Skip to main content
SpringerLink
Log in

Giant basal spicule from the deep-sea glass sponge Monorhaphis chuni: synthesis of the largest bio-silica structure on Earth by silicatein

  • Research Article
  • Published:
Frontiers of Materials Science in China Aims and scope Submit manuscript

Abstract

Like all sponges (phylum Porifera), the glass sponges (Hexactinellida) are provided with an elaborate and distinct body plan, which relies on a filigree skeleton. It is constructed by an array of morphologically determined elements, the spicules. Schulze described the largest siliceous hexactinellid sponge on Earth, the up to 3 m high Monorhaphis chuni, collected during the German Deep Sea Expedition ”Valdivia“ (1898–1899). This species develops an equally large bio-silica structure, the giant basal spicule (3 m × 10 mm). Using these spicules as a model, one can obtain the basic knowledge on the morphology, formation, and development of silica skeletal elements. The silica matrix is composed of almost pure silica, endowing it with unusual optophysical properties, which are superior to those of man-made waveguides. Experiments suggest that the spicules function in vivo as a nonocular photoreception system. The spicules are also provided with exceptional mechanical properties. Like demosponges, the hexactinellids synthesize their silica enzymatically via the enzyme silicatein (27 kDa protein). This enzyme is located in/embedded in the silica layers. This knowledge will surely contribute to a further utilization and exploration of silica in biomaterial/biomedical science.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Kruse M, Müller I M, Muller W E G. Early evolution of metazoan serine/threonine and tyrosine kinases: Identification of selected kinases in marine sponges. Molecular Biology and Evolution, 1997, 14(12): 1326–1334

    PubMed  CAS  Google Scholar 

  2. Kruse M, Leys S P, Müller I M, et al. Phylogenetic position of the hexactinellida within the phylum porifera based on the amino acid sequence of the protein kinase C from Rhabdocalyptus dawsoni. Journal of Molecular Evolution, 1998, 46(6): 721–728

    Article  PubMed  CAS  Google Scholar 

  3. Müller W E G, Wiens M, Adell T, et al, Bauplan of Urmetazoa: Basis for genetic complexity of Metazoa. In: International Review of Cytology — A Survey of Cell Biology, Vol 235. San Diego: Elsevier Academic Press Inc, 2004, 53–92

    Google Scholar 

  4. Müller W E G, Li J H, Schröder H C, et al. The unique skeleton of siliceous sponges (Porifera; Hexactinellida and Demospongiae) that evolved first from the Urmetazoa during the Proterozoic: a review. Biogeosciences, 2007, 4(2): 219–232

    Article  Google Scholar 

  5. Pilcher H. Animal magnetism. Nature, 2005, 435(7045): 1022–1023

    Article  PubMed  ADS  CAS  Google Scholar 

  6. Murray J, Hjort J. The Depths of the Ocean. London: MacMillan, 1912

    Google Scholar 

  7. Schulze F E. Hexactinellida. Wissenschaftliche Ergebnisse der Deutschen Tiefsee-Expedition auf dem Dampfer ”Valdivia◂ 1898–1899. Stuttgart: Gustav Fischer Verlag, 1904

    Google Scholar 

  8. Roux M, Bouchet P, Bourseau J P, et al. L’environment bathyal au large de la Nouvelle-Calédonie: résultats preliminaries de la campagne CALSUB et consequences paléoécologiques. Geological Society of France, 1991, 162: 675–685

    Google Scholar 

  9. Müller W E G, Eckert C, Kropf K, et al. Formation of giant spicules in the deep-sea hexactinellid Monorhaphis chuni (Schulze 1904): electron-microscopic and biochemical studies. Cell and Tissue Research, 2007, 329(2): 363–378

    Article  PubMed  CAS  Google Scholar 

  10. Li J. Monorhaphis intermedia-a new species of Hexactinellida. Oceanologia et Limnologia Sinica, 1987, 18: 135–137

    Google Scholar 

  11. Tabachnick K R. Family Monorhaphididae Ijima, 1927. In: Hooper J N A, van Soest R. Systema Porifera: A Guide to the Classification of Sponges. New York: Kluwer Academic, 2002, 1264–1266

    Google Scholar 

  12. Wang X H, Li J H, Qiao L, et al. Structure and characteristics of giant spicules of the deep sea hexactinellid sponges of the genus Monorhaphis (Hexactinellida: Amphidiscosida: Monorhaphididae). Acta Zoologica Sinica, 2007, 53(3): 557–569

    CAS  Google Scholar 

  13. Sandford F. Physical and chemical analysis of the siliceous skeletons in six sponges of two groups (Demospongiae and Hexactinellida). Microscopy Research and Technique, 2003, 62 (4): 336–355

    Article  PubMed  CAS  Google Scholar 

  14. Uriz M J, Turon X, Becerro M A, et al. Siliceous spicules and skeleton frameworks in sponges: Origin, diversity, ultrastructural patterns, and biological functions. Microscopy Research and Technique, 2003, 62(4): 279–299

