Abstract
Silicatein is the main protein responsible for the formation of spicules, tiny structures that constitute the silica skeleton of marine demosponges (Phylum Porifera). A unique innovation in Porifera that evolved from the cathepsin L family of proteins, it has been reported that two amino acids (S and H) are necessary to form the catalytic triad (SHN) to enable silica condensation. However, a diversity of silicatein sequence variants has since been reported with a variable pattern of presence/absence across sponge groups. Variants containing CHN or C/SQN at the active site appear more common in sponges from the Haplosclerida. Here, we report the expression levels of five silicatein variants through different developmental stages in the haplosclerid Haliclona indistincta. All five silicatein variants were expressed at low levels in the free-swimming larvae, which lack spicules and expression significantly increased at the two developmental phases in which spicules were visible. At these two phases, silicateins of CHN and C/SQN types were much more highly expressed than the SHN type indicating a possible ability of active sites with these alternative amino acids to condense silica and a more complex evolutionary story for spicule formation in marine demosponges than previously understood.
References
Aguilar-Camacho JM, Doonan L, McCormack GP (2019) Evolution of the main skeleton-forming genes in sponges (Phylum Porifera) with special focus on the marine Haplosclerida (Class Demospongiae). Mol Phylogenet Evol 131:245–253. https://doi.org/10.1016/j.ympev.2018.11.015
Bergquist PR, Green CR (1977) An ultrastructural study of settlement and metamorphosis in sponge larvae. Cah Biol Mar 18:289–302
Brutchey RL, Morse DE (2008) Silicatein and the translation of its molecular mechanism of biosilicification into low temperature nanomaterial synthesis. Chem Rev 108(11):4915–4934
Cao X, Fu W, Yu X, Zhang W (2007) Dynamics of spicule production in the marine sponge Hymeniacidon perlevis during in vitro cell culture and seasonal development in the field. Cell Tissue Res 329(3):595–608
Cha JN, Shimizu K, Zhou Y, Christiansen SC, Chmelka BF, Stucky GD, Morse DE (1999) Silicatein filaments and subunits from a marine sponge direct the polymerization of silica and silicones in vitro. P Natl Acad Sci USA 96(2):361–365
Fairhead M, Johnson KA, Kowatz T, McMahon SA, Carter LG, Oke M, Liu H, Naismith JH, van der Walle CF (2008) Crystal structure and silica condensing activities of silicatein α–cathepsin L chimeras. Chem Commun (15):1765–1767
Gauthier A (2015) Analysis of silicatein gene expression and spicule formation in the demosponge Amphimedon queenslandica MS thesis. The University of Queensland, 84 pp.
Kamenev DG, Shkryl YN, Veremeichik GN, Golotin VA, Naryshkina NN, Timofeeva YO, Kovalchuk SN, Semiletova IV, Bulgakov VP (2015) Silicon crystals formation using silicatein-like cathepsin of marine sponge Latrunculia oparinae. J Nanosci Nanotechnol 15(12):10046–10049
Kozhemyako VB, Veremeichik GN, Shkryl YN, Kovalchuk SN, Krasokhin VB, Rasskazov VA, Zhuravlev YN, Bulgakov VP, Kulchin YN (2010) Silicatein genes in spicule-forming and nonspicule-forming Pacific demosponges. Mar Biotechnol 12(4):403–409
Krasko A, Lorenz B, Batel R, Schröder HC, Müller IM, Müller WE (2000) Expression of silicatein and collagen genes in the marine sponge Suberites domuncula is controlled by silicate and myotrophin. FEBS J 267(15):4878–4887
Leys SP (2003) Comparative study of spiculogenesis in demosponge and hexactinellid larvae. Microsc Res Tech 62(4):300–311
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25(4):402–408
Maldonado M (2006) The ecology of the sponge larva. Can J Zool 84(2):175–194
Maldonado M, Bergquist P (2002) Phylum porifera. In: Atlas of marine invertebrae larvae. Academic Press, San Diego, pp 21–50
Maldonado M, George SB, Young CM, Vaquerizo I (1997) Depth regulation in parenchymella larvae of a demosponge: relative roles of skeletogenesis, biochemical changes and behavior. Mar Ecol Prog Ser 148(1–3):115–124
Mohri K, Nakatsukasa M, Masuda Y, Agata K, Funayama N (2008) Toward understanding the morphogenesis of siliceous spicules in freshwater sponge: differential mRNA expression of spicule-type-specific silicatein genes in Ephydatia fluviatilis. Dev Dyn 237(10):3024–3039
Müller WE, Rothenberger M, Boreiko A, Tremel W, Reiber A, Schröder HC (2005) Formation of siliceous spicules in the marine demosponge Suberites domuncula. Cell Tissue Res 321(2):285–297
