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Silicatein expression in the hexactinellid Crateromorpha meyeri: the lead marker gene restricted to siliceous sponges

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Abstract

The siliceous spicules of sponges (Porifera) are synthesized by the enzyme silicatein. This protein and its gene have been identified so far in the Demospongiae, e.g., Tethya aurantium and Suberites domuncula. In the Hexactinellida, the second class of siliceous sponges, the mechanism of synthesis of the largest bio-silica structures on Earth remains obscure. Here, we describe the morphology of the spicules (diactines and stauractines) of the hexactinellid Crateromorpha meyeri. These spicules are composed of silica lamellae concentrically arranged around a central axial canal and contain proteinaceous sheaths (within the siliceous mantel) and proteinaceous axial filaments (within the axial canal). The major protein in the spicules is a 24-kDa protein that strongly reacts with anti-silicatein antibodies in Western blots. Its cDNA has been successfully cloned; the deduced hexactinellid silicatein comprises, in addition to the characteristic catalytic triad amino acids Ser-His-Asn and the “conventional” serine cluster, a “hexactinellid C. meyeri-specific” Ser cluster. We show that anti-silicatein antibodies react specifically with the proteinaceous matrix of the C. meyeri spicules. The characterization of silicatein at the genetic level should contribute to an understanding of the molecular/biochemical mechanism of spiculogenesis in Hexactinellida. These data also indicate that silicatein is an autapomorphic molecule common to both classes of siliceous sponges.

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References

  • Aizenberg J, Weaver JC, Thanawala MS, Sundar VC, Morse DE, Fratzel P (2005) Skeleton of Euplectella sp.: structural hierarchy from nanoscale to the macroscale. Science 309:275–278

    Article  PubMed  CAS  Google Scholar 

  • Barrett AJ, Rawlings ND, Woessner JF (2002) Handbook of proteolytic enzymes. Academic Press, Amsterdam

    Google Scholar 

  • Cha JN, Shimizu K, Zhou Y, Christianssen 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. Proc Natl Acad Sci USA 96:361–365

    Article  PubMed  CAS  Google Scholar 

  • Christensen JE, Dudley EG, Pederson JA, Steele JL (1999) Peptidases and amino acid catabolism in lactic acid bacteria. Antonie van Leeuwenhoek 76:217–246

    Article  PubMed  CAS  Google Scholar 

  • Dayhoff MO, Schwartz RM, Orcutt BC (1978) A model of evolutionary change in protein. In: Dayhoff MO (ed) Atlas of protein sequence and structure. National Biomedical Research Foundation, Washington DC, pp 345–352

    Google Scholar 

  • Deane CM, Blundell TL (2001) CODA: a combined algorithm for predicting the structurally variable regions of protein models. Protein Sci 10:599–612

    Article  PubMed  CAS  Google Scholar 

  • Eckert C, Janussen D (2005) Die Glasschwämme der Sagami-Bucht und ihre Erforschung. Natur und Museum (Frankfurt) 135:105–116

    Google Scholar 

  • Ehrlich H, Heinemann S, Heinemann C, Simon P, Bazhenov VV, Shapkin NP, Born R, Tabachnick KR, Hanke T, Worch H (2008) Nanostructural organization of maturally occurring composites. Part I. Silica-collagen-based biocomposites. J Nanomat. doi:10.1155/2008/623838

  • Felsenstein J (1993) PHYLIP, ver. 3.5. University of Washington, Seattle

    Google Scholar 

  • Hoffmann PA, Schrag DP (2002) The snowball Earth hypothesis: testing the limits of global change. Terra Nova 14:129–155

    Article  Google Scholar 

  • Junqueira LC, Bignolas G, Brentani RR (1979) Picrosirius staining plus polarization microscopy, a specific method for collagen detection in tissue sections. Histochem J 11:447–455

    Article  PubMed  CAS  Google Scholar 

  • Kaluzhnaya OV, Belikov SI, Schröder HC, Wiens M, Giovine M, Krasko A, Müller IM, Müller WEG (2005a) Dynamics of skeletal formation in the Lake Baikal sponge Lubomirskia baicalensis. Part I. Biological and biochemical studies. Naturwissenschaften 92:128–133

    Article  PubMed  CAS  Google Scholar 

  • Kaluzhnaya OV, Belikov SI, Schröder HC, Rothenberger M, Zapf S, Kaandorp JA, Borejko A, Müller IM, Müller WEG (2005b) Dynamics of skeleton formation in the Lake Baikal sponge Lubomirskia baicalensis. Part II. Molecular biological studies. Naturwissenschaften 92:134–138

