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

Jacob M. Musser(European Molecular Biology Laboratory), Klaske J. Schippers(European Molecular Biology Laboratory), Michael Nickel(Schiller International University), Giulia Mizzon(European Molecular Biology Laboratory), Andrea B. Kohn(Whitney Museum of American Art), Constantin Pape(European Molecular Biology Laboratory), Paolo Ronchi(European Molecular Biology Laboratory), Νικόλαος Παπαδόπουλος(European Molecular Biology Laboratory), Alexander J. Tarashansky(Stanford University), Jörg U. Hammel(Schiller International University), Florian Wolf(Schiller International University), Cong Liang(Tianjin University), Ana Hernández-Plaza(Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria), Carlos P. Cantalapiedra(Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria), Kaia Achim(European Molecular Biology Laboratory), Nicole L. Schieber(European Molecular Biology Laboratory), Leslie Pan(European Molecular Biology Laboratory), Fabian Ruperti(Heidelberg University), Warren R. Francis(Ludwig-Maximilians-Universität München), Sergio Vargas(Ludwig-Maximilians-Universität München), Svenja Kling(Heidelberg University), Maike Renkert(European Molecular Biology Laboratory), Maxim Polikarpov(ETH Zurich), Gleb Bourenkov(European Molecular Biology Laboratory), Roberto Feuda(University of Leicester), Imre Gáspár(European Molecular Biology Laboratory), Pawel Burkhardt(University of Bergen), Bo Wang(Stanford University), Peer Bork(European Molecular Biology Laboratory), Martin Beck(European Molecular Biology Laboratory), T. Schneider(European Molecular Biology Laboratory), Anna Kreshuk(European Molecular Biology Laboratory), Gert Wörheide(Bayerische Staatssammlung für Paläontologie und Geologie), Jaime Huerta‐Cepas(Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria), Yannick Schwab(European Molecular Biology Laboratory), Leonid L. Moroz(Allen Institute for Brain Science), Detlev Arendt(Heidelberg University)
Science
November 4, 2021
Cited by 230Open Access
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Abstract

The evolutionary origin of metazoan cell types such as neurons and muscles is not known. Using whole-body single-cell RNA sequencing in a sponge, an animal without nervous system and musculature, we identified 18 distinct cell types. These include nitric oxide–sensitive contractile pinacocytes, amoeboid phagocytes, and secretory neuroid cells that reside in close contact with digestive choanocytes that express scaffolding and receptor proteins. Visualizing neuroid cells by correlative x-ray and electron microscopy revealed secretory vesicles and cellular projections enwrapping choanocyte microvilli and cilia. Our data show a communication system that is organized around sponge digestive chambers, using conserved modules that became incorporated into the pre- and postsynapse in the nervous systems of other animals.


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