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

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.

Fast transcriptional activation of developmental signalling pathways during wound healing of the calcareous sponge Sycon ciliatum

“…We hypothesise that the ability of sponge cells to quickly and effectively transdifferentiate is a trait inherited from pre-metazoan ancestors, which were capable of temporal cell differentiation [47,48,49]. This feature remains evident in extant animal relatives, including choanoflagellates [52]. However, while a comprehensive understanding of the cellular processes in sponge wound healing has been developed, the underlying genetic basis of this process remains largely unexplored.…”

The History of <em>Salpingoeca rosetta</em> as a Model for Reconstructing Animal Origins

“…The expression of fluorescent markers brought the cellular architecture of S. rosetta into living color in a way not possible previously (Figure 3D). The ability to express and perform live imaging of fluorescently tagged proteins also helped to validate the mapping of the jumble and couscous glycosyltransferases (Wetzel et al, 2018), revealed that septins localize to the basal pole of S. rosetta cells (Booth et al, 2018), and revealed the cytoskeletal dynamics that accompany the transition from flagellated swimming cells to crawling amoeboid cells upon confinement (Brunet et al, 2021). In addition, this protocol served as the foundation for transfection of the choanoflagellate Monosiga brevicollis (Woznica et al, 2021).…”

“…Engineering larger insertions, which will likely integrate into the genome with even lower frequencies, will require modifications to improve gene delivery, to increase integration frequencies, and/or to select for stable transgenes. A puromycin resistance gene has already been used for the selection of transgenic cassettes (Wetzel et al, 2018;Brunet et al, 2021;Woznica et al, 2021), but puromycin also affects the feeder bacteria that support choanoflagellate growth, leading to variable selection conditions. The development of more selectable markers that confer resistance to drugs that selectively target eukaryotes would help advance genetics in choanoflagellates and other heterotrophic organisms that require bacterial feeding.…”

STING mediates immune responses in the closest living relatives of animals

“…Choanoflagellates have already served as powerful models for studying the origin of animal multicellularity and cell differentiation ( Levin et al, 2014 ; Alegado et al, 2012 ; Brunet et al, 2021 ; Dayel et al, 2011 ; Woznica et al, 2017 ; Brunet et al, 2019 ; Laundon et al, 2019 ) and are ideally positioned to yield insights into the evolution of animal immune pathways. Therefore, we sought to establish the choanoflagellate Monosiga brevicollis as a model for studying pathogen recognition and immune responses.…”