Diversity and spatial segregation of TRP channels in the closest relatives of animals

Sensory systems, built around specialized cell types, are central to how animals perceive and respond to their environments. However, the evolutionary origin of these systems remains unclear. Here, we show that choanoflagellates, the sister group of animals, possess remarkably diverse repertoires of transient receptor potential (TRP) channels, an ancient superfamily of sensory ion channels. Comparative analyses indicate that most major animal TRP channel families predate the origin of animals and reveal extensive radiations of the TRPM and TRPW families within choanoflagellates, with the latter family likely being lost in the animal lineage. Furthermore, in the choanoflagellate model Salpingoeca rosetta, TRPA, TRPC and TRPV occupy discrete microdomains within the collar complex, a key interface for environmental sensing and feeding. We propose that the evolution of animal sensory systems involved both expansion and reorganization of this ancestral repertoire, with subcellular patterning in unicellular organisms representing a precursor to cell-type specialization in multicellular animals.