Early metazoan cell type diversity and the evolution of multicellular gene regulation

A hallmark of metazoan evolution is the emergence of genomic mechanisms that implement cell type-specific functions. However, the evolution of metazoan cell types and their underlying gene regulatory programs remain largely uncharacterized. Here, we use whole-organism single-cell RNA-seq to map cell type-specific transcription in Porifera (sponges), Ctenophora (comb jellies) and Placozoa species. We describe the repertoires of cell types in these non-bilaterian animals, uncovering diverse instances of previously unknown molecular signatures, such as multiple types of peptidergic cells in Placozoa. Analysis of the regulatory programs of these cell types reveal variable levels of complexity. In placozoans and poriferans, sequence motifs in the promoters are predictive of cell type-specific programs. In contrast, the generation of a higher diversity of cell types in ctenophores is associated to lower specificity of promoter sequences and to the existence of distal regulatory elements. Our findings demonstrate that metazoan cell types can be defined by networks of TFs and proximal promoters, and indicate that further genome regulatory complexity may be required for more diverse cell type repertoires.