1887

Abstract

In bacteria, DNA replication initiation is tightly regulated in order to coordinate chromosome replication with cell growth. In , positive factors and negative regulatory mechanisms playing important roles in the strict control of DNA replication initiation have been reported. However, it remains unclear how bacterial cells recognize the right time for replication initiation during the cell cycle. In the Gram-positive bacterium , much less is known about the regulation of replication initiation, specifically, regarding negative control mechanisms which ensure replication initiation only once per cell cycle. Here we report that replication initiation was greatly enhanced in strains that had the origin of replication () relocated to various loci on the chromosome. When was relocated to new loci further than 250 kb counterclockwise from the native locus, replication initiation became asynchronous and earlier than in the wild-type cells. In two -relocated strains ( at or , 25 ° or 30 ° on the 36 ° chromosome map, respectively), DnaA levels were higher than in the wild-type but not enough to cause earlier initiation of replication. Our results suggest that the initiation capacity of replication is accumulated well before the actual time of initiation, and its release may be suppressed by a unique DNA structure formed near the native locus.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.030080-0
2009-09-01
2024-12-03
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/9/3070.html?itemId=/content/journal/micro/10.1099/mic.0.030080-0&mimeType=html&fmt=ahah

References

  1. Andrup L., Atlung T., Ogasawara N., Yoshikawa H., Hansen F. G. 1988; Interaction of the Bacillus subtilis DnaA-like protein with the Escherichia coli DnaA protein. J Bacteriol 170:1333–1338
    [Google Scholar]
  2. Atlung T., Hansen F. G. 1993; Three distinct chromosome replication states are induced by increasing concentrations of DnaA protein in Escherichia coli . J Bacteriol 175:6537–6545
    [Google Scholar]
  3. Autret S., Levine A., Vannier F., Fujita Y., Séror S. J. 1999; The replication checkpoint control in Bacillus subtilis: identification of a novel RTP-binding sequence essential for the replication fork arrest after induction of the stringent response. Mol Microbiol 31:1665–1679
    [Google Scholar]
  4. Breier A. M., Grossman A. D. 2007; Whole-genome analysis of the chromosome partitioning and sporulation protein Spo0J (ParB) reveals spreading and origin-distal sites on the Bacillus subtilis chromosome. Mol Microbiol 64:703–718
    [Google Scholar]
  5. Burton K. 1956; A study of the conditions and mechanism of the diphenylamine reaction for the colorimetric estimation of DNA. Biochem J 62:315–323
    [Google Scholar]
  6. Campbell J. L., Kleckner N. 1990; E. coli oriC and the dnaA gene promoter are sequestered from dam methyltransferase following the passage of the chromosomal replication fork. Cell 62:967–979
    [Google Scholar]
  7. Goranov A. I., Kuester-Schoeck E., Wang J. D., Grossman A. D. 2006; Characterization of the global transcriptional responses to different types of DNA damage and disruption of replication in Bacillus subtilis . J Bacteriol 188:5595–5605
    [Google Scholar]
  8. Hassan A. K. M., Moriya S., Ogura M., Tanaka T., Kawamura F., Ogasawara N. 1997; Suppression of initiation defects of chromosome replication in Bacillus subtilis dnaA and oriC-deleted mutants by integration of a plasmid replicon into the chromosomes. J Bacteriol 179:2494–2502
    [Google Scholar]
  9. Hayashi M., Ogura Y., Harry E. J., Ogasawara N., Moriya S. 2005; Bacillus subtilis YabA is involved in determining the timing and synchrony of replication initiation. FEMS Microbiol Lett 247:73–79
    [Google Scholar]
  10. Henckes G., Harper F., Levine A., Vannier F., Séror S. J. 1989; Over-replication of the origin region in the dnaB37 mutant of Bacillus subtilis: post-initiation control of chromosomal replication. Proc Natl Acad Sci U S A 86:8660–8663
    [Google Scholar]
  11. Itaya M., Laffan J. J., Sueoka N. 1992; Physical distance between the site of type II DNA binding to the membrane and oriC on the Bacillus subtilis 168 chromosome. J Bacteriol 174:5466–5470
    [Google Scholar]
  12. Kadoya R., Hassan A. K. M., Kasahara Y., Ogasawara N., Moriya S. 2002; Two separate DNA sequences within oriC participate in accurate chromosome segregation in Bacillus subtilis . Mol Microbiol 45:73–87
    [Google Scholar]
  13. Katayama T., Kubota T., Kurokawa K., Crooke E., Sekimizu K. 1998; The initiator function of DnaA protein is negatively regulated by the sliding clamp of the E. coli chromosomal replicase. Cell 94:61–71