Müller WE, Schloßmacher U, Eckert C, Krasko A, Boreiko A, Ushijima H, Wolf S, Tremel W, Müller I, Schröder HC (2007) Analysis of the axial filament in spicules of the demosponge Geodia cydonium: different silicatein composition in microscleres (asters) and megascleres (oxeas and triaenes). Eur J Cell Biol 86(8):473–487
Müller WE, Schröder HC, Burghard Z, Pisignano D, Wang X (2013) Silicateins—a novel paradigm in bioinorganic chemistry: enzymatic synthesis of inorganic polymeric silica. Chem-Eur J 19(19):5790–5804
Nakayama S, Arima K, Kawai K, Mohri K, Inui C, Sugano W, Koba H, Tamada K, Nakata YJ, Kishimoto K, Arai-shindo M, Kojima C, Matsumoto T, Fujimori T, Agata K, Funayama N (2015) Dynamic transport and cementation of skeletal elements build up the pole–and–beam structured skeleton of sponges Curr Biol 25(19): 2549–2554
Rao X, Huang X, Zhou Z, Lin X (2013) An improvement of the 2ˆ (−delta delta CT) method for quantitative real-time polymerase chain reaction data analysis. Biostatistics, Bioinformat Biomathematics 3(3):71
Riesgo A, Maldonado M, López-Legentil S, Giribet G (2015) A proposal for the evolution of cathepsin and silicatein in sponges. J Mol Evol 80(5–6):278–291
Robert X, Gouet P (2014) Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res 42(W1):W320–W324
Schoeppler V, Reich E, Vacelet J, Rosenthal M, Pacureanu A, Rack A, Zaslansky P, Zolotoyabko E, Zlotnikov I (2017) Shaping highly regular glass architectures: a lesson from nature. Sci Adv 3(10):eaao2047
Schröder HC, Wang X, Manfrin A, Yu SH, Grebenjuk VA, Korzhev M, Wiens M, Schlossmacher U, Müller WE (2012) Acquisition of structure-guiding and structure-forming properties during maturation from the pro-silicatein to the silicatein form. J Biol Chem 287(26):22196–22205
Shimizu K, Cha J, Stucky GD, Morse DE (1998) Silicatein α: cathepsin L-like protein in sponge biosilica. P Natl Acad Sci USA 95(11):6234–6238
Shkryl YN, Bulgakov VP, Veremeichik GN, Kovalchuk SN, Kozhemyako VB, Kamenev DG, Semiletova IV, Timofeeva YO, Scchipunov YA, Kulchin YN (2016) Bioinspired enzymatic synthesis of silica nanocrystals provided by recombinant silicatein from the marine sponge Latrunculia oparinae. Bioprocess Biosyst Eng 39(1):53–58
Stephens KM, Galvin J, Lawless A, McCormack GP (2013a) Reproductive cycle and larval characteristics of the sponge Haliclona indistincta (Porifera: Demospongiae). J Mar Biol Assoc UK 93(4):899–907
Stephens KM, Ereskovsky A, Lalor P, McCormack GP (2013b) Ultrastructure of the ciliated cells of the free-swimming larva, and sessile stages, of the marine sponge Haliclona indistincta (Demospongiae: haplosclerida). J Morphol 274(11):1263–1276
Uriz MJ, Turon X, Becerro MA (2000) Silica deposition in demosponges: spiculogenesis in Crambe crambe. Cell Tissue Res 301(2):299–309
Uriz MJ, Turon X, Becerro MA, Agell G (2003) Siliceous spicules and skeleton frameworks in sponges: origin, diversity, ultrastructural patterns, and biological functions. Microsc Res Tech 62(4):279–299
Weaver JC, Morse DE (2003) Molecular biology of demosponge axial filaments and their roles in biosilicification. Microsc Res Tech 62(4):356–367
Werner P, Blumtritt H, Natalio F (2017) Organic crystal lattices in the axial filament of silica spicules of Demospongiae. J Struct Biol 198(3):186–195
Zhou Y, Shimizu K, Cha JN, Stucky GD, Morse DE (1999) Efficient catalysis of polysiloxane synthesis by silicatein α requires specific hydroxy and imidazole functionalities. Angew Chem 38(6):779–782
Funding
JMAC is funded by a Hardiman Scholarship at the National University of Ireland, Galway. This project was funded by a Thomas Crawford scheme awarded to JMAC.
Author information
Authors and Affiliations
Contributions
JMAC and GM designed all the experiments. JMAC conducted the qPCR experiments, statistical analysis, and designed the figures. JMAC and GM interpreted the results and wrote the manuscript.
Corresponding author
Additional information
Communicated by Mark Q. Martindale
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Aguilar-Camacho, J.M., McCormack, G.P. Silicatein expression in Haliclona indistincta (Phylum Porifera, Order Haplosclerida) at different developmental stages. Dev Genes Evol 229, 35–41 (2019). https://doi.org/10.1007/s00427-019-00627-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00427-019-00627-7