Molecular profiling of sponge deflation reveals an ancient relaxant-inflammatory response
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Abstract
A hallmark of animals is the coordination of whole-body movement. Neurons and muscles are central to this, yet coordinated movements also exist in sponges that lack these cell types. Sponges are sessile animals with a complex canal system for filter-feeding. They undergo whole-body movements resembling "contractions" that lead to canal closure and water expulsion. Here, we combine live 3D optical coherence microscopy, pharmacology, and functional proteomics to elucidate the sequence and detail of shape changes, the tissues and molecular physiology involved, and the control of these movements. Morphometric analysis and targeted perturbation suggest that the movement is driven by the relaxation of actomyosin stress fibers in epithelial canal cells, which leads to whole-body deflation via collapse of the incurrent and expansion of the excurrent canal system. Thermal proteome profiling and quantitative phosphoproteomics confirm the control of cellular relaxation by an Akt/NO/PKG/PKA pathway. Agitation-induced deflation leads to differential phosphorylation of proteins forming epithelial cell junctions, implying their mechanosensitive role. Unexpectedly, untargeted metabolomics detect a concomitant decrease in antioxidant molecules during deflation, reflecting an increase in reactive oxygen species. Together with the secretion of proteinases, cytokines, and granulin, this indicates an inflammation-like state of the deflating sponge reminiscent of vascular endothelial cells experiencing oscillatory shear stress. These results suggest the conservation of an ancient relaxant-inflammatory response of perturbed fluid-carrying systems in animals and offer a possible mechanism for whole-body coordination through diffusible paracrine signals and mechanotransduction.
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Lin, J.-S., Lee, S.-K., Chen, Y., Lin, W., & Kao, C. (2011) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf201879e · Cited by 9 · see citing works
Ibrahim, M., Sepah, Y. J., Bittencourt, M. G., Liu, H., Hanout, M., Ferraz, D., Diana, V., & Nguyen, Q. D. (2014) · CRC Press eBooks · doi:10.1201/b17026-18 · Cited by 8 · see citing works
Chiu, W.-C., Chiang, J., & Chiang, F. (2021) · Journal of the Formosan Medical Association · doi:10.1016/j.jfma.2021.03.031 · Cited by 8 · see citing works
Nudibranch predation boosts sponge silicon cycling
López‐Acosta, M., Potel, C., Gallinari, M., Pérez, F. F., & Leynaert, A. (2023) · Scientific Reports · doi:10.1038/s41598-023-27411-y · Cited by 7 · see citing works
Self-citationAnalysis of Progranulin-Mediated Akt and MAPK Activation
Xu, S., Buraschi, S., Tanimoto, R., Stefanello, M., Belfiore, A., Iozzo, R. V., & Morrione, A. (2018) · Methods in molecular biology · doi:10.1007/978-1-4939-8559-3_9 · Cited by 7 · see citing works
Flagged first, then by citations
2 of the 206 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Cell contractility in early animal evolution
Brunet, T. (2023) · Current Biology · doi:10.1016/j.cub.2023.07.054 · Cited by 20 · see citing works
Leys, S. P., Grombacher, L., Field, D., Elliott, G. R. D., Ho, V., KAHN, A. S., Reid, P. J., Riesgo, A., Lanna, E., Bobkov, Y. V., et al. (2025) · EvoDevo · doi:10.1186/s13227-025-00237-7 · Cited by 12 · see citing works
Paix, B., van der Valk, E., & de Voogd, N. J. (2024) · Environmental Microbiome · doi:10.1186/s40793-024-00580-7 · Cited by 10 · see citing works
Eating and Cognition in Two Animals without Neurons: Sponges and Trichoplax
Bechtel, W., & Bich, L. (2024) · Biological Theory · doi:10.1007/s13752-024-00464-6 · Cited by 8 · see citing works
Chemical cognition: chemoconnectomics and convergent evolution of integrative systems in animals
Moroz, L. L., & Romanova, D. Y. (2023) · Animal Cognition · doi:10.1007/s10071-023-01833-7 · Cited by 6 · see citing works
Particle loads, contractile responses and cleaning in the demosponge Halichondria panicea
Goldstein, J., Riisgård, H. U., Kealy, R. A., & Funch, P. (2024) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/j.jembe.2024.152021 · Cited by 5 · see citing works
ATP and glutamate coordinate contractions in the freshwater sponge Ephydatia muelleri
Ho, V., Goss, G. G., & Leys, S. P. (2025) · Journal of Experimental Biology · doi:10.1242/jeb.248010 · Cited by 5 · see citing works
Asexual Reproduction in Sponges: A Review
Ereskovsky, A. V., & Lavrov, A. (2026) · Molecular Reproduction and Development · doi:10.1002/mrd.70083 · Cited by 4 · see citing works
Novel imaging and biophysical approaches to study tissue hydraulics in mammalian folliculogenesis
