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.

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.

Metrics

  • 2,026
    views
  • 297
    downloads
  • 9
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Share this article

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

Further reading

    1. Microbiology and Infectious Disease
    Louise Tzung-Harn Hsieh, Belinda S Hall ... Rachel E Simmonds
    Research Article

    The drivers of tissue necrosis in Mycobacterium ulcerans infection (Buruli ulcer disease) have historically been ascribed solely to the directly cytotoxic action of the diffusible exotoxin, mycolactone. However, its role in the clinically evident vascular component of disease aetiology remains poorly explained. We have now dissected mycolactone’s effects on human primary vascular endothelial cells in vitro. We show that mycolactone-induced changes in endothelial morphology, adhesion, migration, and permeability are dependent on its action at the Sec61 translocon. Unbiased quantitative proteomics identified a profound effect on proteoglycans, driven by rapid loss of type II transmembrane proteins of the Golgi, including enzymes required for glycosaminoglycan (GAG) synthesis, combined with a reduction in the core proteins themselves. Loss of the glycocalyx is likely to be of particular mechanistic importance, since knockdown of galactosyltransferase II (beta-1,3-galactotransferase 6; B3GALT6), the GAG linker-building enzyme, phenocopied the permeability and phenotypic changes induced by mycolactone. Additionally, mycolactone depleted many secreted basement membrane components and microvascular basement membranes were disrupted in vivo during M. ulcerans infection in the mouse model. Remarkably, exogenous addition of laminin-511 reduced endothelial cell rounding, restored cell attachment and reversed the defective migration caused by mycolactone. Hence supplementing mycolactone-depleted extracellular matrix may be a future therapeutic avenue, to improve wound healing rates.

    1. Biochemistry and Chemical Biology
    2. Microbiology and Infectious Disease
    Ana Patrícia Graça, Vadim Nikitushkin ... Gerald Lackner
    Research Article

    Mycofactocin is a redox cofactor essential for the alcohol metabolism of mycobacteria. While the biosynthesis of mycofactocin is well established, the gene mftG, which encodes an oxidoreductase of the glucose-methanol-choline superfamily, remained functionally uncharacterized. Here, we show that MftG enzymes are almost exclusively found in genomes containing mycofactocin biosynthetic genes and are present in 75% of organisms harboring these genes. Gene deletion experiments in Mycolicibacterium smegmatis demonstrated a growth defect of the ∆mftG mutant on ethanol as a carbon source, accompanied by an arrest of cell division reminiscent of mild starvation. Investigation of carbon and cofactor metabolism implied a defect in mycofactocin reoxidation. Cell-free enzyme assays and respirometry using isolated cell membranes indicated that MftG acts as a mycofactocin dehydrogenase shuttling electrons toward the respiratory chain. Transcriptomics studies also indicated remodeling of redox metabolism to compensate for a shortage of redox equivalents. In conclusion, this work closes an important knowledge gap concerning the mycofactocin system and adds a new pathway to the intricate web of redox reactions governing the metabolism of mycobacteria.