A flagellate-to-amoeboid switch in the closest living relatives of animals

  1. Thibaut Brunet  Is a corresponding author
  2. Marvin Albert
  3. William Roman
  4. Maxwell C Coyle
  5. Danielle C Spitzer
  6. Nicole King  Is a corresponding author
  1. Howard Hughes Medical Institute, University of California, Berkeley, United States
  2. University of Zürich, Switzerland
  3. Instituto de Medicina Molecular João Lobo Antunes, Portugal
  4. University of California, Berkeley, United States

Abstract

Amoeboid cells are fundamental to animal biology and broadly distributed across animal diversity, but their evolutionary origin is unclear. The closest living relatives of animals, the choanoflagellates, display a polarized cell architecture (with an apical flagellum encircled by microvilli) that closely resembles that of epithelial cells and suggests homology, but this architecture differs strikingly from the deformable phenotype of animal amoeboid cells. Here, we show that choanoflagellates subjected to confinement differentiate into an amoeboid form by retracting their flagella and activating myosin-based motility. This switch allows escape from confinement and is conserved across choanoflagellate diversity. The conservation of the amoeboid cell phenotype across animals and choanoflagellates, together with the conserved role of myosin, is consistent with the homology of amoeboid motility in both lineages. We hypothesize that the differentiation between animal epithelial and crawling cells might have evolved from a stress-induced phenotypic switch between flagellate and amoeboid forms in their single-celled ancestors.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Thibaut Brunet

    Molecular and Cell Biology, Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, United States
    For correspondence
    t.brunet@berkeley.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1843-1613
  2. Marvin Albert

    Department of Molecular Life Sciences, University of Zürich, Zürich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  3. William Roman

    Instituto de Medicina Molecular João Lobo Antunes, Lisbon, Portugal
    Competing interests
    The authors declare that no competing interests exist.
  4. Maxwell C Coyle

    Department of Molecular and Cell Biology, Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Danielle C Spitzer

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4827-1857
  6. Nicole King

    Department of Molecular and Cell Biology, Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, United States
    For correspondence
    nking@berkeley.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6409-1111

Funding

Howard Hughes Medical Institute

  • Nicole King

EMBO (ALTF 1474-2016)

  • Thibaut Brunet

Human Frontiers Science Program (000053/2017-L)

  • Thibaut Brunet

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

Reviewing Editor

  1. Iñaki Ruiz-Trillo, CSIC-Universitat Pompeu Fabra, Spain

Version history

  1. Received: July 14, 2020
  2. Accepted: January 14, 2021
  3. Accepted Manuscript published: January 15, 2021 (version 1)
  4. Version of Record published: February 19, 2021 (version 2)

Copyright

© 2021, Brunet 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. Thibaut Brunet
  2. Marvin Albert
  3. William Roman
  4. Maxwell C Coyle
  5. Danielle C Spitzer
  6. Nicole King
(2021)
A flagellate-to-amoeboid switch in the closest living relatives of animals
eLife 10:e61037.
https://doi.org/10.7554/eLife.61037

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