Advertisement

Coral Reefs

, Volume 24, Issue 1, pp 149–156 | Cite as

Antibodies against the organic matrix in scleractinians: a new tool to study coral biomineralization

  • Sandrine Puverel
  • Eric Tambutté
  • Didier Zoccola
  • Isabelle Domart-Coulon
  • André Bouchot
  • Séverine Lotto
  • Denis Allemand
  • Sylvie Tambutté
Report

Abstract

Soluble organic matrix (SOM) synthesis and secretion were investigated in two scleractinian corals using antibodies raised against this organic matrix. Results demonstrate that even if other cell types, including zooxanthellae, can supply precursors for SOM synthesis, only calicoblastic cells facing the skeleton are directly responsible for the synthesis and secretion of the SOM components. Results also indicate that, as is the case for other biominerals, skeleton formation is biologically controlled and not chemically dominated as originally believed. In addition to advancing the understanding of mechanisms of coral biomineralization, these antibodies could have numerous applications: for example as markers of skeletogenesis, as tools for cell culture, and in comparative studies among calcifying organisms.

Keywords

Biomineralization Calcification Coral skeleton Immunolabeling Organic matrix Coral cell culture 

Notes

Acknowledgements

We are grateful to Dominique Desgré for coral maintenance. We thank Professor Ramon Serrano from the University of Valencia for providing the membrane antibody. We thank Professor Jean-Pierre Cuif from the University of Orsay (Paris), Professor Patrick Payan from the University of Nice-Sophia Antipolis, Dr Lucilia Pereira-Mouriès and Dr Marshall Hayes for fruitful discussions and improvements to the manuscript. This study was conducted as part of the Centre Scientifique de Monaco 2000–2004 research program, supported by the Government of the Principality of Monaco.