    Article  PubMed  CAS  Google Scholar 

  • Krasko A, Batel R, Schröder HC, Müller IM, Müller WEG (2000) Expression of silicatein and collagen genes in the marine sponge Suberites domuncula is controlled by silicate and myotrophin. Eur J Biochem 267:4878–4887

    Article  PubMed  CAS  Google Scholar 

  • Kruse M, Leys S, Müller IM, Müller WEG (1998) Phylogenetic position of the Hexactinellida within the phylum Porifera based on amino acid sequence of the protein kinase C from Rhabdocalyptus dawsoni. J Mol Evol 46:721–728

    Article  PubMed  CAS  Google Scholar 

  • Müller WEG (2001) How was the metazoan threshold crossed: the hypothetical Urmetazoa. Comp Biochem Physiol [A] 129:433–460

    Google Scholar 

  • Müller WEG, Krasko A, Le Pennec G, Steffen R, Ammar MSA, Wiens M, Müller IM, Schröder HC (2003) Molecular mechanism of spicule formation in the demosponge Suberites domuncula: silicatein - collagen - myotrophin. Progr Mol Subcell Biol 33:195–222

    Google Scholar 

  • Müller WEG, Wiens M, Adell T, Gamulin V, Schröder HC, Müller IM (2004) The bauplan of the Urmetazoa: the basis of the genetic complexity of Metazoa using the siliceous sponges [Porifera] as living fossils. Int Rev Cytol 235:53–92

    Article  PubMed  Google Scholar 

  • Müller WEG, Rothenberger M, Boreiko A, Tremel W, Reiber A, Schröder HC (2005) Formation of siliceous spicules in the marine demosponge Suberites domuncula. Cell Tissue Res 321:285–297

    Article  PubMed  Google Scholar 

  • Müller WEG, Boreiko A, Wang X, Belikov SI, Wiens M, Grebenjuk VA, Schloßmacher U, Schröder HC (2007a) Silicateins, the major biosilica forming enzymes present in demosponges: protein analysis and phylogenetic relationship. Gene 395:62–71

    Article  PubMed  CAS  Google Scholar 

  • Müller WEG, Li J, Schröder HC, Qiao L, Wang X (2007b) The unique skeleton of siliceous sponges (Porifera; Hexactinellida and Demospongiae) that evolved first from the Urmetazoa during the Proterozoic: a review. Biogeosciences 4:219–232

    Article  Google Scholar 

  • Müller WEG, Schloßmacher U, Eckert C, Krasko A, Boreiko A, Ushijima H, Wolf SE, Tremel W, Schröder HC (2007c) 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 86:473–487

    Article  PubMed  CAS  Google Scholar 

  • Müller WEG, Wang X, Belikov SI, Tremel W, Schloßmacher U, Natoli A, Brandt D, Boreiko A, Tahir MN, Müller IM, Schröder HC (2007d) Formation of siliceous spicules in demosponges: example Suberites domuncula. In: Bäuerlein E (ed) Handbook of biomineralization, vol 1: biological aspects and structure formation. Wiley-VCH, Weinheim, pp 59–82

    Google Scholar 

  • Müller WEG, Eckert C, Kropf K, Wang X, Schloßmacher U, Seckert C, Wolf SE, Tremel W, Schröder HC (2007e) Formation of the giant spicules of the deep sea hexactinellid Monorhaphis chuni (Schulze 1904): electron microscopical and biochemical studies. Cell Tissue Res 329:363–378

    Article  PubMed  CAS  Google Scholar 

  • Müller WEG, Boreiko A, Schloßmacher U, Wang X, Tahir MN, Tremel W, Brandt D, Kaandorp JA, Schröder HC (2007f) Fractal-related assembly of the axial filament in the demosponge Suberites domuncula: relevance to biomineralization and the formation of biogenic silica. Biomaterials 28:4501–4511

    Article  PubMed  CAS  Google Scholar 

  • Müller WEG, Boreiko A, Schloßmacher U, Wang X, Eckert C, Kropf K, Li J, Schröder HC (2008a) Identification of a silicatein(-related) protease in the giant spicules of the deep sea hexactinellid Monorhaphis chuni. J Exp Biol 211:300–309

    Article  PubMed  CAS  Google Scholar 

  • Müller WEG, Schloßmacher U, Wang X, Boreiko A, Brandt D, Wolf SE, Tremel W, Schröder HC (2008b) Poly(silicate)-metabolizing silicatein in siliceous spicules and silicasomes of demosponges comprises dual enzymatic activities (silica-polymerase and silica-esterase). FEBS J 275:362–370

