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

Abstract

The evolution of different cell types was a key process of early animal evolution1–3. Two fundamental cell types, epithelial cells and amoeboid cells, are broadly distributed across the animal tree of life4,5 but their origin and early evolution are unclear. Epithelial cells are polarized, have a fixed shape and often bear an apical cilium and microvilli. These features are shared with choanoflagellates – the closest living relatives of animals – and are thought to have been inherited from their last common ancestor with animals1,6,7. The deformable amoeboid cells of animals, on the other hand, seem strikingly different from choanoflagellates and instead evoke more distantly related eukaryotes, such as diverse amoebae – but it has been unclear whether that similarity reflects common ancestry or convergence8. Here, we show that choanoflagellates subjected to spatial confinement differentiate into an amoeboid phenotype by retracting their flagella and microvilli, generating blebs, and activating myosin-based motility. Choanoflagellate cell crawling is polarized by geometrical features of the substrate and allows escape from confined microenvironments. The confinement-induced amoeboid switch is conserved across diverse choanoflagellate species and greatly expands the known phenotypic repertoire of choanoflagellates. The broad phylogenetic distribution of the amoeboid cell phenotype across animals9–14 and choanoflagellates, as well as the conserved role of myosin, suggests that myosin-mediated amoeboid motility was present in the life history of their last common ancestor. Thus, the duality between animal epithelial and crawling cells might have evolved from a temporal phenotypic switch between flagellate and amoeboid forms in their single-celled ancestors3,15,16.

The Single-Celled Ancestors of Animals: A History of Hypotheses

“…Finally, choanoflagellates themselves turned out to be able to reversibly switch to an amoeboid phenotype in response to spatial confinement (Brunet et al 2020), thus reviving Saville-Kent's concept of amoeboid phenotypes in choanoflagellates. Overall, these data converged to suggest that our ancestors along the holozoan stem-line -including the choanozoan ancestor -almost certainly had the ability to generate more cell phenotypes than just a collared flagellate, potentially paving the way to animal cell differentiation; and modern variants of the Choanoblastaea hypothesis have started to incorporate that idea (Arendt et al 2015).…”

“…protists have been largely confirmed. Even though choanoflagellates have recently been shown to switch to an amoeboid form under confinement(Brunet et al 2020), it is unlikely that Saville-Kent would have accidentally confined his samples: indeed, in the same book in which he described P. haeckelii(Kent 1882), he reported the retraction of the choanoflagellate collar complex under confinement and its regeneration after confinement release.If an honest mistake is ruled out, then P. haeckelii might have been real -and close to Saville-Kent's description. However, efforts to re-isolate P. haeckelii from the source location in Kew Gardens by one of us (T.B., together with Barry Leadbeater) have failed so far 5 .…”

Origins of eukaryotic excitability

“…The earliest eukaryote may have been an amoeboflagellate alternating between cilia-driven and amoeboid locomotion. The amoeboid-to-flagellate transition is common among eukaryotes, occurring in Rhizaria [ 213 ], Amoebozoa, Naegleria [ 214 ], several opisthokonts including choanoflagellates [ 215 ], filastereans [ 216 ] and early-branching fungi [ 217 , 218 ].…”

Exon Shuffling Played a Decisive Role in the Evolution of the Genetic Toolkit for the Multicellular Body Plan of Metazoa

“…Interestingly, in response to environmental changes, the choanoflagellate Salpingoeca rosetta differentiates into several distinct cell types. There are solitary cell types (thecate cells, slow swimmers, fast swimmers, amoeboid forms) and two colonial forms, rosettes and chains [ 18 , 19 ]. Thecate cells are sedentary, they attach to a substrate through a secreted goblet-shaped theca.…”

“…Thecate cells are sedentary, they attach to a substrate through a secreted goblet-shaped theca. Choanoflagellates subjected to confinement differentiate from a flagellated form to an amoeboid form by retracting their flagella and activating myosin-based motility [ 19 ].…”