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...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2021-01-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/61037 |
| _version_ | 1811181062584270848 |
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| author | Thibaut Brunet Marvin Albert William Roman Maxwell C Coyle Danielle C Spitzer Nicole King |
| author_facet | Thibaut Brunet Marvin Albert William Roman Maxwell C Coyle Danielle C Spitzer Nicole King |
| author_sort | Thibaut Brunet |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-04-11T09:12:12Z |
| format | Article |
| id | doaj.art-eb91b66f99144b5abd0c4b481927da0d |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T09:12:12Z |
| publishDate | 2021-01-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-eb91b66f99144b5abd0c4b481927da0d2022-12-22T04:32:28ZengeLife Sciences Publications LtdeLife2050-084X2021-01-011010.7554/eLife.61037A flagellate-to-amoeboid switch in the closest living relatives of animalsThibaut Brunet0https://orcid.org/0000-0002-1843-1613Marvin Albert1William Roman2Maxwell C Coyle3Danielle C Spitzer4https://orcid.org/0000-0003-4827-1857Nicole King5https://orcid.org/0000-0002-6409-1111Howard Hughes Medical Institute, Chevy Chase, United States; Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United StatesDepartment of Molecular Life Sciences, University of Zürich, Zurich, SwitzerlandDepartment of Experimental and Health Sciences, Pompeu Fabra University (UPF), CIBERNED, Barcelona, SpainHoward Hughes Medical Institute, Chevy Chase, United States; Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United StatesDepartment of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United StatesHoward Hughes Medical Institute, Chevy Chase, United States; Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United StatesAmoeboid 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.https://elifesciences.org/articles/61037choanoflagellatesSalpingoeca rosettacell type evolutioncellular proprioceptionanimal originstransdifferentiation |
| spellingShingle | Thibaut Brunet Marvin Albert William Roman Maxwell C Coyle Danielle C Spitzer Nicole King A flagellate-to-amoeboid switch in the closest living relatives of animals eLife choanoflagellates Salpingoeca rosetta cell type evolution cellular proprioception animal origins transdifferentiation |
| 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 | choanoflagellates Salpingoeca rosetta cell type evolution cellular proprioception animal origins transdifferentiation |
| url | https://elifesciences.org/articles/61037 |
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