Actin is a fundamental member of an ancient superfamily of structural intracellular proteins and plays a crucial role in cytoskeleton dynamics, ciliogenesis, phagocytosis, and force generation in both prokaryotes and eukaryotes. It is shown that actin has another function in metazoans: patterning biosilica deposition, a role that has spanned over 500 million years. Species of glass sponges (Hexactinellida) and demosponges (Demospongiae), representatives of the first metazoans, with a broad diversity of skeletal structures with hierarchical architecture unchanged since the late Precambrian, are studied. By etching their skeletons, organic templates dominated by individual F-actin filaments, including branched fibers and the longest, thickest actin fiber bundles ever reported, are isolated. It is proposed that these actin-rich filaments are not the primary site of biosilicification, but this highly sophisticated and multi-scale form of biomineralization in metazoans is ptterned.

Biological Faculty St Petersburg State University St Petersburg 199034 Russian Federation

Center for Advanced Technology Adam Mickiewicz University Poznan 61614 Poland

Clinical Sensoring and Monitoring Department of Anesthesiology and Intensive Care Medicine TU Dresden Dresden 01307 Germany

Department of Biochemistry and Medical Chemistry Pomeranian Medical University in Szczecin Szczecin 70111 Poland

Department of Biology Friday Harbor Labs University of Washington Friday Harbor WA 98195 USA

Department of Functional Diagnostics and Physical Medicine Faculty of Health Sciences Pomeranian Medical University in Szczecin Szczecin 71210 Poland

Department of Invertebrate Zoology Biological Faculty Lomonosov Moscow State University Moscow 119991 Russian Federation

Faculty of Chemical Technology Institute of Chemical Technology and Engineering Poznan University of Technology Poznan 60965 Poland

Institut Méditerranéen de Biodiversité et d'Ecologie CNRS IRD Aix Marseille Université Marseille 13003 France

Institute of Bioorganic Chemistry Polish Academy of Sciences Poznan 61704 Poland

Institute of Bioorganic Chemistry Russian Academy of Sciences Moscow 142290 Russian Federation

Institute of Electronic and Sensor Materials TU Bergakademie Freiberg Freiberg 09599 Germany

Institute of Physiology The Czech Academy of Sciences Prague 142 20 Czech Republic

Koltzov Institute of Developmental Biology of Russian Academy of Sciences Moscow 119334 Russian Federation

Laboratory of Experimental Oncology University Medical Center Hamburg Eppendorf Hamburg 20251 Germany

Laboratory of Pharmacology A 5 Zhirmunsky National Scientific Center of Marine Biology Far Eastern Branch Russian Academy of Sciences Vladivostok 690041 Russian Federation

Max Planck Institute for Chemical Physics of Solids Dresden 01187 Germany

Shirshov Institute of Oceanology of Russian Academy of Sciences Moscow 117218 Russian Federation

Zobrazit více v PubMed

Pisani D., Pett W., Dohrmann M., Feuda R., Rota‐Stabelli O., Philippe H., Lartillot N., Wörheide G., Proc. Natl. Acad. Sci. USA 2015, 112, 15402. PubMed PMC

Telford M. J., Moroz L. L., Halanych K. M., Nature 2016, 529, 286. PubMed

Simion P., Philippe H., Baurain D., Jager M., Richter D. J., Di Franco A., Roure B., Satoh N., Quéinnec É., Ereskovsky A., Lapébie P., Corre E., Delsuc F., King N., Wörheide G., Manuel M., Curr. Biol. 2017, 27, 958. PubMed

Dohrmann M., Wörheide G., Sci. Rep. 2017, 7, 3599. PubMed PMC

Systema Porifera: A Guide to the Classification of Sponges (Eds: Hooper J. N. A., van Soest R. W. M.), Kluwer Academic/Plenum Publishers, Dordrecht: 2002.

van Soest R. W. M., Boury‐Esnault N., Vacelet J., Dohrmann M., Erpenbeck D., De Voogd N. J., Santodomingo N., Vanhoorne B., Kelly M., Hooper J. N. A., PLoS One 2012, 7, e35105. PubMed PMC

Wysokowski M., Jesionowski T., Ehrlich H., Am. Mineral. 2018, 103, 665.

