The ancestral animal genetic toolkit revealed by diverse choanoflagellate transcriptomes

Abstract

The changes in gene content that preceded the origin of animals can be reconstructed by comparison with their sister group, the choanoflagellates. However, only two choanoflagellate genomes are currently available, providing poor coverage of their diversity. We sequenced transcriptomes of 19 additional choanoflagellate species to produce a comprehensive reconstruction of the gains and losses that shaped the ancestral animal gene repertoire. We find roughly 1,700 gene families with origins on the animal stem lineage, of which only a core set of 36 are conserved across animals. We find more than 350 gene families that were previously thought to be animal-specific actually evolved before the animal-choanoflagellate divergence, including Notch and Delta, Toll-like receptors, and glycosaminoglycan hydrolases that regulate animal extracellular matrix (ECM). In the choanoflagellate Salpingoeca helianthica, we show that a glycosaminoglycan hydrolase modulates rosette colony size, suggesting a link between ECM regulation and morphogenesis in choanoflagellates and animals.