New hypotheses of cell type diversity and novelty from orthology-driven comparative single cell and nuclei transcriptomics in echinoderms
- Carnegie Mellon University, United States
Abstract
Cell types are the 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 has contributed significantly to understanding the evolution of novel cell types, through the examination of skeletogenic mesenchyme and pigment cells, which are found in sea urchin larvae, but not sea star larvae. This paper outlines the development of a gene expression atlas for the bat sea star, Patiria miniata, using single nuclear RNA sequencing (snRNA-seq) of embryonic stages. The atlas revealed 23 cell clusters covering all expected cell types from the endoderm, mesoderm, and ectoderm germ layers. In particular, four distinct neural clusters, an immune-like 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. The equivalent of S. purpuratus piwil3+ Cells were not detected in P. miniata, while the Left Coelom of P. miniata has no equivalent cell cluster in S. purpuratus. These differences may reflect changes in developmental timing between these species. While considered novel morphologically, the Pigment Cells of S. purpuratus map to clusters containing Immune-like Mesenchyme and Neural cells of P. miniata, while the Skeletogenic Mesenchyme 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.
Data availability
Sequencing data have been supplied as NCBI SRA indicated below. Other data is provided directly in the manuscript and supporting files
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Spurpuratus SC sequencingNCBI BioProject, PRJNA839000.
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Pminiata SC SequencingNCBI BioProject, PRJNA826814.
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A single cell RNA-seq resource for early sea urchin developmentNCBI Gene Expression Omnibus, GSE149221.
Article and author information
Author details
William L Hatleberg
Funding
National Science Foundation (IOS 1557431)
- Veronica Hinman
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Maria Ina Arnone, Stazione Zoologica Anton Dohrn, Italy
Version history
- Preprint posted: May 7, 2022 (view preprint)
- Received: May 7, 2022
- Accepted: June 15, 2023
- Accepted Manuscript published: July 20, 2023 (version 1)
- Version of Record published: August 2, 2023 (version 2)
Copyright
© 2023, Meyer et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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New hypotheses of cell type diversity and novelty from orthology-driven comparative single cell and nuclei transcriptomics in echinoderms
eLife 12:e80090.
https://doi.org/10.7554/eLife.80090
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