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:

A natural toroidal microswimmer with a rotary eukaryotic flagellum

Nature Microbiology volume 4, pages 1620–1626 (2019)Cite this article

Subjects

Abstract

We describe Idionectes vortex gen. nov., sp. nov., a unicellular microeukaryote that swims by continuous inversion of its surface, similar to a vortex ring. This previously unreported mode of motility approximates a hypothetical concept called the ‘toroidal swimmer’, in which a doughnut-shaped object rotates around its circular axis and travels in the opposite direction to its outer surface motion. During swimming, the flagellum of Idionectes rotates relative to its cell body, which is normally a hallmark of prokaryotic rather than eukaryotic flagella.

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

Fig. 1: Life history stages and phylogenetic position of I. vortex.
Fig. 2: Swimming mechanism of I. vortex.
Fig. 3: Flagellar rotation and cytoskeletal details of I. vortex.

Similar content being viewed by others

Data availability

The SSU ribosomal RNA gene sequence of I. vortex is available in GenBank under accession number MK736991, and transcriptomic RNA sequence read data are available for download from the NCBI Sequence Read Archive database under BioProject accession PRJNA531640.

Code availability

The custom code used for the phylogenomic analyses is available from the authors upon request.

References

  1. Cavalier-Smith, T., Chao, E. E. & Lewis, R. Mol. Phylogenet. Evol. 99, 275–296 (2016).

    Article  Google Scholar 

  2. Kang, S. et al. Mol. Biol. Evol. 34, 2258–2270 (2017).

    Article  CAS  Google Scholar 

  3. Kudryavtsev, A. & Pawlowski, J. Protist 164, 13–23 (2013).

    Article  Google Scholar 

  4. Lahr, D. J., Grant, J., Molestina, R., Katz, L. A. & Anderson, O. R. J. Eukaryot. Microbiol. 62, 444–453 (2015).

    Article  Google Scholar 

  5. Brennen, C. & Winet, H. Annu. Rev. Fluid Mech. 9, 339–398 (1977).

    Article  Google Scholar 

  6. Sleigh, M. A. Protoplasma 164, 45–53 (1991).

    Article  Google Scholar 

  7. Purcell, E. M. Am. J. Phys. 45, 3–11 (1977).

    Article  Google Scholar 

  8. Taylor, G. I. Proc. R. Soc. Lond. A 211, 225–239 (1952).

    Article  Google Scholar 

  9. Thaokar, R. M., Schiessel, H. & Kulic, I. M. Eur. Phys. J. B 60, 325–336 (2007).

    Article  CAS  Google Scholar 

  10. Leshansky, A. M. & Kenneth, O. Phys. Fluids 20, 063104 (2008).

    Article  Google Scholar 

  11. Huang, J. & Fauci, L. Phys. Rev. E 95, 043102 (2017).

    Article  Google Scholar 

  12. Sleigh, M. A. Comp. Biochem. Physiol. 94, 359–364 (1989).

    Article  CAS  Google Scholar 

  13. Day, M. A. Erkenntnis 33, 285–296 (1990).

    Article  Google Scholar 

  14. Berg, H. C. & Anderson, R. A. Nature 245, 380–382 (1973).

    Article  CAS  Google Scholar 

  15. Yubuki, N. & Leander, B. S. Plant J. 75, 230–244 (2013).

    Article  CAS  Google Scholar 

  16. Walker, G., Simpson, A. G., Edgcomb, V., Sogin, M. L. & Patterson, D. J. Eur. J. Protistol. 37, 25–49 (2001).

    Article  Google Scholar 

  17. Singer, S. J. & Nicolson, G. L. Science 175, 720–731 (1972).

    Article  CAS  Google Scholar 

  18. Tamm, S. L. & Tamm, S. Proc. Natl Acad. Sci. USA 71, 4589–4593 (1974).

    Article  CAS  Google Scholar 

  19. Omoto, C. K. & Witman, G. B. Nature 290, 708–710 (1981).

    Article  CAS  Google Scholar 

  20. Chwang, A. T. & Wu, T. Y. Proc. R. Soc. Lond. B 178, 327–346 (1971).

    Article  CAS  Google Scholar 

  21. McFadden, G. I. & Melkonian, M. Phycologia 25, 551–557 (1986).

    Article  CAS  Google Scholar 

  22. Sensen, C. W., Heimann, K. & Melkonian, M. Eur. J. Phycol. 28, 93–97 (1993).

    Article  Google Scholar 

  23. Melkonian, M. & Weber, A. Z. Pflanzenphysiol. 76, 120–129 (1975).

    Article  CAS  Google Scholar 

  24. Schindelin, J. et al. Nat. Methods 9, 676–682 (2012).

    Article  CAS  Google Scholar 

  25. Reynolds, E. S. J. Cell Biol. 17, 208–212 (1963).

    Article  CAS  Google Scholar 

  26. Marin, B., Palm, A., Klingberg, M. & Melkonian, M. Protist 154, 99–145 (2003).

    Article  CAS  Google Scholar 

  27. Hultman, T., Bergh, S., Moks, T. & Uhlén, M. BioTechniques 10, 84–93 (1991).

    CAS  PubMed  Google Scholar 

  28. Marin, B., Klingberg, M. & Melkonian, M. Protist 149, 265–276 (1998).

    Article  CAS  Google Scholar 

  29. Stamatakis, A. Bioinformatics 22, 2688–2690 (2006).

    Article  CAS  Google Scholar 

  30. Bolger, A. M., Lohse, M. & Usadel, B. Bioinformatics 30, 2114–2120 (2014).

    Article  CAS  Google Scholar 

  31. Grabherr, M. G. et al. Nat. Biotechnol. 29, 644–652 (2011).

    Article  CAS  Google Scholar 

