Electrical signaling and coordinated behavior in the closest relative of animals

Abstract

The transition between simple to complex multicellularity involves large degrees of division of labor and specialization of cell types. In animals, complex sensory motor systems are primarily built around the fundamental cell types of muscles and neurons, though the evolutionary origin of these cells, and their integration, remains unclear. Here, in order 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 novel 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 information is spread amongst the cells. Our work reveals fundamental insights into how choanoflagellates sense and respond to their environment and offer a new perspective into the integration of cellular and organism wide behavior in the closest protistan relatives of animals.