Turley, J., Leong, K. W., & Chan, C. J. (2024) · Biophysical Reviews · doi:10.1007/s12551-024-01231-4 · Cited by 4 · see citing works
Skorentseva, K. V., Bolshakov, F. V., Saidova, A. A., & Lavrov, A. (2025) · Cell and Tissue Research · doi:10.1007/s00441-025-03960-8 · Cited by 3 · see citing works
Hehmeyer, J., Plessier, F., & Marlow, H. Q. (2024) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-111822-124041 · Cited by 3 · see citing works
How gemmules become sponges: known facts and open questions
Sokolova, A. M., & Ereskovsky, A. V. (2025) · Invertzool · doi:10.15298/invertzool.22.3.01 · Cited by 2 · see citing works
An ancient monoaminergic signaling system coordinates contractility in a nerveless spongePreprint
Zang, R. X., Malaiwong, N., Wang, L., Maziarz, J. D., Jia, K., Drotleff, B., Stein, F., Noor, M., Roberts, C. J., Rettel, M., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.02.14.704838 · Cited by 2 · see citing works
Self-citationKumala, L., & Riisgård, H. U. (2024) · Oceans · doi:10.3390/oceans5040055 · Cited by 1 · see citing works
Manzamine-A: Unraveling the Chemical and Biological Tapestry of a Marine-Derived Drug Lead
Wang, X., Wang, H., Kang, Y., Tang, X., & Ma, L. (2026) · Marine Drugs · doi:10.3390/md24060190 · Cited by 1 · see citing works
Animal granulins: In the GRN scheme of things
Bowhay, C., & Hanington, P. C. (2023) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2023.105115 · Cited by 1 · see citing works
Harrison, D., Diluvio, M., Matveev, E., Corrêa, P., Leo, F. D., & Leys, S. P. (2024) · Marine Ecology Progress Series · doi:10.3354/meps14694
Characterization of an NO-Activated Homodimeric Soluble Guanylate Cyclase from a Choanoflagellate
Wu, Y., Thomas, W. C., Green, Z. B., & Marletta, M. A. (2025) · Biochemistry · doi:10.1021/acs.biochem.5c00228
Goldstein, J., Flensburg, S. B., Garm, A. L., & Funch, P. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.09.23.677974
Alternative integrative systems in nerveless animals: Chemoconnectomics before synapses
Moroz, L. L. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-27380-3.00076-2
A mobile optical coherence microscope for studying aquatic organisms in- and outside the laboratoryPreprint
Wang, L., Davis, S., Quilitz, T., Beavis, T., Bonadonna, M., Lamprousi, M., Montanari, R., Ruperti, F., Stokkermans, A., Wiegand, T., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.07.27.740915
Self-citationKumala, L., Thomsen, M., & Canfield, D. E. (2026) · Frontiers in Physiology · doi:10.3389/fphys.2026.1849630
Learning from tandem mass spectra at scale with a self-supervised foundation model for proteomicsPreprint
Nieuwoudt, M., Reverenna, M., Patel, D., Catzel, R., Houngue, I. H. J., Daniel, J., Eloff, K., Santos, A., Carranza, N. L., Jenkins, T. P., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.09.03.747733
- Authors
- Ruperti, F., Becher, I., Stokkermans, A., Wang, L., Marschlich, N., Potel, C., Maus, E., Stein, F., Drotleff, B., Schippers, K. J., Nickel, M., Prevedel, R., Musser, J. M., Savitski, M. M., & Arendt, D.
- Affiliations
- Heidelberg University (DE)
- European Molecular Biology Laboratory (DE)
- Hubrecht Institute for Developmental Biology and Stem Cell Research (NL)
- Yale University (US)
- Corresponding author
- Wang, Ling
- Musser, Jacob M.
- Savitski, Mikhail M.
- Arendt, Detlev
- ORCID
- Venue
- Current Biology
- Publisher
- Elsevier BV
- Published
- 2024-01
- Volume
- 34
- Issue
- 2
- Pages
- 361-375.e9
- ISSN
- 0960-9822 (ISSN-L)
- PMC
- PMC10418225
- OpenAlex
- W4390579554
- Cited by
- 23
- References
- 206
- Citations by year
- 2026: 6 · 2025: 7 · 2024: 7 · 2023: 3
- FWCI
- 6.29
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Current Biology (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Lirias (submittedVersion)
- PubMed Central (submittedVersion, cc-by-nc)
- Funders
- ERC (864027 / Brillouin4Life, 788921)
- The Paul G Allen Frontiers Group
- Horizon Europe (101094250 /IMAGINE)
- Horizon 2020
- H2020 Marie Skłodowska-Curie Actions (664726, HORIZON-INFRA-2022-TECH-01, 764840)
- Horizon 2020 Framework Programme
- European Molecular Biology Laboratory
- European Research Council
- Topics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › 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 › Cell Biology › Cellular Mechanics and Interactions
- Keywords
- mechanotransduction, epithelial cell junctions, reactive oxygen species, antioxidant depletion, proteinase secretion, cytokines, granulin, paracrine signaling, whole-body coordination, mechanosensitive signaling, thermal proteome profiling, phosphoproteomics, metabolomics, sponges
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
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