossRef][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 Microbiol72:1348–1363 [CrossRef][PubMed]
    [Google Scholar]
  14. Fishov I., Zaritsky A., Grover N. B.. ( 1995;). On microbial states of growth. Mol Microbiol15:789–794 [CrossRef][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 Bacteriol185:630–644 [CrossRef][PubMed]
    [Google Scholar]
  16. Hanawalt P., Wax R.. ( 1964;). Transcription of repressed gene: evidence that it requires DNA replication. Science145:1061–1063 [CrossRef][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 Microbiol142:161–167 [CrossRef][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 Acta82:608–610[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 Biol33:809–822[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 Biol2:e151 [CrossRef][PubMed]
    [Google Scholar]
  22. Huls P. G., Vischer N. O., Woldringh C. L.. ( 1999;). Delayed nucleoid segregation in Escherichia coli . Mol Microbiol33:959–970 [CrossRef][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 Biosci4:431–433[PubMed]
    [Google Scholar]
  24. Jones N. C., Donachie W. D.. ( 1973;). Chromosome replication, transcription and control of cell division in Escherichia coli . Nat New Biol243:100–103[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 Microbiol19:607–616[PubMed][CrossRef]
    [Google Scholar]
  26. Koch A. L., Schaechter M.. ( 1962;). A model for statistics of the cell division process. J Gen Microbiol29:435–454[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 Biol61:503–524 [CrossRef][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 Bacteriol122:931–942[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. Microbiology149:1001–1010 [CrossRef][PubMed]
    [Google Scholar]
  32. Nordman J., Skovgaard O., Wright A.. ( 2007;). A novel class of mutations that affect DNA replication in E. coli . Mol Microbiol64:125–138 [CrossRef][PubMed]
    [Google Scholar]
  33. Norris V.. ( 1995;). Hypothesis: chromosome separation in Escherichia coli involves autocatalytic gene expression, transertion and membrane-domain formation. Mol Microbiol16:1051–1057 [CrossRef][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 Biochem100:165–173 [CrossRef][PubMed]
    [Google Scholar]
  35. Powell E. O.. ( 1956;). Growth rate and generation time of bacteria, with special reference to continuous culture. J Gen Microbiol15:492–511[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 Sci267:303–336 [CrossRef][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 . Nature226:126–131 [CrossRef][PubMed]
    [Google Scholar]
  38. Pritchard R. H., Barth P. T., Collins J.. ( 1969;). Control of DNA synthesis in bacteria. Microbial growth. Symp Soc Gen Microbiol19:263–297
    [Google Scholar]
  39. Rabinovitch A., Zaritsky A., Feingold M.. ( 2003;). DNA-membrane interactions can localize bacterial cell center. J Theor Biol225:493–496 [CrossRef][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 Acta294:1–7[CrossRef]
    [Google Scholar]
  41. Reyes-Lamothe R., Wang X., Sherratt D.. ( 2008;a). Escherichia coli and its chromosome. Trends Microbiol16:238–245 [CrossRef][PubMed]
    [Google Scholar]
  42. Reyes-Lamothe R., Possoz C., Danilova O., Sherratt D. J.. ( 2008;b). Independent positioning and action of Escherichia coli replisomes in live cells. Cell133:90–102 [CrossRef][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 Microbiol74:940–955 [CrossRef][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 Microbiol19:592–606[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 Microbiol51:349–358 [CrossRef][PubMed]
    [Google Scholar]
  46. Slater M., Schaechter M.. ( 1974;). Control of cell division in bacteria. Bacteriol Rev38:199–221[PubMed]
    [Google Scholar]
  47. Sueoka N., Yoshikawa H.. ( 1965;). The chromosome of Bacillus subtilis. I. Theory of marker frequency analysis. Genetics52:747–757[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 J30:154–164 [CrossRef][PubMed]
    [Google Scholar]
  49. Toro E., Shapiro L.. ( 2010;). Bacterial chromosome organization and segregation. Cold Spring Harb Perspect Biol2:a000349 [CrossRef][PubMed]
    [Google Scholar]
  50. Trueba F. J., Woldringh C. L.. ( 1980;). Changes in cell diameter during the division cycle of Escherichia coli . J Bacteriol142:869–878[PubMed]
    [Google Scholar]
  51. von Freiesleben U., Krekling M. A., Hansen F. G., Løbner-Olesen A.. ( 2000;). The eclipse period of Escherichia coli . EMBO J19:6240–6248 [CrossRef][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 J13:2097–2102[PubMed]
    [Google Scholar]
  53. Woldringh C. L.. ( 2002;). The role of co-transcriptional translation and protein translocation (transertion) in bacterial chromosome segregation. Mol Microbiol45:17–29 [CrossRef][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 Lett131:235–242 [CrossRef][PubMed]
    [Google Scholar]
  55. Zaritsky A.. ( 1975;). Rate stimulation of deoxyribonucleic acid synthesis after inhibition. J Bacteriol122:841–846[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 Bacteriol114:824–837[PubMed]
    [Google Scholar]
  57. Zaritsky A., Woldringh C. L.. ( 1978;). Chromosome replication rate and cell shape in Escherichia coli: lack of coupling. J Bacteriol135:581–587[PubMed]
    [Google Scholar]
  58. Zaritsky A., Woldringh C. L.. ( 2003;). Localizing cell division in spherical Escherichia coli by nucleoid occlusion. FEMS Microbiol Lett226:209–214 [CrossRef][PubMed]
    [Google Scholar]
  59. Zaritsky A., Zabrovitz S.. ( 1981;). DNA synthesis in Escherichia coli during a nutritional shift-up. Mol Gen Genet181:564–566 [CrossRef][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. Microbiology145:1015–1022 [CrossRef][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 Bacteriol188:1667–1679 [CrossRef][PubMed]
    [Google Scholar]
  62. Zaritsky A., Vischer N., Rabinovitch A.. ( 2007;). Changes of initiation mass and cell dimensions by the ‘eclipse’. Mol Microbiol63:15–21 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.049403-0
Loading
/content/journal/micro/10.1099/mic.0.049403-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error