New hypotheses of cell type diversity and novelty from comparative single cell and nuclei transcriptomics in echinoderms

Abstract

Cell types are the fundamental building blocks of metazoan biodiversity and offer a powerful perspective for inferring evolutionary phenomena. With the development of single-cell transcriptomic techniques, new definitions of cell types are emerging. This allows a conceptual reassessment of traditional definitions of novel cell types and their evolution. Research in echinoderms, particularly sea star and sea urchin embryos have contributed significantly to understanding the evolution of novel cell types, in particular the primary mesenchyme cells (PMCs) and pigment cells that are found in sea urchin but not sea star embryos. This paper outlines the development of a gene expression atlas for the bat star, Patiria miniata, using single nuclear RNA sequencing (snRNA-seq) of embryonic stages. The atlas revealed 22 cell clusters covering all expected cell types from the endoderm, mesoderm and ectoderm germ layers. In particular, four distinct neural clusters, an immune cluster, and distinct right and left coelom clusters were revealed as distinct cell states. A comparison with Strongylocentrotus purpuratus embryo single cell transcriptomes was performed using 1:1 orthologs to anchor and then compare gene expression patterns. S. purpuratus primordial germ cell equivalents were not detected in P. minata, while the left coelom of P. miniata has no equivalent cell cluster in S. purpuratus. Pigment cells of S. purpuratus map to clusters containing immune mesenchyme and neural cells of P. miniata, while the PMCs of S. purpuratus are revealed as orthologous to the right coelom cluster of P. miniata. These results suggest a new interpretation of the evolution of these well-studied cell types and a reflection on the definition of novel cell types.

A New Model Organism to Investigate Extraocular Photoreception: Opsin and Retinal Gene Expression in the Sea Urchin Paracentrotus lividus

“…The two neuronal opsin2/opsin4 positive cell type families share common neuronal and retinal-like molecular fingerprints. The neuronal fingerprint includes the transcription factor arxl , that in vertebrates is important for forebrain development [ 56 ], the synaptotagmin gene syt4l [ 28 , 30 ] and the neuropeptide NGFFFamide [ 30 , 57 , 58 ]. Moreover, the two opsin2 / opsin4 positive clusters contain transcripts for the retinal marker gene Pl-opsin4 [ 59 ], the notch signaling component Pl-notch2 [ 60 , 61 ] and the transcription factor tbx3 [ 62 ] which are involved in vision-related morphogenetic and physiological procedures in vertebrates.…”

“…Cells with similar expression profiles are grouped into clusters that correspond to distinct cell type families, cell types, or cell states using computational analysis. ScRNA-seq has been used successfully to describe and identify novel cell types in a wide range of organisms, including sponges [ 25 ], cnidarians [ 26 , 27 ], and echinoderms [ 28 , 29 , 30 ], as well as mammals [ 31 ]. In addition, scRNA-seq has been used to decipher complex evolutionary relationships between cell types.…”

Molecular mechanisms of tubulogenesis revealed in the sea star hydro-vascular organ

“…The balance of these factors is regulated by the FGF pathway. In further support of this model, tube cell precursors are enriched in genes related to the extracellular matrix and cell/cell adhesion (Meyer et al, 2022).…”

Evolution of homology: From archetype towards a holistic concept of cell type

“…The epithelial ‘phylogeny’ has been particularly demonstrated to have a more nonbinary, network‐like structure, where strongest connections across phyla do not span continuous paths in the species tree, thus precluding its explanation by vertical evolutionary descent. Genetic heterogeneity inherently marks novel cell types, as can be illustrated, for instance, with a report on sea urchin's larval pigment cells: those are traditionally considered a morphological and functional novelty of echinoid echinoderms and also form a distinct cluster in the urchin's single‐cell atlas, while they turn to comprise a ‘hybrid’ of immune mesenchyme and neuronal‐type GRNs in comparison with a sea star (Meyer et al, 2022). The salient examples of cell type novelty emerging via assembly of different labour‐executing components can be observed among the exceptional diversity of exocrine glands in insects (Brückner et al, 2021; Kishi & Parker, 2021).…”