Sola‐Rabada A., Michaelis M., Oliver D. J., Roe M., Colombi Ciacchi L., Heinz H., Perry C. C., Langmuir 2018, 34, 8255. PubMed

Pisera A., Łukowiak M., Masse S., Tabachnick K., Fromont J., Ehrlich H., Bertolino M., Front. Zool. 2021, 18, 58. PubMed PMC

Povarova N. V., Barinov N. A., Baranov M. S., Markina N. M., Varizhuk A. M., Pozmogova G. E., Klinov D. V., Kozhemyako V. B., Lukyanov K. A., Sci. Rep. 2018, 8, 16759. PubMed PMC

Cha J. N., Shimizu K., Zhou Y., Christiansen S. C., Chmelka B. F., Stucky G. D., Morse D. E., Proc. Natl. Acad. Sci. USA 1999, 96, 361. PubMed PMC

Shimizu K., Cha J., Stucky G. D., Morse D. E., Proc. Natl. Acad. Sci. USA 1998, 95, 6234. PubMed PMC

Shimizu K., Amano T., Bari R., Weaver J. C., Arima J., Mori N., Proc. Natl. Acad. Sci. USA 2015, 112, 11449. PubMed PMC

Ehrlich H., Deutzmann R., Brunner E., Cappellini E., Koon H., Solazzo C., Yang Y., Ashford D., Thomas‐Oates J., Lubeck M., Baessmann C., Nat. Chem. 2010, 2, 1084. PubMed

Ehrlich H., Krautter M., Hanke T., Simon P., Knieb C., Heinemann S., Worch H., J. Exp. Zool. 2007, 308B, 473. PubMed

Ehrlich H., Maldonado M., Parker A. R., Kulchin Y. N., Schilling J., Koehler B., Skrzypczak U., Simon P., Reiswig H. M., Tsurkan M. V., Brunner E., Adv. Opt. Mater. 2016, 4, 1608.

Thesaurus of Sponge Morphology in Smithsonian Contributions to Zoology (Eds: Boury‐Esnault N., Rützler K.), Smithsonian Institution Press, Washington DC: 1997.

Uriz M. J., Turon X., Becerro M. A., Agell G., Microsc. Res. Techniq. 2003, 62, 279. PubMed

Schoeppler V., Reich E., Vacelet J., Rosenthal M., Pacureanu A., Rack A., Zaslansky P., Zolotoyabko E., Zlotnikov I., Sci. Adv. 2017, 3, eaao2047. PubMed PMC

Levi C., C. R. Acad. Sci. 1963, 256, 497.

Drum R. W., J. Ultrastruct. Res. 1968, 22, 12. PubMed

Leys S. P., Biol. Bull. 1995, 188, 241. PubMed

Elliot G. D., Leys S. P., J. Exp. Biol. 2007, 210, 3736. PubMed

Mitchell J., Nichols S. A., EvoDevo 2019, 10, 26. PubMed PMC

Colgren J., Nichols S. A., A muscle‐related contractile tissue specified by myocardin‐related transcription factor activity in Porifera. bioRxiv. 2021, 10.1101/2021.04.11.439235. DOI

Palmer W. G., J. Chem. Soc. 1930, 1656.

Shore R. E., Biol. Bull. 1972, 143, 689. PubMed

Weaver J. C., Pietrasanta L. I., Hedin N., Chmelka B. F., Hansma P. K., Morse D. E., J. Struct. Biol. 2003, 144, 271. PubMed

Sabella C., Faszewski E., Himic L, Colpitts K. M., Kaltenbach J., Burger M. M., Fernandez‐Busquets X., J. Immun. 2007, 179, 5927. PubMed

Greenberg S. G., Davies P., Schein J. D., Binder L. I., J. Biol. Chem. 1992, 2, 564. PubMed

Frigeri L. G., Radabaugh T. R., Haynes P. A., Hildebrand M., Mol. Cell Proteomics 2006, 5, 182. PubMed

Lou Y.‐R., Kanninen L., Kaehr B., Townson J. L., Niklander J., Harjumäki R., Brinker C. J., Yliperttula M., Sci. Rep. 2015, 5, 13635. PubMed PMC

