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

Amoeboid cell types 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) th...

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Autores principales: Brunet, Thibaut, Albert, Marvin, Roman, William, Coyle, Maxwell C, Spitzer, Danielle C, King, Nicole
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7895527/
https://www.ncbi.nlm.nih.gov/pubmed/33448265
http://dx.doi.org/10.7554/eLife.61037
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author Brunet, Thibaut
Albert, Marvin
Roman, William
Coyle, Maxwell C
Spitzer, Danielle C
King, Nicole
author_facet Brunet, Thibaut
Albert, Marvin
Roman, William
Coyle, Maxwell C
Spitzer, Danielle C
King, Nicole
author_sort Brunet, Thibaut
collection PubMed
description Amoeboid cell types 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 resembles that of epithelial cells and suggests homology, but this architecture differs strikingly from the deformable phenotype of animal amoeboid cells, which instead evoke more distantly related eukaryotes, such as diverse amoebae. Here, we show that choanoflagellates subjected to confinement become amoeboid 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 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 switch between flagellate and amoeboid forms in their single-celled ancestors.
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spelling pubmed-78955272021-02-22 A flagellate-to-amoeboid switch in the closest living relatives of animals Brunet, Thibaut Albert, Marvin Roman, William Coyle, Maxwell C Spitzer, Danielle C King, Nicole eLife Cell Biology Amoeboid cell types 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 resembles that of epithelial cells and suggests homology, but this architecture differs strikingly from the deformable phenotype of animal amoeboid cells, which instead evoke more distantly related eukaryotes, such as diverse amoebae. Here, we show that choanoflagellates subjected to confinement become amoeboid 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 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 switch between flagellate and amoeboid forms in their single-celled ancestors. eLife Sciences Publications, Ltd 2021-01-15 /pmc/articles/PMC7895527/ /pubmed/33448265 http://dx.doi.org/10.7554/eLife.61037 Text en © 2021, Brunet et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cell Biology
Brunet, Thibaut
Albert, Marvin
Roman, William
Coyle, Maxwell C
Spitzer, Danielle C
King, Nicole
A flagellate-to-amoeboid switch in the closest living relatives of animals
title A flagellate-to-amoeboid switch in the closest living relatives of animals
title_full A flagellate-to-amoeboid switch in the closest living relatives of animals
title_fullStr A flagellate-to-amoeboid switch in the closest living relatives of animals
title_full_unstemmed A flagellate-to-amoeboid switch in the closest living relatives of animals
title_short A flagellate-to-amoeboid switch in the closest living relatives of animals
title_sort flagellate-to-amoeboid switch in the closest living relatives of animals
topic Cell Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7895527/
https://www.ncbi.nlm.nih.gov/pubmed/33448265
http://dx.doi.org/10.7554/eLife.61037
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