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

Nature Microbiology volume 2, Article number: 16182 (2016) | Download Citation

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.

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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

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

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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.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Silvia Bulgheresi.

Supplementary information

PDF files

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    Supplementary information

    Supplementary Figures 1–12

Videos

  1. 1.

    Supplementary Video 1

    3D animations of the CLSM-imaged cell shown in Supplementary Figure 10a.

  2. 2.

    Supplementary Video 2

    3D animations of the CLSM-imaged cells shown in Supplementary Figure 10b.

  3. 3.

    Supplementary Video 3

    3D animations of the CLSM-imaged cells shown in Supplementary Figure 10c.

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DOI

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

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