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

Author:

Musser Jacob M.1ORCID,Schippers Klaske J.1ORCID,Nickel Michael123,Mizzon Giulia4ORCID,Kohn Andrea B.5ORCID,Pape Constantin6,Ronchi Paolo4ORCID,Papadopoulos Nikolaos1ORCID,Tarashansky Alexander J.7,Hammel Jörg U.28ORCID,Wolf Florian2ORCID,Liang Cong9ORCID,Hernández-Plaza Ana10ORCID,Cantalapiedra Carlos P.10ORCID,Achim Kaia1ORCID,Schieber Nicole L.6ORCID,Pan Leslie1ORCID,Ruperti Fabian111ORCID,Francis Warren R.12ORCID,Vargas Sergio12ORCID,Kling Svenja113ORCID,Renkert Maike1ORCID,Polikarpov Maxim1415ORCID,Bourenkov Gleb14ORCID,Feuda Roberto16ORCID,Gaspar Imre117ORCID,Burkhardt Pawel18ORCID,Wang Bo719ORCID,Bork Peer20ORCID,Beck Martin20ORCID,Schneider Thomas R.14ORCID,Kreshuk Anna6ORCID,Wörheide Gert31221,Huerta-Cepas Jaime1020,Schwab Yannick46ORCID,Moroz Leonid L.52223ORCID,Arendt Detlev113ORCID

Affiliation:

1. Developmental Biology Unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany.

2. Friedrich-Schiller-Universität Jena, Institut für Zoologie und Evolutionsforschung mit Phyletischem Museum, Ernst-Haeckel-Haus und Biologiedidaktik, 07743 Jena, Germany.

3. GeoBio-Center, Ludwig-Maximilians-Universität München, 80333 München, Germany.

4. Electron Microscopy Core Facility, European Molecular Biology Laboratory, 69117 Heidelberg, Germany.

5. Whitney Laboratory for Marine Bioscience, University of Florida, St. Augustine, FL 32080, USA.

6. Cell Biology and Biophysics Unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany.

7. Department of Bioengineering, Stanford University, Stanford, CA 94305, USA.

8. Institute for Materials Physics, Helmholtz-Zentrum Hereon, 21502 Geesthacht, Germany.

9. Center for Applied Mathematics, Tianjin University, Tianjin 300072, China.

10. Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid (UPM) and Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA), 28223 Madrid, Spain.

11. Collaboration for joint Ph.D. degree between EMBL and Heidelberg University, Faculty of Biosciences 69117 Heidelberg, Germany.

12. Department of Earth and Environmental Sciences, Paleontology & Geobiology, Ludwig-Maximilians-Universität München, 80333 München, Germany.

13. Centre for Organismal Studies (COS), University of Heidelberg, 69120 Heidelberg, Germany.

14. Hamburg Unit c/o DESY, European Molecular Biology Laboratory, Hamburg, 22607 Germany.

15. Department of Information Technology and Electrical Engineering, ETH Zurich, CH-8092 Zurich, Switzerland.

16. Department of Genetics and Genome Biology, University of Leicester, Leicester LE1 7RH, UK.

17. Department of Totipotency, Max Planck Institute of Biochemistry, 82152 Martinsried, Germany.

18. Sars International Centre for Marine Molecular Biology, University of Bergen, 5008 Bergen, Norway.

19. Department of Developmental Biology, Stanford University School of Medicine, Stanford, CA 94305, USA.

20. Structural and Computational Biology Unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany.

21. Bayerische Staatssammlung für Paläontologie und Geologie (SNSB), 80333 München, Germany.

22. Department of Neuroscience and Brain Institute, University of Florida, Gainesville, FL 32610, USA.

23. McKnight Brain Institute, University of Florida, Gainesville, FL 32610, USA.

Abstract

Sponges and evolutionary origins Sponges represent our distant animal relatives. They do not have a nervous system but do have a simple body for filter feeding. Surveying the cell types in the freshwater sponge Spongilla lacustris , Musser et al . found that many genes important in synaptic communication are expressed in cells of the small digestive chambers. They found secretory machinery characteristic of the presynapse in small multipolar cells contacting all other cells and also the receptive apparatus of the postsynapse in the choanocytes that generate water flow and digest microbial food. These results suggest that the first directed communication in animals may have evolved to regulate feeding, serving as a starting point on the long path toward nervous system evolution. —BAP

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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