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

Xiao-hong WANG, Xue-hua ZHANG, Heinz C. SCHRÖDER, Werner E. G. MÜLLER

PDF(1021 KB)
PDF(1021 KB)
Front. Mater. Sci. ›› 2009, Vol. 3 ›› Issue (3) : 226-240. DOI: 10.1007/s11706-009-0044-x
RESEARCH ARTICLE
RESEARCH ARTICLE

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

Author information +
History +

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.

Keywords

sponge / Porifera / Hexactinellida / spicule / giant basal spicule / silicatein / biomaterial science

Cite this article

Download citation ▾
Xiao-hong WANG, Xue-hua ZHANG, Heinz C. SCHRÖDER, Werner E. G. MÜLLER. 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 Chin, 2009, 3(3): 226‒240 https://doi.org/10.1007/s11706-009-0044-x

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
[2]
Kruse M, Leys S P, Müller I M, . 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
[3]
Müller W E G, Wiens M, Adell T, , 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
[4]
Müller W E G, Li J H, Schröder H C, . 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
[5]
Pilcher H. Animal magnetism. Nature, 2005, 435(7045): 1022–1023
[6]
Murray J, Hjort J. The Depths of the Ocean. London: MacMillan, 1912
[7]
Schulze F E.Hexactinellida. Wissenschaftliche Ergebnisse der Deutschen Tiefsee-Expedition auf dem Dampfer “Valdivia” 1898–1899. Stuttgart: Gustav Fischer Verlag, 1904
[8]
Roux M, Bouchet P, Bourseau J P, . 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
[9]
Müller W E G, Eckert C, Kropf K, . 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
[10]
Li J. Monorhaphis intermedia-a new species of Hexactinellida. Oceanologia et Limnologia Sinica, 1987, 18: 135–137
[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
[12]
Wang X H, Li J H, Qiao L, . 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
[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
[14]
Uriz M J, Turon X, Becerro M A, . Siliceous spicules and skeleton frameworks in sponges: Origin, diversity, ultrastructural patterns, and biological functions. Microscopy Research and Technique, 2003, 62(4): 279–299
[15]
Uriz M J. Mineral spiculogenesis in sponges. Canadian Journal of Zoology, 2006, 84: 322–356
[16]
Müller W E G, Jochum K P, Stoll B, . Formation of giant spicule from quartz glass by the deep sea sponge Monorhaphis. Chemistry of Materials, 2008, 20(14): 4703–4711
[17]
Müller W E G, Wang X H, Kropf K, . 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
[18]
Levi C, Barton J L, Guillemet C, . A remarkably strong natural glassy rod — the anchoring spicule of the Monorhaphis sponge. Journal of Materials Science Letters, 1989, 8(3): 337–339
[19]
Müller W E G, Boreiko A, Schlossmacher U, . 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
[20]
Müller W E G, Boreiko A, Wang X H, . Silicateins, the major biosilica forming enzymes present in demosponges: Protein analysis and phylogenetic relationship. Gene, 2007, 395(1–2): 62–71
[21]
Müller W E G, Rothenberger M, Boreiko A, . Formation of siliceous spicules in the marine demosponge Suberites domuncula. Cell and Tissue Research, 2005, 321(2): 285–297
[22]
Müller W E G, Boreiko A, Schlossmacher U, . 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
[23]
Müller W E G, Schlossacher U, Wang X, . 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
[24]
Wang X H, Schloβmacher U, Jochum K P, . 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, . Silicatein alpha: Cathepsin L-like protein in sponge biosilica. Proceedings of the National Academy of Sciences of the United States of America, 1998, 95(11): 6234–6238
[27]
Cha J N, Shimizu K, Zhou Y, . 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
[28]
Krasko A, Lorenz B, Batel R, . 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
[29]
Müller W E G, Wang X H, Kropf K, . Silicatein expression in the hexactinellid Crateromorpha meyeri: the lead marker gene restricted to siliceous sponges. Cell and Tissue Research, 2008, 333(2): 339–351
[30]
Müller W E, Krasko A, Le Pennec G, . Molecular mechanism of spicule formation in the demosponge Suberites domuncula: silicatein-collagen-myotrophin. Progress in Molecular and Subcellular Biology, 2003, 33: 195–221
[31]
Wiens M, Belikov S I, Kaluzhnaya O V, . 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
[32]
Müller W E G, Boreiko A, Schlossmacher U, . 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
[33]
Ramachandran G N, Ramakrishnan C, Sasisekharan V. Stereochemistry of polypeptide chain configurations. Journal of Molecular Biology, 1963, 7(1): 95–99
[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
[36]
Mayer G, Trejo R, Lara-Curzio E, . 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
[37]
Perovic S, Krasko A, Prokic I, . 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
[38]
Chevreux B, Pfisterer T, Drescher B, . Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Research, 2004, 14(6): 1147–1159
[39]
Pavans de Ceccatty M. Coordination in sponges — foundations of integration. American Zoologist, 1974, 14(3): 895–903
[40]
Mackie G O. Is there a conduction system in sponges? Colloq Int Centre Natl Res Sci, 1979, 291: 145–151
[41]
Leys S P, Degnan B M. Cytological basis of photoresponsive behavior in a sponge larva. Biological Bulletin, 2001, 201(3): 323–338
[42]
Leys S P, Cronin T W, Degnan B M, . Spectral sensitivity in a sponge larva. Journal of Comparative Physiology A — Neuroethology Sensory Neural and Behavioral Physiology, 2002, 188(3): 199–202
[43]
Cattaneo-Vietti R, Bavestrello G, Cerrano C, . Optical fibres in an Antarctic sponge. Nature, 1996, 383(6599): 397–398
[44]
Aizenberg J, Sundar V C, Yablon A D, . 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
[45]
Müller W E G, Wendt K, Geppert C, . Novel photoreception system in sponges? Unique transmission properties of the stalk spicules from the hexactinellid Hyalonema sieboldi. Biosensors & Bioelectronics, 2006, 21(7): 1149–1155
[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
[47]
Krasko A, Schröder H C, Batel R, . Iron induces proliferation and morphogenesis in primmorphs from the marine sponge Suberites domuncula. DNA and Cell Biology, 2002, 21(1): 67–80
[48]
Schröder H C, Perovic-Ottstadt S, Wiens M, . Differentiation capacity of epithelial cells in the sponge Suberites domuncula. Cell and Tissue Research, 2004, 316(2): 271–280

Acknowledgements

We thank the Marine Biological Museum of Institute of Oceanography, Chinese Academy of Sciences (Qingdao, China) for providing us with the Monorhaphis spicules for our research. This work was supported by grants from the Bundesministerium für Bildung und Forschung Germany (Project “Center of Excellence BIOTECmarin”), the International Human Frontier Science Program, the European Commission, the International S & T Cooperation Program of China (Grant No. 2008DFA00980), the Basic Scientific Research Program in China (Grant No. 200607CSJ-05) and the National Natural Science Foundation of China (Grant No. 50402023).

RIGHTS & PERMISSIONS

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg
AI Summary AI Mindmap
PDF(1021 KB)

Accesses

Citations

Detail

Sections
Recommended

/