    Article  PubMed  CAS  Google Scholar 

  • Müller WEG, Wang X, Kropf K, Ushijima H, Geurtsen W, Eckert C, Tahir MN, Tremel W, Boreiko A, Schloßmacher U, Li J, Schröder HC (2008c) Bioorganic/inorganic hybrid composition of sponge spicules: matrix of the giant spicules and of the comitalia of the deep sea hexactinellid Monorhaphis. J Struct Biol 161:188–203

    Article  PubMed  CAS  Google Scholar 

  • Nicholas KB, Nicholas HB Jr (1997) GeneDoc: a tool for editing and annotating multiple sequence alignments. Version 1.1.004. Distributed by the author; cris.com/×ketchup/genedoc.shtml

  • Ramachandran GN, Ramakrishnan C, Sasisekharan V (1963) Stereochemistry of polypeptide chain configurations. J Mol Biol 7:95–99

    Article  PubMed  CAS  Google Scholar 

  • Reitner J (1992) Coralline Spongien. Der Versuch einer phylogenetisch-taxonomischen Analyse. Berl Geowiss Abh 1:1–352

    Google Scholar 

  • Reitner J, Wörheide G (2002) Non-lithistid Demospongiae-origins of their palaeobiodiversity and highlights in history of preservation. In: Hooper JNA, Soest RWM van (eds) Systema porifera: a guide to the classification of sponges. Kluwer Academic/Plenum, New York, pp 52–70

    Google Scholar 

  • Robinson PN (2007) A Java program for drawing Ramachandran plots. From: peter.robinson@charite.de

  • Sali A, Blundell TL (1993) Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234:779–815

    Article  PubMed  CAS  Google Scholar 

  • Sandford F (2003) Physical and chemical analysis of the siliceous skeletons in six sponges of the two groups (Demospongiae and Hexactinellida). Microsc Res Tech 62:336–355

    Article  PubMed  CAS  Google Scholar 

  • Schäcke H, Müller IM, Müller WEG (1994) Tyrosine kinase from the marine sponge Geodia cydonium. In: Müller WEG (ed) Use of aquatic invertebrates as tools for monitoring of environmental hazards. Fischer, Stuttgart, pp 201–211

    Google Scholar 

  • Schröder HC, Perović-Ottstadt S, Rothenberger M, Wiens M, Schwertner H, Batel R, Korzhev M, Müller IM, Müller WEG (2004) Silica transport in the demosponge Suberites domuncula: fluorescence emission analysis using the PDMPO probe and cloning of a potential transporter. Biochem J 381:665–673

    Article  PubMed  Google Scholar 

  • Schröder HC, Boreiko A, Korzhev M, Tahir MN, Tremel W, Eckert C, Ushijima H, Müller IM, Müller WEG (2006) Co-expression and functional interaction of silicatein with galectin: matrix-guided formation of siliceous spicules in the marine demosponge Suberites domuncula. J Biol Chem 281:12001–12009

    Article  PubMed  CAS  Google Scholar 

  • Schröder HC, Brandt D, Schloßmacher U, Wang X, Tahir MN, Tremel W, Belikov SI, Müller WEG (2007a) Enzymatic production of biosilica-glass using enzymes from sponges: basic aspects and application in nanobiotechnology (material sciences and medicine). Naturwissenschaften 94:39–359

    Article  CAS  Google Scholar 

  • Schröder HC, Natalio F, Shukoor I, Tremel W, Schloßmacher U, Wang X, Müller WEG (2007b) Apposition of silica lamellae during growth of spicules in the demosponge Suberites domuncula: biological/biochemical studies and chemical/biomimetical confirmation. J Struct Biol 159:325–334

    Article  PubMed  CAS  Google Scholar 

  • Schultze M (1860) Die Hyalonemen. Adolph Marcus, Bonn

    Google Scholar 

  • Schulze FE (1887) Report on the Hexactinellida collected by H.M.S. Challenger during the years 1873–76. In: Thomson CW, Murray J (eds) Report of the scientific results of the voyage of H.M.S. Challenger during the years 1873–76, vol LIII. Eyre & Spottiswoode, London

    Google Scholar 

  • Schulze FE (1904) Hexactinellida. Wissenschaftliche Ergebnisse der Deutschen Tiefsee-Expedition, vol 4. Fischer, Jena

    Google Scholar 

  • Schulze P (1925) Zum morphologischen Feinbau der Kieselschwammnadeln. Z Morphol Ökol Tiere 4:615–625

    Article  Google Scholar 

  • Schütze J, Custodio MR, Efremova SM, Müller IM, Müller WEG (1999) Evolutionary relationship of Metazoa within the eukaryotes based on molecular data from Porifera. Proc R Soc Lond [Biol] 266:63–73

