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.

  • Brief Communication
  • Published:

Asynchronous division by non-ring FtsZ in the gammaproteobacterial symbiont of Robbea hypermnestra

Nature Microbiology volume 2, Article number: 16182 (2017) Cite this article

Subjects

Abstract

The reproduction mode of uncultivable microorganisms deserves investigation as it can largely diverge from conventional transverse binary fission. Here, we show that the rod-shaped gammaproteobacterium thriving on the surface of the Robbea hypermnestra nematode divides by FtsZ-based, non-synchronous invagination of its poles—that is, the host-attached and fimbriae-rich pole invaginates earlier than the distal one. We conclude that, in a naturally occurring animal symbiont, binary fission is host-oriented and does not require native FtsZ to polymerize into a ring at any septation stage.

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: Asynchronicity of Rhs cell fission and polarity.
Figure 2: Rhs FtsZ localization pattern.

Similar content being viewed by others

References

  1. Leisch, N. et al. Curr. Biol. 22, R831–R832 (2012).

    Article  CAS  Google Scholar 

  2. Pende, N. et al. Nat. Commun. 5, 4803 (2014).

    Article  CAS  Google Scholar 

  3. Bulgheresi, S. Environ. Microbiol. 18, 2305–2318 (2016).

    Article  Google Scholar 

  4. Margolin, W. Nat. Rev. Mol. Cell Biol. 6, 862–871 (2005).

    Article  CAS  Google Scholar 

  5. Bi, E. F. & Lutkenhaus, J. Nature 354, 161–164 (1991).

    Article  CAS  Google Scholar 

  6. Adams, D. W. & Errington, J. Nat. Rev. Microbiol. 7, 642–653 (2009).

    Article  CAS  Google Scholar 

  7. de Boer, P. A. Curr. Opin. Microbiol. 13, 730–737 (2010).

    Article  CAS  Google Scholar 

  8. Erickson, H. P., Anderson, D. E. & Osawa, M. Microbiol. Mol. Biol. Rev. 74, 504–528 (2010).

    Article  CAS  Google Scholar 

  9. Mingorance, J., Rivas, G., Vélez, M., Gómez-Puertas, P. & Vicente, M. Trends Microbiol. 18, 348–356 (2010).

    Article  CAS  Google Scholar 

  10. Osawa, M. & Erickson, H. P. Proc. Natl Acad. Sci. USA 110, 11000–11004 (2013).

    Article  CAS  Google Scholar 

  11. Coltharp, C., Buss, J., Plumer, T. M. & Xiao, J. Proc. Natl Acad. Sci. USA 113, E1044–E1053 (2016).

    Article  CAS  Google Scholar 

  12. Milam, S. L., Osawa, M. & Erickson, H. P. Biophys. J. 103, 59–68 (2012).

    Article  CAS  Google Scholar 

  13. Szwedziak, P., Wang, Q., Bharat, T. A., Tsim, M. & Lowe, J. eLife 3, 642 (2014).

    Article  Google Scholar 

  14. Haeusser, D. P. & Margolin, W. Nat. Rev. Microbiol. 14, 305–319 (2016).

    Article  CAS  Google Scholar 

  15. Bayer, C. et al. Environ. Microbiol. Rep. 1, 136–144 (2009).

    Article  CAS  Google Scholar 

  16. Ott, J. A., Gruber-Vodicka, H. R., Leisch, N. & Zimmermann, J. Syst. Biodivers. 12, 434–455 (2014).

    Article  Google Scholar 

  17. Klemm, P. Eur. J. Biochem. 117, 617–627 (1981).

    Article  CAS  Google Scholar 

  18. Bakker, D., Willemsen, P. T., Simons, L. H., van Zijderveld, F. G. & de Graaf, F. K. Mol. Microbiol. 6, 247–255 (1992).

    Article  CAS  Google Scholar 

  19. Xia, P., Song, Y., Zou, Y., Yang, Y. & Zhu, G. J. Basic Microbiol. 55, 1118–1124 (2015).

    Article  CAS  Google Scholar 

  20. Westerlund-Wikström, B. & Korhonen, T. K. Int. J. Med. Microbiol. 295, 479–486 (2005).

    Article  Google Scholar 

  21. Krogfelt, K. A. Rev. Infect. Dis. 13, 721–735 (1991).

    Article  CAS  Google Scholar 

  22. Sung, M. A., Fleming, K., Chen, H. A. & Matthews, S. EMBO Rep. 2, 621–627 (2001).

    Article  CAS  Google Scholar 

  23. Van den Broeck, W., Cox, E., Oudega, B. & Goddeeris, B. M. Vet. Microbiol. 71, 223–244 (2000).

    Article  CAS  Google Scholar 

  24. Van Gerven, N., De Greve, H. & Hernalsteens, J. P. A. Van Leeuw. J. Microb. 93, 219–226 (2008).

    Article  CAS  Google Scholar 

  25. Holden, S. J. et al. Proc. Natl Acad. Sci. USA 111, 4566–4571 (2014).

    Article  CAS  Google Scholar 

  26. Sato, M. et al. Planta 229, 781–791 (2009).

    Article  CAS  Google Scholar 

  27. Zaritsky, A. et al. Biochimie 81, 897–900 (1999).

    Article  CAS  Google Scholar 

  28. Addinall, S. G. & Lutkenhaus, J. Mol. Microbiol. 22, 231–237 (1996).

    Article  CAS  Google Scholar 

  29. Li, Z., Trimble, M. J., Brun, Y. V. & Jensen, G. J. EMBO J. 26, 4694–4708 (2007).

    Article  CAS  Google Scholar 

  30. den Blaauwen, T., Andreu, J. M. & Monasterio, O. Bioorg. Chem. 55, 27–38 (2014).

