Rapid repurposing of microvillar content drives a flagellate-to-amoeboid switch in the closest relative of animals
- 1Institut Pasteur
Abstract
Animal cells extensively remodel their cytoskeleton during differentiation and can notably switch between two major motility modes: flagellum-based swimming and actin-based crawling. We previously showed that choanoflagellates, the closest living relatives of animals and classically viewed as obligate flagellated swimmers, can retract their collar complex and adopt an amoeboid form within seconds under spatial confinement, independently of regulated gene expression. Here, using live imaging, ultrastructural expansion microscopy, and cryo-electron tomography in Salpingoeca rosetta, we identify rapid, cell-wide cytoskeletal remodeling as the ultrastructural basis of this switch. Unconfined choanoflagellates lack a detectable actin cortex but display an apical flagellum and cortical microtubules, with F-actin being largely restricted to microvilli. Confinement triggers calcium release from intracellular stores, which induces microvillar retraction and absorption of microvillar material into the cell body, including actin, ezrin-radixin-moesin 1, and plasma membrane. Remodeling of the internalized F-actin and repurposing of associated proteins supports de novo actin cortex formation, which is necessary for amoeboid motility. In parallel, cortical microtubules are disassembled, and the reabsorbed microvillar plasma membrane increases the surface area of the cell body, allowing the cell to flatten under confinement. Cryo-electron tomography reveals stepwise actin reorganization from internalized microvillar bundles to a cortical contractile meshwork combining bundles and scattered filaments. This work reveals considerable ultrastructural plasticity in the cytoskeletal architecture of choanoflagellates and supports an ancestral role for microvilli as reservoirs of membrane and cytoskeleton to potentiate cell phenotypic transitions.
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BibTeX
@misc{freiredelgado2026rapid,
title = {{Rapid repurposing of microvillar content drives a flagellate-to-amoeboid switch in the closest relative of animals}},
author = {M. Freire-Delgado and D. de Haan and S. Tachon and A. D. Gazi and M. Ansel and E. K. Pillai and M. Albert and C. Combredet and A. Salles and J.-Y. Tinevez and T. Brunet},
howpublished = {bioRxiv},
year = {2026},
month = aug,
doi = {10.64898/2026.08.28.747835},
url = {https://www.biorxiv.org/content/10.64898/2026.08.28.747835v1},
note = {CC BY},
}
RIS
TY - UNPB
TI - Rapid repurposing of microvillar content drives a flagellate-to-amoeboid switch in the closest relative of animals
AU - M. Freire-Delgado
AU - D. de Haan
AU - S. Tachon
AU - A. D. Gazi
AU - M. Ansel
AU - E. K. Pillai
AU - M. Albert
AU - C. Combredet
AU - A. Salles
AU - J.-Y. Tinevez
AU - T. Brunet
PY - 2026
DA - 2026/08/28
PB - bioRxiv
DO - 10.64898/2026.08.28.747835
UR - https://www.biorxiv.org/content/10.64898/2026.08.28.747835v1
AB - Animal cells extensively remodel their cytoskeleton during differentiation and can notably switch between two major motility modes: flagellum-based swimming and actin-based crawling. We previously showed that choanoflagellates, the closest living relatives of animals and classically viewed as obligate flagellated swimmers, can retract their collar complex and adopt an amoeboid form within seconds under spatial confinement, independently of regulated gene expression. Here, using live imaging, ultrastructural expansion microscopy, and cryo-electron tomography in Salpingoeca rosetta, we identify rapid, cell-wide cytoskeletal remodeling as the ultrastructural basis of this switch. Unconfined choanoflagellates lack a detectable actin cortex but display an apical flagellum and cortical microtubules, with F-actin being largely restricted to microvilli. Confinement triggers calcium release from intracellular stores, which induces microvillar retraction and absorption of microvillar material into the cell body, including actin, ezrin-radixin-moesin 1, and plasma membrane. Remodeling of the internalized F-actin and repurposing of associated proteins supports de novo actin cortex formation, which is necessary for amoeboid motility. In parallel, cortical microtubules are disassembled, and the reabsorbed microvillar plasma membrane increases the surface area of the cell body, allowing the cell to flatten under confinement. Cryo-electron tomography reveals stepwise actin reorganization from internalized microvillar bundles to a cortical contractile meshwork combining bundles and scattered filaments. This work reveals considerable ultrastructural plasticity in the cytoskeletal architecture of choanoflagellates and supports an ancestral role for microvilli as reservoirs of membrane and cytoskeleton to potentiate cell phenotypic transitions.
ER -