Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Cell division licensing in the multi-chromosomal Vibrio cholerae bacterium

Nature Microbiology volume 1, Article number: 16094 (2016) Cite this article

Subjects

Abstract

Cell division must be coordinated with chromosome replication and segregation to ensure the faithful transmission of genetic information during proliferation. In most bacteria, assembly of the division apparatus, the divisome, starts with the polymerization of a tubulin homologue, FtsZ, into a ring-like structure at mid-cell, the Z-ring1. It typically occurs at half of the cell cycle when most of the replication and segregation cycle of the unique chromosome they generally harbour is achieved2. The chromosome itself participates in the regulation of cell division, at least in part because it serves as a scaffold to position FtsZ polymerization antagonists3. However, about 10% of bacteria have more than one chromosome4, which raises questions about the way they license cell division3. For instance, the genome of Vibrio cholerae, the agent of cholera, is divided between a 3 Mbp replicon that originates from the chromosome of its mono-chromosomal ancestor, Chr1, and a 1 Mbp plasmid-derived replicon, Chr2 (ref. 5). Here, we show that Chr2 harbours binding motifs for an inhibitor of Z-ring formation, which helps accurately position the V. cholerae divisome at mid-cell and postpones its assembly to the very end of the cell cycle.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Cell cycle choreography of V. cholerae FtsZ.
Figure 2: FtsZ localization in ΔminCD and ΔslmA V. cholerae cells.
Figure 3: V. cholerae SlmA binding sites genomic distribution and cell cycle choreography.
Figure 4: Altering the replication and segregation cycle of Chr2 perturbs the V. cholerae cell cycle.

Similar content being viewed by others

References

  1. Bi, E. F. & Lutkenhaus, J. FtsZ ring structure associated with division in Escherichia coli. Nature 354, 161–164 (1991).

    Article  Google Scholar 

  2. den Blaauwen, T. Prokaryotic cell division: flexible and diverse. Curr. Opin. Microbiol. 16, 738–744 (2013).

    Article  Google Scholar 

  3. Adams, D. W., Wu, L. J. & Errington, J. Cell cycle regulation by the bacterial nucleoid. Curr. Opin. Microbiol. 22, 94–101 (2014).

    Article  Google Scholar 

  4. Val, M.-E., Soler-Bistué, A., Bland, M. J. & Mazel, D. Management of multipartite genomes: the Vibrio cholerae model. Curr. Opin. Microbiol. 22, 120–126 (2014).

    Article  Google Scholar 

  5. Heidelberg, J. F. et al. DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406, 477–483 (2000).

    Article  Google Scholar 

  6. Srivastava, P., Fekete, R. A. & Chattoraj, D. K. Segregation of the replication terminus of the two Vibrio cholerae chromosomes. J. Bacteriol. 188, 1060–1070 (2006).

    Article  Google Scholar 

  7. Val, M.-E. et al. FtsK-dependent dimer resolution on multiple chromosomes in the pathogen Vibrio cholerae. PLoS Genet. 4, e1000201 (2008).

    Article  Google Scholar 

  8. Demarre, G., Galli, E. & Barre, F.-X. The ftsK family of DNA pumps. Adv. Exp. Med. Biol. 767, 245–262 (2013).

    Article  Google Scholar 

  9. De Boer, P. A., Crossley, R. E. & Rothfield, L. I. A division inhibitor and a topological specificity factor coded for by the minicell locus determine proper placement of the division septum in E. coli. Cell 56, 641–649 (1989).

    Article  Google Scholar 

  10. Ortiz, C., Natale, P., Cueto, L. & Vicente, M. The keepers of the ring: regulators of FtsZ assembly. FEMS Microbiol. Rev. 40, 57–67 (2016).

    Article  Google Scholar 

  11. Lutkenhaus, J. Assembly dynamics of the bacterial MinCDE system and spatial regulation of the Z ring. Annu. Rev. Biochem. 76, 539–562 (2007).

    Article  Google Scholar 

  12. David, A. et al. The two cis-acting sites, parS1 and oriC1, contribute to the longitudinal organisation of Vibrio cholerae chromosome I. PLoS Genet. 10, e1004448 (2014).

    Article  Google Scholar 

  13. Fogel, M. A. & Waldor, M. K. A dynamic, mitotic-like mechanism for bacterial chromosome segregation. Genes Dev. 20, 3269–3282 (2006).

    Article  Google Scholar 

  14. Demarre, G. et al. Differential management of the replication terminus regions of the two Vibrio cholerae chromosomes during cell division. PLoS Genet. 10, e1004557 (2014).

    Article  Google Scholar 

  15. Mercier, R. et al. The MatP/matS site-specific system organizes the terminus region of the E. coli chromosome into a macrodomain. Cell 135, 475–485 (2008).

    Article  Google Scholar 

  16. Woldringh, C. L., Mulder, E., Huls, P. G. & Vischer, N. Toporegulation of bacterial division according to the nucleoid occlusion model. Res. Microbiol. 142, 309–320 (1991).

    Article  Google Scholar 

  17. Bernhardt, T. G. & de Boer, P. A. SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over chromosomes in E. coli. Mol. Cell 18, 555–564 (2005).