    Article  PubMed  CAS  Google Scholar 

  15. Uriz M J. Mineral spiculogenesis in sponges. Canadian Journal of Zoology, 2006, 84: 322–356

    Article  CAS  Google Scholar 

  16. Muller W E G, Jochum K P, Stoll B, et al. Formation of giant spicule from quartz glass by the deep sea sponge Monorhaphis. Chemistry of Materials, 2008, 20(14): 4703–4711

    Article  CAS  Google Scholar 

  17. Muller W E G, Wang X H, Kropf K, et al. Bioorganic/inorganic hybrid composition of sponge spicules: Matrix of the giant spicules and of the comitalia of the deep sea hexactinellid Monorhaphis. Journal of Structural Biology, 2008, 161(2): 188–203

    Article  PubMed  CAS  Google Scholar 

  18. Levi C, Barton J L, Guillemet C, et al. A remarkably strong natural glassy rod — the anchoring spicule of the Monorhaphis sponge. Journal of Materials Science Letters, 1989, 8(3): 337–339

    Article  CAS  Google Scholar 

  19. Müller W E G, Boreiko A, Schlossmacher U, et al. Identification of a silicatein(-related) protease in the giant spicules of the deep-sea hexactinellid Monorhaphis chuni. Journal of Experimental Biology, 2008, 211(3): 300–309

    Article  PubMed  CAS  Google Scholar 

  20. Müller W E G, Boreiko A, Wang X H, et al. Silicateins, the major biosilica forming enzymes present in demosponges: Protein analysis and phylogenetic relationship. Gene, 2007, 395(1-2): 62–71

    Article  PubMed  CAS  Google Scholar 

  21. Muller W E G, Rothenberger M, Boreiko A, et al. Formation of siliceous spicules in the marine demosponge Suberites domuncula. Cell and Tissue Research, 2005, 321(2): 285–297

    Article  PubMed  Google Scholar 

  22. Müller W E G, Boreiko A, Schlossmacher U, et al. Identification of a silicatein(-related) protease in the giant spicules of the deep-sea hexactinellid Monorhaphis chuni. Journal of Experimental Biology, 2008, 211(3): 300–309

    Article  PubMed  CAS  Google Scholar 

  23. Müller W E G, Schlossacher U, Wang X, et al. Poly(silicate)-metabolizing silicatein in siliceous spicules and silicasomes of demosponges comprises dual enzymatic activities (silica polymerase and silica esterase). FEBS Journal, 2008, 275(2): 362–370

    PubMed  Google Scholar 

  24. Wang X H, Schloßmacher U, Jochum K P, et al. Silica-protein composite layers of the giant basal spicules from Monorhaphis: basis for their mechanical stability. Pure and Applied Chemistry, 2009 (in press)

  25. Sumerel J L, Morse D E. Biotechnological advances in biosilicification. In: Silicon Biomineralization, Vol 33. Berlin: Springer-Verlag Berlin, 225–247

  26. Shimizu K, Cha J, Stucky G D, et al. Silicatein alpha: Cathepsin Llike protein in sponge biosilica. Proceedings of the National Academy of Sciences of the United States of America, 1998, 95(11): 6234–6238

    Article  PubMed  ADS  CAS  Google Scholar 

  27. Cha J N, Shimizu K, Zhou Y, et al. Silicatein filaments and subunits from a marine sponge direct the polymerization of silica and silicones in vitro. Proceedings of the National Academy of Sciences of the United States of America, 1999, 96(2): 361–365

    Article  PubMed  ADS  CAS  Google Scholar 

  28. Krasko A, Lorenz B, Batel R, et al. Expression of silicatein and collagen genes in the marine sponge Suberites domuncula is controlled by silicate and myotrophin. European Journal of Biochemistry, 2000, 267(15): 4878–4887

    Article  PubMed  CAS  Google Scholar 

  29. Müller W E G, Wang X H, Kropf K, et al. Silicatein expression in the hexactinellid Crateromorpha meyeri: the lead marker gene restricted to siliceous sponges. Cell and Tissue Research, 2008, 333 (2): 339–351

    Article  PubMed  CAS  Google Scholar 

  30. Müller W E, Krasko A, Le Pennec G, et al. Molecular mechanism of spicule formation in the demosponge Suberites domuncula: silicatein-collagen-myotrophin. Progress in Molecular and Subcellular Biology, 2003, 33: 195–221

    PubMed  Google Scholar 

  31. Wiens M, Belikov S I, Kaluzhnaya O V, et al. Molecular control of serial module formation along the apical-basal axis in the sponge Lubomirskia baicalensis: silicateins, mannose-binding lectin and mago nashi. Development Genes and Evolution, 2006, 216(5): 229–242

    Article  PubMed  CAS  Google Scholar 

  32. Müller W E G, Boreiko A, Schlossmacher U, et al. Fractal-related assembly of the axial filament in the demosponge Suberites domuncula: Relevance to biomineralization and the formation of biogenic silica. Biomaterials, 2007, 28(30): 4501–4511

    Article  PubMed  CAS  Google Scholar 

  33. Ramachandran G N, Ramakrishnan C, Sasisekharan V. Stereo-chemistry of polypeptide chain configurations. Journal of Molecular Biology, 1963, 7(1): 95–99

    Article  PubMed  CAS  Google Scholar 

  34. Robinson P N. A Java program for drawing Ramachandran plots. peter.robinson@charite.de, 2007

  35. Mayer G. Rigid biological systems as models for synthetic composites. Science, 2005, 310(5751): 1144–1147

    Article  PubMed  ADS  CAS  Google Scholar 

  36. Mayer G, Trejo R, Lara-Curzio E, et al. Lessons for new classes of inorganic/organic composites from the spicules and skeleton of the sea sponge Euplectella aspergillum. Mechanical Properties of Bioinspired and Biological Materials, 2005, 844: 79–86

    Google Scholar 

  37. Perovic S, Krasko A, Prokic I, et al. Origin of neuronal-like receptors in Metazoa: cloning of a metabotropic glutamate GABA-like receptor from the marine sponge Geodia cydonium. Cell and Tissue Research, 1999, 296(2): 395–404

    Article  PubMed  CAS  Google Scholar 

  38. Chevreux B, Pfisterer T, Drescher B, et al. Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Research, 2004, 14 (6): 1147–1159

    Article  PubMed  CAS  Google Scholar 

  39. Pavans de Ceccatty M. Coordination in sponges — foundations of integration. American Zoologist, 1974, 14(3): 895–903

    Google Scholar 

  40. Mackie G O. Is there a conduction system in sponges? Colloq Int Centre Natl Res Sci, 1979, 291: 145–151

    Google Scholar 

  41. Leys S P, Degnan B M. Cytological basis of photoresponsive behavior in a sponge larva. Biological Bulletin, 2001, 201(3): 323–338

    Article  PubMed  CAS  Google Scholar 

  42. Leys S P, Cronin T W, Degnan B M, et al. Spectral sensitivity in a sponge larva. Journal of Comparative Physiology A — Neuroethology Sensory Neural and Behavioral Physiology, 2002, 188(3): 199–202

    Article  Google Scholar 

  43. Cattaneo-Vietti R, Bavestrello G, Cerrano C, et al. Optical fibres in an Antarctic sponge. Nature, 1996, 383(6599): 397–398

    Article  ADS  CAS  Google Scholar 

  44. Aizenberg J, Sundar V C, Yablon A D, et al. Biological glass fibers: Correlation between optical and structural properties. Proceedings of the National Academy of Sciences of the United States of America, 2004, 101(10): 3358–3363

    Article  PubMed  ADS  CAS  Google Scholar 

  45. Müller W E G, Wendt K, Geppert C, et al. Novel photoreception system in sponges? Unique transmission properties of the stalk spicules from the hexactinellid Hyalonema sieboldi. Biosensors & Bioelectronics, 2006, 21(7): 1149–1155

    Article  CAS  Google Scholar 

  46. Murr M M, Morse D E. Fractal intermediates in the self-assembly of silicatein filaments. Proceedings of the National Academy of Sciences of the United States of America, 2005, 102(33): 11657–11662

    Article  PubMed  ADS  CAS  Google Scholar 

  47. Krasko A, Schröder H C, Batel R, et al. Iron induces proliferation and morphogenesis in primmorphs from the marine sponge Suberites domuncula. DNA and Cell Biology, 2002, 21(1):67–80

    Article  PubMed  CAS  Google Scholar 

  48. Schröder H C, Perovic-Ottstadt S, Wiens M, et al. Differentiation capacity of epithelial cells in the sponge Suberites domuncula. Cell and Tissue Research, 2004, 316(2): 271–280

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. National Research Center for Geoanalysis, 26 Baiwanzhuang Dajie, Beijing, 100037, China

    Xiao-hong Wang

  2. Laboratory of Guangzhou Marine Geological Surey, Guangzhou, 510760, China

    Xue-hua Zhang

  3. Institut für Physiologische Chemie, Abteilung Angewandte Molekularbiologie, Universität, Duesbergweg 6, D-55099, Mainz, Germany

    Heinz C. Schröder & Werner E. G. Müller

Authors
  1. Xiao-hong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xue-hua Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Heinz C. Schröder
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Werner E. G. Müller
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Xiao-hong Wang or Werner E. G. Müller.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, Xh., Zhang, Xh., Schröder, H.C. et al. Giant basal spicule from the deep-sea glass sponge Monorhaphis chuni: synthesis of the largest bio-silica structure on Earth by silicatein. Front. Mater. Sci. China 3, 226–240 (2009). https://doi.org/10.1007/s11706-009-0044-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11706-009-0044-x

Keywords

Search

Navigation