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

Abstract

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 programmes remains largely uncharacterized. Here, we use whole-organism single-cell RNA sequencing 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 programmes of these cell types reveals variable levels of complexity. In placozoans and poriferans, sequence motifs in the promoters are predictive of cell-type-specific programmes. By contrast, the generation of a higher diversity of cell types in ctenophores is associated with lower specificity of promoter sequences and the existence of distal regulatory elements. Our findings demonstrate that metazoan cell types can be defined by networks of transcription factors and proximal promoters, and indicate that further genome regulatory complexity may be required for more diverse cell type repertoires.

Profiling cellular diversity in sponges informs animal cell type and nervous system evolution

“…S5L), as well as a whole actomyosin-contractility module(Fig. 2K), consistent with findings in the marine demosponge Amphimedon queenslandica(12), and with pinacocytes being the main contractile cell types mediating whole-body rhythmic contractions in sponges(13). We also observed expression of the transcription factors Serum response factor (Srf), a master regulator of the cellular contractile apparatus(14), and Cysteine and glycine-rich protein (Csrp1/2/3, aka Muscle LIM protein) encoding cofactors of Srf, suggesting sponges may contain a conserved regulatory module for actomyosin contractility(Fig.…”

Neuromuscular organization of the Ctenophore Pleurobrachia bachei

“…Recent advances of comparative single‐cell genomic point to insufficient knowledge about the cellular diversity in basal metazoans in general, and ctenophores in particular. In fact, recent single‐cell RNA‐seq profiling of two ctenophores (Moroz, ; Sebe‐Pedros et al, ) indicated that many cells could not be reliably recognized using conventional approaches. The absence of cell‐specific molecular markers for ctenophore neurons and muscles is a noticeable obstacle in the field.…”

A screen for gene paralogies delineating evolutionary branching order of early Metazoa

“…To date, most phylogenetic analyses have used single-copy orthologs, with different genes and approaches finding support for either Ctenophora (RYAN et al 2013;MOROZ et al 2014;BOROWIEC et al 2015;WHELAN et al 2015;SHEN et al 2017) or Porifera (PISANI et al 2015;FEUDA et al 2017;SIMION et al 2017) as the sister taxon of all other animals. In contrast to sequence-based phylogenies, comparative analysis of single-cell transcriptomes from different lineages and cell types is consistent with an independent origin of neuron-like cells in ctenophores (SEBE-PEDROS et al 2018). Another recent study that does not rely directly on sequence analysis provides evidence that the sponge choanocyte does not correspond to the sponge cell type most similar transcriptomically to the choanoflagellate cell type (SOGABE et al 2019).…”

“…Another recent study that does not rely directly on sequence analysis provides evidence that the sponge choanocyte does not correspond to the sponge cell type most similar transcriptomically to the choanoflagellate cell type (SOGABE et al 2019). Thus to date, few studies (SEBE-PEDROS et al 2018;SOGABE et al 2019) have addressed the question of early animal branching without using single-copy genes for phylogenetic analysis.…”