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

Jacob M. Musser; Klaske J. Schippers; Michael Nickel; Giulia Mizzon; Andrea B. Kohn; Constantin Pape; Paolo Ronchi; Νικόλαος Παπαδόπουλος; Alexander J. Tarashansky; Jörg U. Hammel; Florian Wolf; Cong Liang; Ana Hernández-Plaza; Carlos P. Cantalapiedra; Kaia Achim; Nicole L. Schieber; Leslie Pan; Fabian Ruperti; Warren Russell Francis; Sergio Vargas; Svenja Kling; Maike Renkert; Maxim Polikarpov; Gleb P. Bourenkov; Roberto Feuda; Imre Gáspár; Pawel Burkhardt; Bo Wang; Peer Bork B; Martin Beck

doi:10.1126/science.abj2949

Developmental BiologyScienceNov 4, 2021

Peer-reviewed journal article

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

Jacob M. Musser iD, Klaske J. Schippers iD, Michael Nickel iD, Giulia Mizzon iD, Andrea B. Kohn iD, Constantin Pape iD, Paolo Ronchi iD, Νικόλαος Παπαδόπουλος iD, Alexander J. Tarashansky iD, Jörg U. Hammel iD, Florian Wolf iD, Cong Liang iD, Ana Hernández-Plaza iD, Carlos P. Cantalapiedra iD, Kaia Achim iD, Nicole L. Schieber iD, Leslie Pan iD, Fabian Ruperti iD, Warren Russell Francis iD, Sergio Vargas iD, Svenja Kling iD, Maike Renkert iD, Maxim Polikarpov iD, Gleb P. Bourenkov iD, Roberto Feuda iD, , Detlev Arendt iD

Abstract

The evolutionary origin of metazoan cell types such as neurons, muscles, digestive, and immune cells, remains unsolved. Using whole-body single-cell RNA sequencing in a sponge, an animal without nervous system and musculature, we identify 18 distinct cell types comprising four major families. This includes nitric-oxide sensitive contractile cells, digestive cells active in macropinocytosis, and a family of amoeboid-neuroid cells involved in innate immunity. We uncover presynaptic genes in an amoeboid-neuroid cell type, and postsynaptic genes in digestive choanocytes, suggesting asymmetric and targeted communication. Corroborating this, long neurite-like extensions from neuroid cells directly contact and enwrap choanocyte microvillar collars. Our data indicate a link between neuroid and immune functions in sponges, and suggest that a primordial neuro-immune system cleared intruders and controlled ciliary beating for feeding.

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