    Article  Google Scholar 

  • Shimizu K, Cha J, Stucky GD, Morse DE (1998) Silicatein alpha: cathepsin L-like protein in sponge biosilica. Proc Natl Acad Sci USA 95:6234–6238

    Article  PubMed  CAS  Google Scholar 

  • Taskiran D, Taskiran E, Yercan H, Kutay FZ (1999) Quantification of total collagen in rabbit tendon by the Sirius Red method. Turk J Med Sci 29:7–9

    CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Uriz MJ, Turon X, Becerro MA, Agell G (2003) Siliceous spicules and skeleton frameworks in sponges: origin, diversity, ultrastructural patterns, biological functions. Microsc Res Tech 62:279–299

    Article  PubMed  CAS  Google Scholar 

  • Vriend G, What IF (1990) A molecular modeling and drug design program. J Mol Graph 8:52–56

    Article  PubMed  CAS  Google Scholar 

  • Walker G (2003) Snowball Earth: the story of the great global catastrophe that spawned life as we know it. Crown, New York

    Google Scholar 

  • Wang X, Wang Y (2006) An introduction to the study on natural characteristics of sponge spicules and bionic applications. Adv Earth Sci 21:37–42

    Google Scholar 

  • Wang X, Li J, Qiao L, Schröder HC, Eckert C, Kropf K, Wang Y, Feng QL, Müller WEG (2007) Structure and characteristics of giant spicules of the deep sea hexactinellid sponges of the genus Monorhaphis (Hexactinellida: Amphidiscosida: Monorhaphididae). Acta Zool Sinica 53:557–569

    CAS  Google Scholar 

  • Weaver JC, Morse DE (2003) Molecular biology of demosponge axial filaments and their roles in biosilicification. Microsc Res Tech 62:356–367

    Article  PubMed  CAS  Google Scholar 

  • Weaver JC, Aizenberg J, Fantner GE, Kisailus D, Woesz A, Allen P, Fields K, Porter MJ, Zok FW, Hansma PK, Fratzl P, Morse DE (2007) Hierarchical assembly of the siliceous skeletal lattice of the hexactinellid sponge Euplectella aspergillum. J Struct Biol 158:93–106

    Article  PubMed  CAS  Google Scholar 

  • Wiens M, Belikov SI, Kaluzhnaya OV, Krasko A, Schröder HC, Perovic-Ottstadt S, Müller WEG (2006) Molecular control of serial module formation along the apical-basal axis in the sponge Lubomirskia baicalensis: silicateins, mannose-binding lectin and mago nashi. Dev Genes Evol 216:229–242

    Article  PubMed  CAS  Google Scholar 

  • Zhao B, Janson CA, Amegadzie BY, D’Alessio K, Griffin C, Hanning CR, Jones C, Kurdyla J, McQueney M, Qiu X, Smith WW, Abdel-Meguid SS (1997) Crystal structure of human osteoclast cathepsin K complex with E-64. Nat Struct Biol 4:109–111

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank Mr. G. Glasser (Research group “Surface Chemistry”, Prof. H.J. Butt and Dr. I. Lieberwirth; Max Planck Institute for Polymer Research, Mainz) for excellent assistance with the electron-microscopic analysis. The investigated material and photographs of the animals were kindly supplied by Dr. Dorthe Janussen (Department of Marine Evertebrates I, Research Institute and Natural Museum Senckenberg, Frankfurt/Main). Thanks are also due to Mr. C. Eckert (Institut für Physiologische Chemie, University of Mainz) for help during the collection of the material.

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Correspondence to Werner E. G. Müller.

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Sequences (cDNAs) from Crateromorpha meyeri have been deposited (EMBL/GenBank) as follows: for silicatein (SILCA_CRAME; accession no. AM920776), for cathepsin-like protein 1 (catl1_CRAME; AM904719), for cathepsin-like protein 2 (catl2_CRAME; AM904720), for cathepsin-like protein 3 (catl3_CRAME; AM904721), and for cathepsin-like protein 4 (catl4_CRAME; AM904722).

This work was supported by grants from the Deutsche Forschungsgemeinschaft/Wi 2116/2-2), the Bundesministerium für Bildung und Forschung, Germany (project: Center of Excellence BIOTECmarin), the Basic Science Research Program in China (no. 200607CSJ05), the China International Science and Technology Cooperation Program (no. 20071395), and the International Human Frontier Science Program.

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Müller, W.E.G., Wang, X., Kropf, K. et al. Silicatein expression in the hexactinellid Crateromorpha meyeri: the lead marker gene restricted to siliceous sponges. Cell Tissue Res 333, 339–351 (2008). https://doi.org/10.1007/s00441-008-0624-6

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