Research Article

Light-regulated collective contractility in a multicellular choanoflagellate

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Science  18 Oct 2019:
Vol. 366, Issue 6463, pp. 326-334
DOI: 10.1126/science.aay2346

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Origins of collective contraction

In contrast to plants and fungi, animals can deform their bodies by the collective activity of contractile cells. Collective contractility underlies processes such as gastrulation and muscle-based motility. Brunet et al. report that a close relative of animals, a choanoflagellate they name Choanoeca flexa, forms cup-shaped colonies that undergo collective contractility, leading to a rapid change in colony morphology (see the Perspective by Tomancak). C. flexa colonies are each composed of a monolayer of polarized cells. In response to sudden darkness, a light-sensing protein triggers coordinated, polarized contraction of C. flexa cells, which results in colony inversion. The cellular mechanisms underlying this process are conserved between C. flexa and animals, indicating that their last common ancestor was also capable of polarized cell contraction.

Science, this issue p. 326; see also p. 300

Abstract

Collective cell contractions that generate global tissue deformations are a signature feature of animal movement and morphogenesis. However, the origin of collective contractility in animals remains unclear. While surveying the Caribbean island of Curaçao for choanoflagellates, the closest living relatives of animals, we isolated a previously undescribed species (here named Choanoeca flexa sp. nov.) that forms multicellular cup-shaped colonies. The colonies rapidly invert their curvature in response to changing light levels, which they detect through a rhodopsin–cyclic guanosine monophosphate pathway. Inversion requires actomyosin-mediated apical contractility and allows alternation between feeding and swimming behavior. C. flexa thus rapidly converts sensory inputs directly into multicellular contractions. These findings may inform reconstructions of hypothesized animal ancestors that existed before the evolution of specialized sensory and contractile cells.

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