    Article  Google Scholar 

  18. Val, M.-E., Skovgaard, O., Ducos-Galand, M., Bland, M. J. & Mazel, D. Genome engineering in Vibrio cholerae: a feasible approach to address biological issues. PLoS Genet. 8, e1002472 (2012).

    Article  Google Scholar 

  19. Cambridge, J., Blinkova, A., Magnan, D., Bates, D. & Walker, J. R. A replication-inhibited unsegregated nucleoid at mid-cell blocks Z-ring formation and cell division independently of SOS and the SlmA nucleoid occlusion protein in Escherichia coli. J. Bacteriol. 196, 36–49 (2014).

    Article  Google Scholar 

  20. Bailey, M. W., Bisicchia, P., Warren, B. T., Sherratt, D. J. & Männik, J. Evidence for divisome localization mechanisms independent of the Min system and SlmA in Escherichia coli. PLoS Genet. 10, e1004504 (2014).

    Article  Google Scholar 

  21. Rasmussen, T., Jensen, R. B. & Skovgaard, O. The two chromosomes of Vibrio cholerae are initiated at different time points in the cell cycle. EMBO J. 26, 3124–3131 (2007).

    Article  Google Scholar 

  22. Sliusarenko, O., Heinritz, J., Emonet, T. & Jacobs-Wagner, C. High-throughput, subpixel precision analysis of bacterial morphogenesis and intracellular spatio-temporal dynamics. Mol. Microbiol. 80, 612–627 (2011).

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank M.-E. Val and D. Mazel for the gift of strain MCH1 and N. Dubarry and the other team members for insightful comments. The authors acknowledge financial support from the European Research Council under the European Community's Seventh Framework Programme (FP7/2007-2013 grant agreement no. 281590), the Fondation Bettencourt Schueller (2012 Coup d'Elan award) and the ‘Lidex-Biologie Intégrative des Génomes’ project of the Paris-Saclay IDEX (ANR-11-IDEX-0003-02). The light microscopy facility of Imagerie-Gif is a member of the Infrastructures en Biologie Santé et Agronomie (IBiSA), and is supported by the French national Research Agency under Investments for the Future programmes ‘France-BioImaging’ and the Labex ‘Saclay Plant Science’ (ANR-10-INSB-04-01 and ANR-11-IDEX-0003-02, respectively).

Author information

Authors and Affiliations

  1. Institute for Integrative Biology of the Cell (I2BC), Université Paris-Saclay, CEA, CNRS, Université Paris Sud, 1 avenue de la Terrasse, 91198 Gif sur Yvette, France

    Elisa Galli, Mickaël Poidevin, Romain Le Bars, Jean-Michel Desfontaines, Leila Muresan, Evelyne Paly, Yoshiharu Yamaichi & François-Xavier Barre

Authors
  1. Elisa Galli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mickaël Poidevin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Romain Le Bars
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jean-Michel Desfontaines
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Leila Muresan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Evelyne Paly
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yoshiharu Yamaichi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. François-Xavier Barre
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

E.G., M.P., Y.Y. and F.X.B. conceived and designed the experiments. E.G., M.P., R.L.B. and E.P. performed the experiments. E.G., M.P., Y.Y., J.-M.D. and F.X.B. analysed the data. E.G., J.-M.D. and L.M. contributed reagents/materials/analysis tools. E.G., M.P., Y.Y. and F.X.B. wrote the paper.

Corresponding author

Correspondence to François-Xavier Barre.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary information

Supplementary Figures 1-10, Supplementary Tables 1-5 and Supplementary References. (PDF 7635 kb)

Supplementary Video 1

3D FtsZ-mEos2 structures throughout the V. cholerae cell cycle observed using PALM. Cells grown in M9 minimal medium supplemented with 0.2% fructose and 1 µg ml−1 thiamine. (MP4 6440 kb)

Supplementary Video 2

Time-lapse analysis of MinD-YGFP localization in V. cholerae cells. One frame was taken every 20 seconds. Cells grown in M9 minimal medium supplemented with 0.2% fructose and 1 µg ml−1 thiamine (AVI 190 kb)

Supplementary Video 3

Time-lapse analysis of MinD-YGFP and FtsZ-RFPT localization in V. cholerae cells. One frame was taken every 20 seconds. Cells grown in M9 minimal medium supplemented with 0.2% fructose and 1 µg ml−1 thiamine. (AVI 207 kb)

Supplementary Video 4

Mini-cell formation in MCH1. One frame was taken every 3 minutes. Cells were grown in LB (AVI 115 kb)

Supplementary Video 5

Formation of an anucleate cell after a highly asymmetric division in MCH1. Genomic DNA is labelled with a HUα-RFPT fusion. One frame was taken every 3 minutes. Cells grown in M9 minimal medium supplemented with 0.2% fructose and 1 µg ml−1 thiamine. (AVI 55 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Galli, E., Poidevin, M., Le Bars, R. et al. Cell division licensing in the multi-chromosomal Vibrio cholerae bacterium. Nat Microbiol 1, 16094 (2016). https://doi.org/10.1038/nmicrobiol.2016.94

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/nmicrobiol.2016.94

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing