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Mineralization of the metre-long biosilica structures of glass sponges is templated on hydroxylated collagen

Abstract

The minerals involved in the formation of metazoan skeletons principally comprise glassy silica, calcium phosphate or carbonate. Because of their ancient heritage, glass sponges (Hexactinellida) may shed light on fundamental questions such as molecular evolution, the unique chemistry and formation of the first skeletal silica-based structures, and the origin of multicellular animals. We have studied anchoring spicules from the metre-long stalk of the glass rope sponge (Hyalonema sieboldi; Porifera, Class Hexactinellida), which are remarkable for their size, durability, flexibility and optical properties. Using slow-alkali etching of biosilica, we isolated the organic fraction, which was revealed to be dominated by a hydroxylated fibrillar collagen that contains an unusual [Gly–3Hyp–4Hyp] motif. We speculate that this motif is predisposed for silica precipitation, and provides a novel template for biosilicification in nature.

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Figure 1: Marine glass sponge Hyalonema sieboldi, a typical member of the Hyalonematidae family.
Figure 2: Analysis of the isolated spicular organic matrix.
Figure 3: HR-TEM images of silicification on H. sieboldii collagen.

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References

  1. Shimizu, K., Cha, J., Stucky, G. D. & Morse, D. E. Silicatein alpha: cathepsin L-like protein in sponge biosilica. Proc. Natl Acad. Sci. USA 95, 6234–6238 (1998).

    Article  CAS  Google Scholar 

  2. Cha, J. N. et al. 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 (1999).

    Article  CAS  Google Scholar 

  3. Müller, W. E. G. et al. Silicateins, the major biosilica forming enzymes present in demosponges: protein analysis and phylogenetic relationship. Gene 395, 62–71 (2007).

    Article  Google Scholar 

  4. Müller, W. E. G. et al. Unique transmission properties of the stalk spicules from the hexactinellid Hyalonema sieboldi. Biosens. Bioelectron. 21, 1149–1155 (2006).

    Article  Google Scholar 

  5. Dayton, P. K. Observations of growth, dispersal and population dynamics of some sponges in McMurdo Sound, Antarctica, in Colloques internationaux du C.N.R.S. 291. Biologie des spongiaires (eds Levi, C. & Boury-Esnault, N.), 271–282 (Editions du Centre National de la Recherche Scientifique, 1979).

    Google Scholar 

  6. Ehrlich, H. & Worch, H. Collagen, a huge matrix in glass-sponge flexible spicules of the meter-long Hyalonema sieboldi, in Handbook of Biomineralization Vol. 1. The Biology of Biominerals Structure Formation (ed. Bäuerlein, E.) 23–41 (Wiley VCH, 2007).

    Google Scholar 

  7. Müller, W. E. G. et al. Silicatein expression in the hexactinellid Crateromorpha meyeri: the lead marker gene restricted to siliceous sponges. Cell Tissue Res. 333, 339–351 (2008).

    Article  Google Scholar 

  8. Ehrlich, H. et al. A modern approach to demineralization of spicules in glass sponges (Porifera: Hexactinellida) for the purpose of extraction and examination of the protein matrix. Russ. J. Marine Biol. 32, 186–193 (2006).

    Article  CAS  Google Scholar 

  9. Ehrlich, H. et al. Nanostructural organization of naturally occurring composites. Part I. Silica-collagen-based biocomposites. J. Nanomater. doi:10.1155/2008/623838 (2008).

  10. Ehrlich, H., Heinemann, S., Hanke, T. & Worch, H. Hybrid materials from a silicate-treated collagen matrix, methods for the production thereof and the use thereof. International patent WO2008/023025 (2008).

  11. Travis, D. F., Francois, C. J., Bonar, L. C. & Glimcher, M. J. Comparative studies of the organic matrices of invertebrate mineralized tissues. J. Ultrastruct. Res. 18, 519–550 (1967).

    Article  CAS  Google Scholar 

  12. Ehrlich, H. et al. Nanostructural organization of naturally occurring composites. Part II. Silica-chitin-based biocomposites. J. Nanomater. doi:10.1155/2008/670235 (2008).

  13. Leys, S. P. Cytoskeletal architecture and organelle transport in giant syncytia formed by fusion of hexactinellid sponge tissues. Biol. Bull. 188, 241–254 (1995).

    Article  CAS  Google Scholar 

  14. Diehl-Seifert, B. et al. Attachment of sponge cells to collagen substrata: effect of a collagen assembly factor. J. Cell Sci. 79, 271–285 (1985).

    CAS  PubMed  Google Scholar 

  15. Nakajima, T. & Volcani, B. E. 3,4-Dihydroxyproline: a new amino acid in diatom cell walls. Science 164, 1400–1401 (1969).

