Single cell RNA sequencing of the Strongylocentrotus purpuratus larva reveals the blueprint of major cell types and nervous system of a non-chordate deuterostome

  1. Periklis Paganos
  2. Danila Voronov
  3. Jacob M Musser
  4. Detlev Arendt
  5. Maria Ina Arnone  Is a corresponding author
  1. Stazione Zoologica Anton Dohrn (SZN), Italy
  2. European Molecular Biology Laboratory, Germany
  3. Stazione Zoologica Anton Dohrn, Italy

Abstract

Identifying the molecular fingerprint of organismal cell types is key for understanding their function and evolution. Here, we use single cell RNA sequencing (scRNA-seq) to survey the cell types of the sea urchin early pluteus larva, representing an important developmental transition from non-feeding to feeding larva. We identify 21 distinct cell clusters, representing cells of the digestive, skeletal, immune, and nervous systems. Further subclustering of these reveal a highly detailed portrait of cell diversity across the larva, including the identification of neuronal cell types. We then validate important gene regulatory networks driving sea urchin development and reveal new domains of activity within the larval body. Focusing on neurons that co-express Pdx-1 and Brn1/2/4, we identify an unprecedented number of genes shared by this population of neurons in sea urchin and vertebrate endocrine pancreatic cells. Using differential expression results from Pdx-1 knockdown experiments, we show that Pdx1 is necessary for the acquisition of the neuronal identity of these cells. We hypothesize that a network similar to the one orchestrated by Pdx1 in the sea urchin neurons was active in an ancestral cell type and then inherited by neuronal and pancreatic developmental lineages in sea urchins and vertebrates.

Data availability

Sequencing data (mapped reads) have been deposited in Dyrad under the unique identifier doi:10.5061/dryad.n5tb2rbvz

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Periklis Paganos

    Department of Biology and Evolution of Marine Organisms, Stazione Zoologica Anton Dohrn (SZN), Naples, Italy
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9525-4625
  2. Danila Voronov

    Department of Biology and Evolution of Marine Organisms, Stazione Zoologica Anton Dohrn (SZN), Naples, Italy
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2972-6484
  3. Jacob M Musser

    Developmental Biology Unit, European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Detlev Arendt

    Developmental Biology Unit, European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7833-050X
  5. Maria Ina Arnone

    Department of Biology and Evolution of Marine Organisms, Stazione Zoologica Anton Dohrn, Naples, Italy
    For correspondence
    miarnone@szn.it
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9012-7624

Funding

H2020 Marie Skłodowska-Curie Actions (766053)

  • Periklis Paganos
  • Detlev Arendt
  • Maria Ina Arnone

H2020 European Research Council (788921)

  • Jacob M Musser
  • Detlev Arendt

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Kristin Tessmar-Raible, University of Vienna, Austria

Version history

  1. Preprint posted: March 16, 2021 (view preprint)
  2. Received: May 17, 2021
  3. Accepted: November 24, 2021
  4. Accepted Manuscript published: November 25, 2021 (version 1)
  5. Version of Record published: December 17, 2021 (version 2)

Copyright

© 2021, Paganos 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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  1. Periklis Paganos
  2. Danila Voronov
  3. Jacob M Musser
  4. Detlev Arendt
  5. Maria Ina Arnone
(2021)
Single cell RNA sequencing of the Strongylocentrotus purpuratus larva reveals the blueprint of major cell types and nervous system of a non-chordate deuterostome
eLife 10:e70416.
https://doi.org/10.7554/eLife.70416

Share this article

https://doi.org/10.7554/eLife.70416

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