    [Google Scholar]
  14. Kato J., Katayama T. 2001; Hda, a novel DnaA-related protein, regulates the replication cycle in Escherichia coli . EMBO J 20:4253–4262
    [Google Scholar]
  15. Keyamura K., Fujikawa N., Ishida T., Ozaki S., Su'etsugu M., Fujimitsu K., Kagawa W., Yokoyama S., Kurumizaka H., Katayama T. 2007; The interaction of DiaA and DnaA regulates the replication cycle in E. coli by directly promoting ATP DnaA-specific initiation complexes. Genes Dev 21:2083–2099
    [Google Scholar]
  16. Kitagawa R., Ozaki T., Moriya S., Ogawa T. 1998; Negative control of replication initiation by a novel chromosomal locus exhibiting exceptional affinity for Escherichia coli DnaA protein. Genes Dev 12:3032–3043
    [Google Scholar]
  17. Kunst F., Msadek T., Rapoport G. 1994; Signal transduction network controlling degradative enzyme synthesis and competence in Bacillus subtilis . In Regulation of Bacterial Differentiation pp 1–20 Edited by Piggot P. J., Moran C. P. Jr, Youngman P. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  18. Kunst F., Ogasawara N., Moszer I., Albertini A. M., Alloni G., Azevedo V., Bertero M. G., Bessieres P., Bolotin A. other authors 1997; The complete genome sequence of the Gram-positive bacterium Bacillus subtilis . Nature 390:249–256
    [Google Scholar]
  19. Kurokawa K., Nishida S., Emoto A., Sekimizu K., Katayama K. 1999; Replication cycle-coordinated change of the adenine nucleotide-bound forms of DnaA protein in Escherichia coli . EMBO J 18:6642–6652
    [Google Scholar]
  20. Lee P. S., Lin D. C., Moriya S., Grossman A. D. 2003; Effects of the chromosome partitioning protein Spo0J (ParB) on oriC positioning and replication initiation in Bacillus subtilis . J Bacteriol 185:1326–1337
    [Google Scholar]
  21. Levine A., Vannier F., Dehbi M., Henckes G., Séror S. J. 1991; The stringent response blocks DNA replication outside the ori region in Bacillus subtilis and at the origin in Escherichia coli . J Mol Biol 219:605–613
    [Google Scholar]
  22. Levine A., Autret S., Séror S. J. 1995; A checkpoint involving RTP, the replication terminator protein, arrests replication downstream of the origin during the stringent response in Bacillus subtilis . Mol Microbiol 15:287–295
    [Google Scholar]
  23. Lin D. C., Grossman A. D. 1998; Identification and characterization of a bacterial chromosome partitioning site. Cell 92:675–685
    [Google Scholar]
  24. Lindow J. C., Kuwano M., Moriya S., Grossman A. D. 2002; Subcellular localization of the Bacillus subtilis structural maintenance of chromosomes (SMC) protein. Mol Microbiol 46:997–1009
    [Google Scholar]
  25. Løbner-Olesen A., Skarstad K., Hansen F. G., von Meyenburg K., Boye E. 1989; The DnaA protein determines the initiation mass of Escherichia coli K-12. Cell 57:881–889
    [Google Scholar]
  26. Lowry O. H., Rosebrough N. J., Farr A. L., Randall R. J. 1951; Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
    [Google Scholar]
  27. Lu M., Campbell J. L., Boye E., Kleckner N. 1994; SeqA: a negative modulator of replication initiation in E. coli . Cell 77:413–426
    [Google Scholar]
  28. Mercier R., Petit M.-A., Schbath S., Robin S., Karoui M. E., Boccard F., Espeli O. 2008; The MatP/ matS site-specific system organizes the terminus region of the E. coli chromosome into a macrodomain. Cell 135:475–485
    [Google Scholar]
  29. Moriya S., Fukuoka T., Ogasawara N., Yoshikawa H. 1988; Regulation of initiation of the chromosomal replication by DnaA-boxes in the origin region of the Bacillus subtilis chromosome. EMBO J 7:2911–2917
    [Google Scholar]
  30. Moriya S., Kato K., Yoshikawa H., Ogasawara N. 1990; Isolation of a dnaA mutant of Bacillus subtilis defective in initiation of replication: amount of DnaA protein determines cells' initiation potential. EMBO J 9:2905–2910
    [Google Scholar]
  31. Moriya S., Atlung T., Hansen F. G., Yoshikawa H., Ogasawara N. 1992; Cloning of an autonomously replicating sequence ( ars) from the Bacillus subtilis chromosome. Mol Microbiol 6:309–315
    [Google Scholar]
  32. Moriya S., Hassan A. K. M., Kadoya R., Ogasawara N. 1997; Mechanism of anucleate cell production in the oriC-deleted mutants of Bacillus subtilis . DNA Res 4:115–126
    [Google Scholar]
  33. Moriya S., Tsujikawa E., Hassan A. K. M., Asai K., Kodama T., Ogasawara N. 1998; A Bacillus subtilis gene-encoding protein homologous to eukaryotic SMC motor protein is necessary for chromosome partition. Mol Microbiol 29:179–187
    [Google Scholar]
  34. Murray H., Errington J. 2008; Dynamic control of the DNA replication initiation protein DnaA by Soj/ParA. Cell 135:74–84