    Article  CAS  Google Scholar 

  16. Hecky, R. E., Mopper, K., Kilham, P. & Degens, E. T. The amino acid and sugar composition of diatom cell walls. Mar. Biol. 19, 323–331 (1973).

    Article  CAS  Google Scholar 

  17. Sadava, D. & Volcani, B. E. Studies on the biochemistry and fine structure of silica shell formation in diatoms. Formation of hydroxyproline and dihydroxyproliner in Nitzschia angularis. Planta 135, 7–11 (1977).

    Article  CAS  Google Scholar 

  18. Schumacher, M. A., Mizuno, K. & Bachinger, H. P. The crystal structure of a collagen-like polypeptide with 3(S)-hydroxyproline residues in the Xaa position forms a standard 7/2 collagen triple helix. J. Biol. Chem. 281, 27566–27574 (2006).

    Article  CAS  Google Scholar 

  19. Tilburey, G. E., Patwardhan, S. V., Huang, J., Kaplan, D. L. & Perry, C. C. Are hydroxyl-containing biomolecules important in biosilicification? A model study. J. Phys. Chem. B 111, 4630–4638 (2007).

    Article  CAS  Google Scholar 

  20. Kulchin, Y. N. et al. Optical fibres based on natural biological minerals—sea sponge spicules. Quantum Electron. 38, 51–55 (2008).

    Article  CAS  Google Scholar 

  21. Pouget, E. et al. Hierarchical architectures by synergy between dynamical template self-assembly and biomineralization. Nature Mater. 6, 434–439 (2007).

    Article  CAS  Google Scholar 

  22. Exposito, J.-Y., Cluzel, C., Garrone, R. & Lethias, C. Evolution of collagens. Anat. Rec. 268, 302–316 (2002).

    Article  CAS  Google Scholar 

  23. Livingston, B. T. et al. A genome-wide analysis of biomineralization-related proteins in the sea urchin Strongylocentrotus purparatus. Dev. Biol. 300, 335–348 (2006).

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Acknowledgements

This work was partially supported by NE/C511148/1 grant to M.J.C. and J.T.-O., by a joint grant from Deutscher Akademischer Austauschdienst (DAAD) (grant ref. 325; A/08/72558) and Russian Ministry of Education and Science (RMES) (AVCP grant no. 8066) to V.V.B., and by the Erasmus Mundus External Co-operation Programme of the European Union 2009 to D.K. The Centre of Excellence in Mass Spectrometry (CoEMS) at York is supported by Science City York and Yorkshire Forward using funds from the Northern Way Initiative. The authors also thank H. Lichte for use of the facilities at the Special Electron Microscopy Laboratory for high-resolution and holography at Triebenberg, TU Dresden, Germany. The authors thank G. Bavestrello, K. Tabachnick, M. Hofreiter, H. Roempler and E. Bäeuerlein for their helpful discussions. Finally, the authors are very grateful to S. Paasch, H. Meissner, G. Richter, T. Hanke, O. Trommer, A. Mensch, S. Heinemann for excellent technical assistance. G.W. acknowledges funding from the German Science Foundation (DFG). Financial support by DFG (Graduiertenkolleg 378) to R.H. and T.L. and the European Fund for Regional Structure Development (EFRE, European Union and Free State Saxonia) to R.H. is gratefully acknowledged.

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All authors contributed to the design or execution of experiments, or analysed data. H.E. supervised the experiments, carried out demineralization experiments, performed collagen isolation, and wrote the manuscript. P.S. performed SEM and HRTEM, and prepared figures. A.E. collected, prepared and identified sponge samples and contributed to writing the manuscript. M.M., D.V.V., K.K. and S.L.M. performed NEXAFS experiments and designed figures. M.T. and V.V.B. carried out collagen modification. S.H. performed FTIR and prepared figures. E.B. performed NMR. R.D. performed Edman degradation and R.H. and T.L. performed amino acid analysis and mass spectrometry. M.C., H.K., C.S., Y.Y., E.C., D.A., M.L., C.B. and J.T.-O. were involved in acquiring and interpreting the mass spectrometric data, and M.C., H.K., E.C., D.A. and J.T.-O contributed to the writing of the manuscript. H.W., M.C., H.E., G.W., J.R., V.S. and E.B. analysed the results with regard to evolutionary implications and mechanisms of biomineralization, designed concepts, and wrote the manuscript.

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Correspondence to Hermann Ehrlich or Matthew J. Collins.

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Ehrlich, H., Deutzmann, R., Brunner, E. et al. Mineralization of the metre-long biosilica structures of glass sponges is templated on hydroxylated collagen. Nature Chem 2, 1084–1088 (2010). https://doi.org/10.1038/nchem.899

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