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Profiling cellular diversity in sponges informs animal cell type and nervous system evolution
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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
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“Consistent with a neuron-bearing metazoan ancestor, sponges possess secretory cell types15 and extensive molecular components associated with presynaptic function that could be derived from a primitive neurosecretory cell.”
From Ancient gene linkages support ctenophores as sister to other animals (2023) · cites this paper as [15]
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Self-citation
Metadata
- Authors
- Musser, J. M., Schippers, K. J., Nickel, M., Mizzon, G., Kohn, A. B., Pape, C., Ronchi, P., Papadopoulos, N., Tarashansky, A. J., Hammel, J. U., Wolf, F., Liang, C., Hernández-Plaza, A., Cantalapiedra, C. P., Achim, K., Schieber, N. L., Pan, L., Ruperti, F., Francis, W. R., Vargas, S., Kling, S., Renkert, M., Polikarpov, M., Bourenkov, G., Feuda, R., Gaspar, I., Burkhardt, P., Wang, B., Bork, P., Beck, M., Schneider, T. R., Kreshuk, A., Wörheide, G., Huerta-Cepas, J., Schwab, Y., Moroz, L. L., & Arendt, D.
- Affiliations
- European Molecular Biology Laboratory (DE)
- University of Florida (US)
- Developmental Biology Unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany.
- Stanford University (US)
- Helmholtz-Zentrum Hereon (DE)
- Friedrich Schiller University Jena (DE)
- Tianjin University (CN)
- Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (ES)
- Heidelberg University (DE)
- Ludwig-Maximilians-Universität München (DE)
- Deutsches Elektronen-Synchrotron DESY (DE)
- University of Leicester (GB)
- University of Bergen (NO)
- Stanford Medicine (US)
- Structural and Computational Biology Unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany.
- Bayerische Staatssammlung für Paläontologie und Geologie (DE)
- 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.
- Corresponding author
- Musser, Jacob M.
- Moroz, Leonid L.
- Arendt, Detlev
- ORCID
- Musser, Jacob M.
- Schippers, Klaske J.
- Nickel, Michael
- Mizzon, Giulia
- Kohn, Andrea B.
- Pape, Constantin
- Ronchi, Paolo
- Papadopoulos, Nikolaos
- Tarashansky, Alexander J.
- Hammel, Jörg U.
- Wolf, Florian
- Liang, Cong
- Hernández-Plaza, Ana
- Cantalapiedra, Carlos P.
- Achim, Kaia
- Schieber, Nicole L.
- Pan, Leslie
- Ruperti, Fabian
- Francis, Warren R.
- Vargas, Sergio
- Kling, Svenja
- Renkert, Maike
- Polikarpov, Maxim
- Bourenkov, Gleb
- Feuda, Roberto
- Gaspar, Imre
- Burkhardt, Pawel
- Wang, Bo
- Bork, Peer
- Beck, Martin
- Schneider, Thomas R.
- Kreshuk, Anna
- Wörheide, Gert
- Schwab, Yannick
- Moroz, Leonid L.
- Arendt, Detlev
- Venue
- Science
- Published
- 2021-11-05
- Volume
- 374
- Issue
- 6568
- Pages
- 717-723
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC9233960
- OpenAlex
- W3210441301
- Semantic Scholar
- 648b94efda391a39ec07edbf8f34c52de3af5442
- Cited by
- 242
- References
- 128
- Citations by year
- 2026: 25 · 2025: 42 · 2024: 43 · 2023: 49 · 2022: 43 · 2021: 27
- FWCI
- 30.39
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Locations
- Science (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion, cc-by-nc-nd)
- Desy publication database (The Deutsches Elektronen-Synchrotron) (submittedVersion)
- Archivio istituzionale della ricerca (Alma Mater Studiorum Università di Bologna) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- Funders
- National Science Foundation (1557923, 1146575, 2017-2021, 1548121, 1645219)
- Villum Fonden (00016518)
- Ministerio de Ciencia, Innovación y Universidades (10.13039.501100011033, SEV-2016-0672, 13039, PGC 2018, PGC2018-098073-A-I00 MCIU/AEI/FEDER, 10.13039, .13039/501100011033, PGC2018-098073-A-I00, 501100011033)
- European Commission (10.13039/501100011033, 13039/501100011033, 501100011033, HORIZON2020, 788921, 764840)
- Ludwig-Maximilians-Universität München
- National Institutes of Health
- Agencia Estatal de Investigación (AEI//10.13039/501100011033/, SEV-2016–0672, 501100011033, 10.13039/501100011033, 13039, .13039/501100011033, 10.13039, PGC2018-098073-A-I00, PGC2018)
- National Institute of Neurological Disorders and Stroke (R01NS114491)
- FP7 Ideas: European Research Council (294810)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Marine Sponges and Natural Products
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- sponges, cell type diversity, nervous system evolution, choanocytes, phagocytes, secretory vesicles, single-cell transcriptomics
- MeSH terms
- RNA-Seq, Animals, Cell Communication, Cilia, Digestive System, Biological Evolution, Mesoderm, Nervous System, Nervous System Physiological Phenomena, Nitric Oxide, Porifera, Signal Transduction, Cell Surface Extensions, Secretory Vesicles, Single-Cell Analysis, Transcriptome
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