    [Google Scholar]
  35. Murray H., Ferreira H., Errington J. 2006; The bacterial chromosome segregation protein Spo0J spreads along DNA from parS nucleation sites. Mol Microbiol 61:1352–1361
    [Google Scholar]
  36. Niki H., Yamaichi Y., Hiraga S. 2000; Dynamic organization of chromosomal DNA in Escherichia coli . Genes Dev 14:212–223
    [Google Scholar]
  37. Noirot-Gros M.-F., Dervyn E., Wu L. J., Mervelet P., Errington J., Ehrlich S. D., Noirot P. 2002; An expanded view of bacterial DNA replication. Proc Natl Acad Sci U S A 99:8342–8347
    [Google Scholar]
  38. Noirot-Gros M.-F., Velten M., Yoshimura M., McGovern S., Morimoto T., Ehrlich S. D., Ogasawara N., Polard P., Noirot P. 2006; Functional dissection of YabA, a negative regulator of DNA replication initiation in Bacillus subtilis . Proc Natl Acad Sci U S A 103:2368–2373
    [Google Scholar]
  39. Ogawa T., Yamada Y., Kuroda T., Kishi T., Moriya S. 2002; The datA locus predominantly contributes to the initiator titration mechanism in the control of replication initiation in Escherichia coli . Mol Microbiol 44:1367–1375
    [Google Scholar]
  40. Ogden G. B., Pratt M. J., Schaechter M. 1988; The replication origin of the Escherichia coli chromosome binds to cell membranes only when hemimethylated. Cell 54:127–135
    [Google Scholar]
  41. Ogura Y., Imai Y., Ogasawara N., Moriya S. 2001; Autoregulation of the dnaA–dnaN operon and effects of DnaA protein levels on replication initiation in Bacillus subtilis . J Bacteriol 183:3833–3841
    [Google Scholar]
  42. Ogura Y., Ogasawara N., Harry E. J., Moriya S. 2003; Increasing the ratio of Soj to Spo0J promotes replication initiation in Bacillus subtilis . J Bacteriol 185:6316–6324
    [Google Scholar]
  43. Sargent M. G., Bennett M. F. 1986; Identification of a specific membrane-particle-associated DNA sequence in Bacillus subtilis . J Bacteriol 166:38–43
    [Google Scholar]
  44. Sato Y., McCollum M., McKenzie T., Laffan J., Zuberi A., Sueoka N. 1991; In vitro type II binding of chromosomal DNA to membrane in Bacillus subtilis . J Bacteriol 173:7732–7735
    [Google Scholar]
  45. Soufo C. D., Soufo H. D. J., Noirot-Gros M.-F., Steindorf A., Noirot P., Graumann P. L. 2008; Cell-cycle-dependent spatial sequestration of the DnaA replication initiator protein in Bacillus subtilis . Dev Cell 15:935–941
    [Google Scholar]
  46. Torheim N. K., Boye E., Løbner-Olesen A., Stokke T., Skarstad K. 2000; The Escherichia coli SeqA protein destabilizes mutant DnaA204 protein. Mol Microbiol 37:629–638
    [Google Scholar]
  47. von Meyenburg K., Hansen F. G. 1987; Regulation of chromosome replication.. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology , vol. 2 pp 1555–1577 Edited by Neidhardt F. C., Ingraham J. L., Low K. B., Magasanik B., Schaechter M., Umbarger H. E. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  48. Wang J. D., Berkmen M. B., Grossman A. D. 2007a; Genome-wide coorientation of replication and transcription reduces adverse effects on replication in Bacillus subtilis . Proc Natl Acad Sci U S A 104:5608–5613
    [Google Scholar]
  49. Wang J. D., Sanders G. M., Grossman A. D. 2007b; Nutritional control of elongation of DNA replication by (p)ppGpp. Cell 128:865–875
    [Google Scholar]
  50. Weart R. B., Lee A. H., Chien A.-C., Haeusser D. P., Hill N. S., Levin P. A. 2007; A metabolic sensor governing cell size in bacteria. Cell 130:335–347
    [Google Scholar]
  51. Winston S., Sueoka N. 1980; DNA–membrane association is necessary for initiation of chromosomal and plasmid replication in Bacillus subtilis . Proc Natl Acad Sci U S A 77:2834–2838
    [Google Scholar]
  52. Wu L. J., Errington J. 2002; A large dispersed chromosomal region required for chromosome segregation in sporulating cells of Bacillus subtilis . EMBO J 21:4001–4011
    [Google Scholar]
  53. Yamaguchi K., Yoshikawa H. 1977; Chromosome–membrane association in Bacillus subtilis. III. Isolation and characterization of a DNA-protein complex carrying replication origin markers. J Mol Biol 110:219–253
    [Google Scholar]
  54. Yoshikawa H., Wake G. 1993; Initiation and termination of chromosome replication. . In Bacillus subtilis and other Gram-Positive Bacteria: Biochemistry, Physiology, and Molecular Genetics pp 507–528 Edited by Sonenshein A. L., Hoch J. A, Losick R. Washington, DC: American Society for Microbiology;
    [Google Scholar]
/content/journal/micro/10.1099/mic.0.030080-0
Loading
/content/journal/micro/10.1099/mic.0.030080-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
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