A natural toroidal microswimmer with a rotary eukaryotic flagellum

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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.

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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.

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.

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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

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.

Correspondence to Sebastian Hess.

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The authors declare no competing interests.

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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.

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

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