Coordination of two opposite flagella allows high-speed swimming and active turning of individual zoospores

  1. Quang D Tran  Is a corresponding author
  2. Eric Galiana
  3. Philippe Thomen
  4. Céline Cohen
  5. François Orange
  6. Fernando Peruani
  7. Xavier Noblin  Is a corresponding author
  1. Institut Jacques Monod, France
  2. Université Côte d'Azur, France
  3. CY Cergy Paris Université, France

Abstract

Phytophthora species cause diseases in a large variety of plants and represent a serious agricultural threat, leading, every year, to multibillion dollar losses. Infection occurs when these biflagellated zoospores move across the soil at their characteristic high speed and reach the roots of a host plant. Despite the relevance of zoospore spreading in the epidemics of plant diseases, characteristics of individual swimming of zoospores have not been fully investigated. It remains unknown about the characteristics of two opposite beating flagella during translation and turning, and the roles of each flagellum on zoospore swimming. Here, combining experiments and modeling, we show how these two flagella contribute to generate thrust when beating together, and identify the mastigonemes-attached anterior flagellum as the main source of thrust. Furthermore, we find that turning involves a complex active process, in which the posterior flagellum temporarily stops, while the anterior flagellum keeps on beating and changes its gait from sinusoidal waves to power and recovery strokes, similar to Chlamydomonas's breaststroke, to reorient its body to a new direction. Our study is a fundamental step towards a better understanding of the spreading of plant pathogens' motile forms, and shows that the motility pattern of these biflagellated zoospores represents a distinct eukaryotic version of the celebrated 'run-and-tumble' motility class exhibited by peritrichous bacteria.

Data availability

All data generated and simulation files are available via Zenodo using this URL: https://doi.org/10.5281/zenodo.4710633. In the data, we include:(1) datasets of all zoospore positions along multiple trajectories in the experiment of Figure 2,(2) a MATLAB file to compute all the statistical results in Figure 2(D-G),(3) a MATLAB file containing the simulation model presented in Figure 2(H),(4) datasets of zoospore positions, speed, moving directions, body orientations during the turning, presented in Figure 4(A-D).

The following data sets were generated

Article and author information

Author details

  1. Quang D Tran

    CNRS, UMR 7592, Institut Jacques Monod, Paris, France
    For correspondence
    duc-quang.tran@ijm.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5637-0647
  2. Eric Galiana

    INRAE UMR 1355, CNRS UMR 7254, Université Côte d'Azur, Sophia Antipolis, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Philippe Thomen

    INRAE UMR 1355, CNRS UMR 7254, Université Côte d'Azur, Nice, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Céline Cohen

    INRAE UMR 1355, CNRS UMR 7254, Université Côte d'Azur, Nice, France
    Competing interests
    The authors declare that no competing interests exist.
  5. François Orange

    INRAE UMR 1355, CNRS UMR 7254, Université Côte d'Azur, Nice, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Fernando Peruani

    CNRS UMR 8089, CY Cergy Paris Université, Cergy-Pontoise, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Xavier Noblin

    INRAE UMR 1355, CNRS UMR 7254, Université Côte d'Azur, Nice, France
    For correspondence
    xavier.noblin@univ-cotedazur.fr
    Competing interests
    The authors declare that no competing interests exist.

Funding

Centre National de la Recherche Scientifique (ANR-15-IDEX-01)

  • Eric Galiana
  • Xavier Noblin

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Raymond E Goldstein, University of Cambridge, United Kingdom

Version history

  1. Preprint posted: April 23, 2021 (view preprint)
  2. Received: June 12, 2021
  3. Accepted: March 25, 2022
  4. Accepted Manuscript published: March 28, 2022 (version 1)
  5. Accepted Manuscript updated: April 4, 2022 (version 2)
  6. Version of Record published: May 3, 2022 (version 3)

Copyright

© 2022, Tran et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Quang D Tran
  2. Eric Galiana
  3. Philippe Thomen
  4. Céline Cohen
  5. François Orange
  6. Fernando Peruani
  7. Xavier Noblin
(2022)
Coordination of two opposite flagella allows high-speed swimming and active turning of individual zoospores
eLife 11:e71227.
https://doi.org/10.7554/eLife.71227

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https://doi.org/10.7554/eLife.71227