Adams A. E. M., Pringle J. R., Method Enzymol. 1991, 194, 729. PubMed

Wulf E., Deboben A., Bautz F. A., Faulstich H., Wieland T., Proc. Natl. Acad. Sci. USA 1979, 76, 4498. PubMed PMC

Revilla‐I‐Domingo R., Schmidt C., Zifko C., Raible F., Genetics 2018, 210, 435. PubMed PMC

Katoh K., Ichikawa H., Ishikawa H., J. Electron. Microsc. 1991, 40, 70. PubMed

Saczko‐Brack D., Warchol E., Rogez B., Kröss M., Heissler S. M., Sellers J. R., Batters C., Veigel C., Proc. Natl. Acad. Sci. USA 2016, 113, E8387. PubMed PMC

Nguyen L. T., Hirst L. S., Phys. Rev. 2011, 83, 031910. PubMed

Claessens M. M. A. E., Semmrich C., Ramos L., Bausch A. R., Proc. Natl. Acad. Sci. USA 2008, 105, 8819. PubMed PMC

Oda T., Yanagisawa H., Commun. Biol. 2020, 3, 585. PubMed PMC

von der Ecken J., Müller M., Lehman W., Mannstein D. J., Nature 2015, 519, 114. PubMed PMC

Tesson B., Hildebrand M., PlosOne 2010, 5, e14300. PubMed PMC

Van de Meene A. M. L., Pickett‐Heaps J. D., Eur. J. Phycol. 2004, 39, 93.

Schmid A. M. M., Nova Hedwiga 1980, 33,811.

Blank G. S., Sullivan C. W., J. Phycol. 1983, 19, 39.

Cohn S. A., Nash J., Pickett‐Heaps J. D., Protoplasma 1989, 149, 130.

Durak G. M., Brownlee C., Wheeler G. L., Sci. Rep. 2017, 7, 15409. PubMed PMC

Ayscough K. R., Stryker J., Pokala N., Sanders M., Crews P., Drubin D. G., J. Cell Biol. 1997, 137, 399. PubMed PMC

Spector I., Shochet N. R., Kashman Y., Groweiss A., Science 1983, 219, 493. PubMed

Ganot P., Tambutté E., Caminiti‐Segonds N., Toullec G., Allemand D., Tambutté S., eLife 2020, 9, e50022. PubMed PMC

Novick P., Botstein D., Cell 1985, 40, 405. PubMed

Morton W. M., Ayscough K. R., McLaughlin P. J., Nat. Cell Biol. 2000, 2, 376. PubMed

Tyszka J., Bickmeyer U., Raitzsch M., Bijma J., Kaczmarek K., Mewes A., Topa P., Janse M., Proc. Natl. Acad. Sci. USA 2019, 116, 4111. PubMed PMC

Simpson T. L., Gil M., Connes R., Diaz J. P., Paris J., J. Morphol. 1985, 183, 117. PubMed

Risca V. I., Wang E. B., Chaudhuri O., Chia J. J., Geissler P. L., Fletcher D. A., Proc. Natl. Acad. Sci. USA 2012, 109, 2913. PubMed PMC

Eckert C., Schröder H. C., Brandt D., Perovic‐Ottstadt S., Müller W. E. G., J. Histochem. Cytochem. 2006, 54, 1031. PubMed

Görlich S., Samuel A. J., Best R. J., Seidel R., Vacelet J., Leonarski F. K., Tomizaki T., Rellinghaus B., Pohl D., Zlotnikov I., Proc. Natl. Acad. Sci. USA 2020, 117, 31088. PubMed PMC

Aizenberg J., Weaver J. C., Thanawala M. S., Sundar V. C., Morse D. E., Fratzl P., Science 2005, 309, 275. PubMed

Letort G., Politi A. Z., Ennomani H., Théry M., Nedelec F., Blanchoin L., PLoS Comput. Biol. 2015, 11, e1004245. PubMed PMC

Antcliffe J., Callow R., Brasier M. G., Biol. Rev. 2014, 89, 972. PubMed

Discovery of mammalian collagens I and III within ancient poriferan biopolymer spongin