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© Thibaut Brunet
C. flexa colonies fixed at different stages of inversion
Laboratory Junior Group (G5)

Evolutionary cell biology and evolution of morphogenesis

Department of Cell Biology & Infection

About

We study a simple but unsolved question: what did the first animals look like? What was their form and function? How did morphogenesis first emerge from the behavior of individual cells, and how was it subsequently modified at the dawn of animal evolution? While the very first multicellular ancestors of animals were likely microscopic (and too small to leave fossils), we can gain insights into these questions via the comparative study of living groups. Our lab investigates the cell biology, morphogenesis and behavior of choanoflagellates, the closest known living relatives of animals. Choanoflagellates can switch between unicellular and multicellular lifestyles, display temporal cell differentiation, and have recently become amenable to functional molecular genetics. We want to understand how the cell shape of choanoflagellates is controlled, how it dynamically responds to the environment, and how choanoflagellates sometimes develop into multicellular colonies capable of emergent collective behavior. We address these questions through an interdisciplinary and comparative approach, applying concepts and tools from diverse fields (cell biology, developmental biology, molecular biology, biophysics) to multiple species of choanoflagellates – including the model species S. rosetta and M. brevicollis, and the recently discovered C. flexa.

 

Unicellular form of S. rosetta and multicellular form of C. flexa

 

Projects

Our research follows 4 main directions:

1. Multicellular inversion and the origin of collective contractility: In 2018, we co-discovered Choanoeca flexa, a new species of choanoflagellate that forms cup-shaped hemispherical colonies capable of fast and reversible inversions of their global curvature in a matter of seconds. We are actively researching the sensory pathways that control inversion as well as the intracellular and intercellular mechanisms that realize it.

2. Evolution of cell adhesion and the origin of epithelia: We are also interested in understanding how the first epithelia evolved. What were the early molecular and biophysical principles of intercellular adhesion? What were early tissues like and how did they function? We are addressing this topic by dissecting mechanisms of intercellular adhesion in choanoflagellate colonies.

3. Evolution of cellular proprioception and of the amoeboid switch: in 2021, we reported a novel cellular phenotype in choanoflagellates: subjected to confinement, they retract their microvilli and flagellum, and switch to an amoeboid phenotype that uses blebs to escape from confined microenvironments. We want to uncover the mechanisms of this switch: how do choanoflagellates detect confinement, and how are cell shape and behavior dramatically remodeled in a matter of seconds?

4. Morphogenesis in single cells: Morphogenesis does not only exist in organisms, and single eukaryotic cells often present strikingly elaborate shapes. The most conspicuous morphological feature of choanoflagellates is the “collar complex”: a ring of microvilli that surrounds their flagellum. We want to understand how the collar complex is assembled, and to reconstitute its evolutionary history.

Publications

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Pictures & Media

The choanoflagellate Salpingoeca urceolata performing amoeboid crawling under confinement (Brunet et al 2021)

Stages in the inversion behavior of C. flexa illustrated in distinct fixed samples (green = cytoplasm, red = F-actin). (Tomancak, 2019)

C. flexa in its flagella-in conformation (green = cytoplasm, red = F-actin)

C. flexa in its flagella-out conformation (green = cytoplasm, red = F-actin)

Both conformations of C. flexa side-by-side (green = cytoplasm, red = F-actin)