  32. Harding, T., Brown, M. W., Simpson, A. G. & Roger, A. J. Genome Biol. Evol. 8, 2241–2258 (2016).

    Article  CAS  Google Scholar 

  33. Katoh, K. & Standley, D. M. Mol. Biol. Evol. 30, 772–780 (2013).

    Article  CAS  Google Scholar 

  34. Criscuolo, A. & Gribaldo, S. BMC Evol. Biol. 10, 210 (2010).

    Article  Google Scholar 

  35. Nguyen, L. T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. Mol. Biol. Evol. 32, 268–274 (2015).

    Article  CAS  Google Scholar 

  36. Minh, B. Q., Nguyen, M. A. T. & von Haeseler, A. Mol. Biol. Evol. 30, 1188–1195 (2013).

    Article  CAS  Google Scholar 

  37. Wang, H. C., Minh, B. Q., Susko, E. & Roger, A. J. Syst. Biol. 67, 216–235 (2017).

    Article  Google Scholar 

Download references

Acknowledgements

We thank M. Kreutz and K. Hoef-Emden for providing natural samples, M. Melkonian and the CCAC for laboratory resources and algal cultures, Labor Dr. Schäffner (Solingen) for access to a field emission scanning electron microscope, and R. Goldstein, A. Rutenberg, A. Speers, A. Leshansky, G. Witman and S. Geimer for discussions and comments on the manuscript. This research was supported by the Studienstiftung des Deutschen Volkes (fellowship to S.H.) and German Research Foundation (DFG grant HE 7560/1-1 to S.H.). The work carried out in A.J.R.’s laboratory was supported by a Discovery Grant (2017-06792) from the Natural Sciences and Engineering Research Council of Canada (NSERC) awarded to A.J.R. The work conducted in A.G.B.S.’s laboratory was supported by NSERC Discovery Grant 298366-2014.

Author information

Author notes

  1. Sebastian Hess

    Present address: Institute of Zoology, University of Cologne, Cologne, Germany

  2. Laura Eme

    Present address: Department of Cell and Molecular Biology, Science for Life Laboratory, Uppsala University, Uppsala, Sweden

Authors and Affiliations

  1. Centre for Comparative Genomics and Evolutionary Bioinformatics, Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, Nova Scotia, Canada

    Sebastian Hess, Laura Eme & Andrew J. Roger

  2. Centre for Comparative Genomics and Evolutionary Bioinformatics, Department of Biology, Dalhousie University, Halifax, Nova Scotia, Canada

    Sebastian Hess & Alastair G. B. Simpson

Authors
  1. Sebastian Hess
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Laura Eme
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andrew J. Roger
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alastair G. B. Simpson
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

S.H. performed the experiments and analysed the microscopy data. S.H. and L.E. performed the phylogenomic analyses. A.G.B.S. and A.J.R. provided the laboratory resources. S.H. and A.G.B.S. wrote the manuscript with input from all co-authors.

Corresponding author

Correspondence to Sebastian Hess.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figs. 1–4, Suppementary Tables 1–7, Supplementary Video legends and Supplementary References.

Reporting Summary

Supplementary Table 8

Taxa and proteins analysed in phylogenomic analyses.

Supplementary Video 1

Tumbling cells of I. vortex, imaged by DIC and shown at natural speed.

Supplementary Video 2

Smooth swimmers of I. vortex, imaged by DIC and shown at natural speed and in slow motion (1/4 natural speed).

Supplementary Video 3

Behaviour of deflected particles at the flagellum of I. vortex, imaged by DIC and shown in slow motion (1/3 natural speed).

Supplementary Video 4

Flagellar fluid layer of I. vortex during swimming, imaged by DIC and shown in slow motion (1/3 natural speed).

Supplementary Video 5

Flow fields of swimming cells visualized by motion tracking of latex microbeads, imaged by DIC with differential background subtraction and shown in slow motion (1/2 natural speed).

Supplementary Video 6

Relative flagellar rotation in I. vortex, imaged by DIC and shown at natural speed and in slow motion (1/4 natural speed).

Supplementary Video 7

Oscillating flagellar tip in rotating cells of I. vortex, imaged by DIC and shown in slow motion (1/3 natural speed).

Supplementary Video 8

Fluid flow around the static flagellum of I. vortex, imaged by DIC with motion tracking and shown at natural speed.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hess, S., Eme, L., Roger, A.J. et al. A natural toroidal microswimmer with a rotary eukaryotic flagellum. Nat Microbiol 4, 1620–1626 (2019). https://doi.org/10.1038/s41564-019-0478-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41564-019-0478-6

This article is cited by

Search

Advanced search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

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