Electrical signaling and coordinated behavior in the closest relative of animals

Abstract

The transition from simple to complex multicellularity involves division of labor and specialization of cell types. In animals, complex sensory-motor systems are primarily built around specialized cells of muscles and neurons, though the evolutionary origins of these and their integration remain unclear. Here, to investigate sensory-behavior coupling in the closest relatives of animals, we established a line of the choanoflagellate, Salpingoeca rosetta, which stably expresses the calcium indicator RGECO1. Using this, we identify a previously unknown cellular behavior associated with electrical signaling, in which ciliary arrest is coupled with apical-basal contraction of the cell. This behavior and the associated calcium transients are synchronized in the multicellular state and result in coordinated ciliary arrest and colony-wide contraction, suggesting that information is spread among the cells. Our work reveals fundamental insights into how choanoflagellates sense and respond to their environment and enhances our understanding of the integration of cellular and organism-wide behavior in the closest protistan relatives of animals.