    Article  CAS  Google Scholar 

  31. Montanaro, J., Gruber, D. & Leisch, N. PeerJ 4, e1860 (2016).

    Article  Google Scholar 

  32. den Blaauwen, T., Aarsman, M. E. G. Vischer, N. O. E. & Nanninga, N. Mol. Microbiol. 47, 539–547 (2003).

    Article  CAS  Google Scholar 

  33. Schizas, N. V., Street, G. T., Coull, B. C., Chandler, G. T. & Quattro, J. M. Mol. Mar. Biol. Biotech. 6, 381–383 (1997).

    CAS  Google Scholar 

  34. Vischer, N. O. et al. Front. Microbiol. 6, 586 (2015).

    Article  Google Scholar 

  35. Koppelman, C. et al. Mol. Microbiol. 51, 645–657 (2004).

    Article  CAS  Google Scholar 

  36. Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. Nat. Meth. 9, 671–675 (2012).

    Article  CAS  Google Scholar 

  37. van der Ploeg, R. et al. Mol. Microbiol. 87, 1074–1087 (2013).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Austrian Science Fund (FWF) project P22470 (N.L. and S.B.), a uni:docs fellowship from the University of Vienna (N.P.), PhD completion grant 2014 of the University of Vienna (N.L.), the Max Planck Society (N.L. and H.R.G-V.), an ERC grant (N.L.) and by FWF project P28593 (P.M.W.). The authors acknowledge the Cell Imaging and Ultrastructure Research Core Facility of the University of Vienna and the Van Leeuwenhoek Centre for Advanced Microscopy of the University of Amsterdam for technical support. The authors thank J. A. Ott for providing some of the specimens, M. Loose and three anonymous reviewers for helping to improve the manuscript, and the Department of Ecogenomics & Systems Biology (University of Vienna) for inspiring discussions. This work is contribution 991 from the Carrie Bow Cay Laboratory, Caribbean Coral Reef Ecosystem Program, National Museum of Natural History, Washington DC.

Author information

Authors and Affiliations

  1. Department of Ecogenomics and Systems Biology, Archaeal Biology and Ecogenomics Division, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria

    Nikolaus Leisch, Nika Pende, Philipp M. Weber, Sophie S. Abby & Silvia Bulgheresi

  2. Max Planck Institute for Marine Microbiology, Celsiusstrasse 1, D-28359 Bremen, Germany

    Nikolaus Leisch, Harald R. Gruber-Vodicka & Benedikt Geier

  3. Bacterial Cell Biology, Swammerdam Institute of Life Sciences, Faculty of Science, University of Amsterdam, Boelelaan 1108, 1081 HZ Amsterdam, Netherlands

    Jolanda Verheul, Norbert O. E. Vischer & Tanneke den Blaauwen

Authors
  1. Nikolaus Leisch
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nika Pende
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Philipp M. Weber
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Harald R. Gruber-Vodicka
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jolanda Verheul
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Norbert O. E. Vischer
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sophie S. Abby
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Benedikt Geier
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Tanneke den Blaauwen
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Silvia Bulgheresi
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

N.L. conceived and designed some of the experiments, performed experiments, analysed the data, contributed materials and wrote a first draft of the paper. N.P. performed experiments, analysed the data, contributed materials. P.M.W. performed experiments and analysed the data. H.R.G.V. contributed materials. J.V. performed experiments. N.V. and S.S.A. contributed analysis tools. B.G. analysed the data. T.d.B. analysed the data, contributed analysis tools, and assessed and commented on the results and conclusions. S.B. conceived and designed the study, contributed materials and wrote the paper.

Corresponding author

Correspondence to Silvia Bulgheresi.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary information

Supplementary Figures 1–12 (PDF 1479 kb)

Supplementary Video 1

3D animations of the CLSM-imaged cell shown in Supplementary Figure 10a. (MPG 32226 kb)

Supplementary Video 2

3D animations of the CLSM-imaged cells shown in Supplementary Figure 10b. (MPG 31515 kb)

Supplementary Video 3

3D animations of the CLSM-imaged cells shown in Supplementary Figure 10c. (MPG 29664 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Leisch, N., Pende, N., Weber, P. et al. Asynchronous division by non-ring FtsZ in the gammaproteobacterial symbiont of Robbea hypermnestra. Nat Microbiol 2, 16182 (2017). https://doi.org/10.1038/nmicrobiol.2016.182

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/nmicrobiol.2016.182

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