1887

Abstract

(CB15) initiates chromosome replication only in stalked cells and not in swarmers. To better understand this dimorphic control of chromosome replication, we isolated replication origins (s) from freshwater (FWC) and marine (MCS) species. Previous studies implicated integration host factor (IHF) and CcrM DNA methylation sites in replication control. However, IHF and CcrM sites identified in the model FWC CB15 were only conserved among closely related FWCs. DnaA boxes and CtrA binding sites are established CB15 components. CtrA is a two-component regulator that blocks chromosome replication selectively in CB15 swarmers. DnaA boxes and CtrA sites were found in five FWC and three MCS s. Usually, a DnaA box and a CtrA site were paired, suggesting that CtrA binding regulates DnaA activity. We tested this hypothesis by site-directed mutagenesis of an MCS10 which contains only one CtrA binding site overlapping a critical DnaA box. This overlapping site is unique in the whole MCS10 genome. Selective DnaA box mutations decreased replication, while selective CtrA binding site mutations increased replication of MCS10 plasmids. Therefore, both FWC and MCS s use CtrA to repress replication. Despite this similarity, phylogenetic analysis unexpectedly shows that CtrA usage evolved separately among these s. We discuss consensus s and convergent evolution in differentiating bacteria.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.025528-0
2009-04-01
2019-10-22
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/4/1215.html?itemId=/content/journal/micro/10.1099/mic.0.025528-0&mimeType=html&fmt=ahah

References

  1. Abraham, W. R., Strompl, C., Meyer, H., Lindholst, S., Moore, E. R., Christ, R., Vancanneyt, M., Tindall, B. J., Bennasar, A. & other authors ( 1999; ). Phylogeny and polyphasic taxonomy of Caulobacter species. Proposal of Maricaulis gen. nov. with Maricaulis maris (Poindexter) comb. nov. as the type species, and emended description of the genera Brevundimonas and Caulobacter. Int J Syst Bacteriol 49, 1053–1073.[CrossRef]
    [Google Scholar]
  2. Bellefontaine, A.-F., Pierreux, C. E., Mertens, P., Vandenhaute, J., Letesson, J.-J. & De Bolle, X. ( 2002; ). Plasticity of a transcriptional regulatory network among alpha-proteobacteria is supported by the identification of CtrA targets in Brucella abortus. Mol Microbiol 43, 945–960.[CrossRef]
    [Google Scholar]
  3. Bowers, L. M., Shapland, E. B. & Ryan, K. R. ( 2008; ). Who's in charge here? Regulating cell cycle regulators. Curr Opin Microbiol 11, 547–552.[CrossRef]
    [Google Scholar]
  4. Brassinga, A. K. C., Siam, R. & Marczynski, G. T. ( 2001; ). Conserved gene cluster at replication origins of the alpha-proteobacteria Caulobacter crescentus and Rickettsia prowazekii. J Bacteriol 183, 1824–1829.[CrossRef]
    [Google Scholar]
  5. Brassinga, A. K. C., Siam, R., McSween, W., Winkler, H., Wood, D. & Marczynski, G. T. ( 2002; ). Conserved response regulator and IHF binding sites in the alpha-proteobacteria Caulobacter crescentus and Rickettsia prowazekii chromosome replication origins. J Bacteriol 184, 5789–5799.[CrossRef]
    [Google Scholar]
  6. Castilla-Llorente, V., Munoz-Espin, D., Villar, L., Salas, M. & Meijer, W. J. ( 2006; ). Spo0A, the key transcriptional regulator for entrance into sporulation, is an inhibitor of DNA replication. EMBO J 25, 3890–3899.[CrossRef]
    [Google Scholar]
  7. Ditta, G., Stanfield, S., Corbin, D. & Helinski, D. R. ( 1980; ). Broad host range DNA cloning system for Gram-negative bacteria. Proc Natl Acad Sci U S A 77, 7347–7351.[CrossRef]
    [Google Scholar]
  8. Domian, I. J., Quon, K. C. & Shapiro, L. ( 1997; ). Cell type-specific phosphorylation and proteolysis of a transcriptional regulator controls the G1 to S transition in a bacterial cell cycle. Cell 90, 415–424.[CrossRef]
    [Google Scholar]
  9. Fuller, R. S., Funnell, B. E. & Kornberg, A. ( 1984; ). The DnaA protein complex with the E. coli chromosomal replication origin (oriC) and other DNA sites. Cell 38, 889–900.[CrossRef]
    [Google Scholar]
  10. Goodman, S. D., Velten, N. J., Gao, Q., Robinson, S. & Segall, A. M. ( 1999; ). In vitro selection of integration host factor binding sites. J Bacteriol 181, 3246–3255.
    [Google Scholar]
  11. Gorbatyuk, B. & Marczynski, G. T. ( 2001; ). Physiological consequences of blocked Caulobacter crescentus DnaA expression, an essential DNA replication gene. Mol Microbiol 40, 485–497.[CrossRef]
    [Google Scholar]
  12. Gorbatyuk, B. & Marczynski, G. T. ( 2005; ). Regulated degradation of chromosome replication proteins DnaA and CtrA in Caulobacter crescentus. Mol Microbiol 55, 1233–1245.
    [Google Scholar]
  13. Hottes, A. K., Shapiro, L. & McAdams, H. H. ( 2005; ). DnaA coordinates replication initiation and cell cycle transcription in Caulobacter crescentus. Mol Microbiol 58, 1340–1353.[CrossRef]
    [Google Scholar]
  14. Kaguni, J. M. ( 2006; ). DnaA: controlling the initiation of bacterial DNA replication and more. Annu Rev Microbiol 60, 351–371.[CrossRef]
    [Google Scholar]
  15. Laub, M. T., Chen, S. L., Shapiro, L. & McAdams, H. H. ( 2002; ). Genes directly controlled by CtrA, a master regulator of the Caulobacter cell cycle. Proc Natl Acad Sci U S A 99, 4632–4637.[CrossRef]
    [Google Scholar]
  16. Leonard, A. C. & Helmstetter, C. E. ( 1986; ). Cell cycle-specific replication of Escherichia coli minichromosomes. Proc Natl Acad Sci U S A 83, 5101–5105.[CrossRef]
    [Google Scholar]
  17. Li, Z. & Crooke, E. ( 1999; ). Functional analysis of affinity-purified polyhistidine-tagged DnaA protein. Protein Expr Purif 17, 41–48.[CrossRef]
    [Google Scholar]
  18. Marczynski, G. T. & Shapiro, L. ( 1992; ). Cell-cycle control of a cloned chromosomal origin of replication from Caulobacter crescentus. J Mol Biol 226, 959–977.[CrossRef]
    [Google Scholar]
  19. Marczynski, G. T., Lentine, K. & Shapiro, L. ( 1995; ). A developmentally regulated chromosomal origin of replication uses essential transcription elements. Genes Dev 9, 1543–1557.[CrossRef]
    [Google Scholar]
  20. McAdams, H. H. & Shapiro, L. ( 2003; ). A bacterial cell-cycle regulatory network operating in time and space. Science 301, 1874–1877.[CrossRef]
    [Google Scholar]
  21. 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.[CrossRef]
    [Google Scholar]
  22. Mott, M. L. & Berger, J. M. ( 2007; ). DNA replication initiation: mechanisms and regulation in bacteria. Nat Rev Microbiol 5, 343–354.[CrossRef]
    [Google Scholar]
  23. Muir, R. E. & Gober, J. W. ( 2005; ). Role of integration host factor in the transcriptional activation of flagellar gene expression in Caulobacter crescentus. J Bacteriol 187, 949–960.[CrossRef]
    [Google Scholar]
  24. Nierman, W. C., Feldblyum, T. V., Laub, M. T., Paulsen, I. T., Nelson, K. E., Eisen, J., Heidelberg, J. F., Alley, M. R. K., Ohta, N. & other authors ( 2001; ). Complete genome sequence of Caulobacter crescentus. Proc Natl Acad Sci U S A 98, 4136–4141.[CrossRef]
    [Google Scholar]
  25. Ogasawara, N., Moriya, S. & Yoshikawa, H. ( 1991; ). Initiation of chromosome replication: structure and function of oriC and DnaA protein in eubacteria. Res Microbiol 142, 851–859.[CrossRef]
    [Google Scholar]
  26. Ouimet, M.-C. & Marczynski, G. T. ( 2000; ). Analysis of a cell-cycle promoter bound by a response regulator. J Mol Biol 302, 761–775.[CrossRef]
    [Google Scholar]
  27. Quon, K. C., Yang, B., Domian, I. J., Shapiro, L. & Marczynski, G. T. ( 1998; ). Negative control of bacterial DNA replication by a cell cycle regulatory protein that binds at the chromosome origin. Proc Natl Acad Sci U S A 95, 120–125.[CrossRef]
    [Google Scholar]
  28. Reisenauer, A., Kahng, L. S., McCollum, S. & Shapiro, L. ( 1999; ). Bacterial DNA methylation: a cell cycle regulator? J Bacteriol 181, 5135–5139.
    [Google Scholar]
  29. Siam, R. & Marczynski, G. T. ( 2000; ). Cell cycle regulator phosphorylation stimulates two distinct modes of binding at a chromosome replication origin. EMBO J 19, 1138–1147.[CrossRef]
    [Google Scholar]
  30. Siam, R., Brassinga, A. K. & Marczynski, G. T. ( 2003; ). A dual binding site for integration host factor and the response regulator CtrA inside the Caulobacter crescentus replication origin. J Bacteriol 185, 5563–5572.[CrossRef]
    [Google Scholar]
  31. Sibley, C. D., MacLellan, S. R. & Finan, T. ( 2006; ). The Sinorhizobium meliloti chromosomal origin of replication. Microbiology 152, 443–455.[CrossRef]
    [Google Scholar]
  32. Smith, D. W., Garland, A. M., Herman, G., Enns, R. E., Baker, T. A. & Zyskind, J. W. ( 1985; ). Importance of state of methylation of oriC GATC sites in initiation of DNA replication in Escherichia coli. EMBO J 4, 1319–1326.
    [Google Scholar]
  33. Stahl, D. A., Key, R., Flesher, B. & Smit, J. ( 1992; ). The phylogeny of marine and freshwater caulobacters reflects their habitat. J Bacteriol 174, 2193–2198.
    [Google Scholar]
  34. Stephens, C. M., Zweiger, G. & Shapiro, L. ( 1995; ). Coordinate cell cycle control of a Caulobacter DNA methyltransferase and the flagellar genetic hierarchy. J Bacteriol 177, 1662–1669.
    [Google Scholar]
  35. Stephens, C. M., Reisenauer, A., Wright, R. & Shapiro, L. ( 1996; ). A cell cycle-regulated bacterial DNA methyltransferase is essential for viability. Proc Natl Acad Sci U S A 93, 1210–1214.[CrossRef]
    [Google Scholar]
  36. Wright, R., Stephens, C. & Shapiro, L. ( 1997; ). The CcrM DNA methyltransferase is widespread in the alpha subdivision of proteobacteria, and its essential functions are conserved in Rhizobium meliloti and Caulobacter crescentus. J Bacteriol 179, 5869–5877.
    [Google Scholar]
  37. Wu, J., Ohta, N. & Newton, A. ( 1998; ). An essential, multicomponent signal transduction pathway required for cell cycle regulation in Caulobacter. Proc Natl Acad Sci U S A 95, 1443–1448.[CrossRef]
    [Google Scholar]
  38. Zakrzewska-Czerwinska, J., Jakimowicz, D., Zawilak-Pawlik, A. & Messer, W. ( 2007; ). Regulation of the initiation of chromosomal replication in bacteria. FEMS Microbiol Rev 31, 378–387.[CrossRef]
    [Google Scholar]
  39. Zyskind, J. W., Cleary, J. M., Brusilow, W. S. A., Harding, N. E. & Smith, D. W. ( 1983; ). Chromosome replication origin from the marine bacterium Vibrio harveyi functions in Escherichia coli: oriC consensus sequence. Proc Natl Acad Sci U S A 80, 1164–1168.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.025528-0
Loading
/content/journal/micro/10.1099/mic.0.025528-0
Loading

Data & Media loading...

Supplements

[PDF file](19 KB)

PDF

[PDF file](410 KB)

PDF

[PDF file](86 KB)

PDF

[PDF file](19 KB)

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