Single Nucleus Profiling Highlights the All-Brain Echinoderm Nervous System

Abstract

Metazoans comprise diverse tissues and cell types, each essential for the survival of the organism. Most of these cell types are established early in embryogenesis and persist into adulthood. However, in indirectly developing sea urchins, the continuity between embryonic and adult stages is thus interrupted by a planktonic larval stage that undergoes complete metamorphosis. In addition, while the gene regulatory networks governing distinct embryonic and larval cell lineages are well studied, the molecular and morphological identities of post-metamorphic sea urchin cell types remain poorly understood. Here, we reconstructed the cell type atlas of post-metamorphic Paracentrotus lividus juveniles using single-nucleus transcriptomics, shedding light on the conservation of genetic regulatory mechanisms in post-metamorphic cell types. We identified cell signatures corresponding to eight distinct cell type groups and analyzed at least twenty-nine neuronal cell families, including fifteen unique photoreceptor cell signatures. By combining single cell transcriptomics with spatial gene expression analysis and high-resolution electron microscopy, we identified homologues of vertebrate neuronal genes and photoreceptive opsins expressed throughout the sea urchin body. These findings provide evidence that the echinoderm body plan is not only predominantly head-like, but also exhibits an all-brain organization in an animal previously considered to have a primitive nervous system.