References

  1. Allemand D, Zoccola D, Tambutté E (2000) Physiological mechanisms underlying biomineralization process in the scleractinian coral Stylophora pistillata. In: Goldberg M, Boskey A, Robinson C (eds) Proceedings of the 6th international conference on chemistry and biology of mineralized tissues, Vittel, pp 3–6Google Scholar
  2. Ameye L, Hermann R, Killian C, Wilt F, Dubois P (1999) Ultrastructural localization of proteins involved in sea urchin biomineralization. J Histochem Cytochem 47:1189–1200PubMedGoogle Scholar
  3. Arnaud E, De Pollak C, Meunier A, Sedel L, Damien C, Petite H (1999) Osteogenesis with coral is increased by BMP and BMC in a rat cranioplasty. Biomaterials 20(20):1909–1918CrossRefPubMedGoogle Scholar
  4. Barnes DJ, Chalker BE (1990) Calcification and photosynthesis in reef-building corals and algae. In: Dubinsky Z (ed) Coral reefs. Elsevier, Amsterdam, pp 109–131Google Scholar
  5. Bryan WH, Hill D (1941) Spherulitic crystallization as a mechanism of skeletal growth in the hexacorals. P Roy Soc Queensl 52:78–91Google Scholar
  6. Clode PL, Marshall AT (2003) Calcium associated with a fibrillar organic matrix in the scleractinian coral Galaxea fascicularis. Protoplasma 220:153–161CrossRefPubMedGoogle Scholar
  7. Constantz BR (1986) Coral skeleton construction: a physiochemically dominated process. Palaios 1:152–157Google Scholar
  8. Constantz B, Weiner S (1988) Acidic macromolecules associated with the mineral phase of scleractinian coral skeletons. J Exp Zool 248:253–258Google Scholar
  9. Cuif JP, Dauphin Y, Gautret P (1997) Biomineralization features in scleractinian coral skeletons: source of new taxonomic criteria. Boletin de la Real Sociedad Espanola de Historia natural (Seccion Geologica) 92:129–141Google Scholar
  10. Cuif JP, Dauphin Y, Freiwald A, Gautret P, Zibrowius H (1999) Biochemical markers of zooxanthellae symbiosis in soluble matrices of skeleton of 24 Scleractinia species. Comp Biochem Physiol 123A:269–278Google Scholar
  11. Dauphin Y (2001) Comparative studies of skeletal soluble matrices from some Scleractinian corals and Molluscs. Int J Biol Macromol 28:293–304CrossRefPubMedGoogle Scholar
  12. Demers C, Reggie Hamdy C, Corsi K, Chellat F, Tabrizian M, Yahia L (2002) Natural coral exoskeleton as a bone graft substitute: a review. Biomed Mater Eng 12:15–35PubMedGoogle Scholar
  13. Dewel RA (2000) Colonial origin for Eumetazoa: major morphological transitions and the origin of bilaterian complexity. J Morphol 243:35–74CrossRefPubMedGoogle Scholar
  14. Domart-Coulon IJ, Elbert DC, Scully EP, Calimlim PS, Ostrander GK (2001) Aragonite crystallization in primary cell cultures of multicellular isolates from a hard coral, Pocillopora damicornis. Proc Natl Acad Sci U S A 98:11885–11890CrossRefPubMedGoogle Scholar
  15. Domart-Coulon I, Tambutté S, Tambutté E, Allemand D (2004) Short term viability of soft tissue detached from the skeleton of reef-building corals. J Exp Mar Biol Ecol 309:199–217CrossRefGoogle Scholar
  16. Falini G, Albeck S, Weiner S, Addadi L (1996) Control of aragonite or calcite polymorphism by mollusk shell macromolecules. Science 271:67–69Google Scholar
  17. Field KG, Olsen GJ, Lane DJ, Giovannoni SJ, Ghiselin MT, Raff EC, Pace NR, Raff RA (1988) Molecular phylogeny of the animal kingdom. Science 239:748–753PubMedGoogle Scholar
  18. Frank U, Rabinowitz B, Rinkevich B (1994) In vitro establishment of continuous cell cultures and cell lines from ten colonial cnidarians. Mar Biol 120:491–499Google Scholar
  19. Freshney RI (1987) Culture of animal cells. A manual of basic technique, 2nd edn. Wiley-Liss Inc., New York, pp 1–6Google Scholar
  20. Fukuda I, Ooki S, Fujita T, Murayama E, Nagasawa H, Isa Y, Watanabe T (2003) Molecular cloning of a cDNA encoding a soluble protein in the coral exoskeleton. Biochem Biophys Res Commun 304:11–17CrossRefPubMedGoogle Scholar
  21. Gattuso JP, Allemand D, Frankignoulle M (1999) Photosynthesis and calcification at cellular, organismal and community levels in coral reefs: a review on interactions and control by carbonate chemistry. Amer Zool 39:160–183Google Scholar
  22. Gautret P, Marin F (1992) Evaluation of diagenesis in scleractinian corals and calcified desmosponges by substitution index measurement and intraskeletal organic matrix analysis. Courier Forschungs- institut Senckenberg 164:317–327Google Scholar
  23. Gautret P, Cuif JP, Freiwald A (1997) Composition of soluble mineralizing matrices in zooxanthellate and non-zooxanthellate scleractinian corals: biochemical assessment of photosynthetic metabolism through the study of a skeletal feature. Facies 36:189–194Google Scholar
  24. Gautret P, Cuif JP, Stolarski J (2000) Organic components of the skeleton of scleractinian corals—evidence from in situ acridine orange staining. Acta Palaeontol Pol 45:107–118Google Scholar
  25. Goldberg WM (2001) Acid polysaccharides in the skeletal matrix and calicoblastic epithelium of the stony coral Mycetophyllia reesi. Tissue Cell 33:376–387CrossRefPubMedGoogle Scholar
  26. Grobstein C (1965) Differentiation: environmental factors, chemical and cellular. In: Willmer EN (ed) Cells and tissues in culture. Methods, biology and physiology, vol 1. Academic, London, pp 463–488Google Scholar
  27. Johnston IS (1979) The organization of a structural organic matrix within the skeleton of a reef-building coral. Scanning Electron Microsc II:421–431Google Scholar
  28. Johnston IS (1980) The ultrastructure of skeletogenesis in zooxanthellate corals. Int Rev Cytol 67:171–214Google Scholar
  29. Kingsley RJ, Bernhardt AM, Wilbur KM, Watabe N (1987) Scleroblast cultures from the gorgonian Leptogorgia virgulata Lam. (coelenterata, gorgonacea). In Vitro Cell Dev Biol 23:297–302Google Scholar
  30. Kopecky EJ, Ostrander GK (1999) Isolation and primary culture of viable multicellular endothelial isolates from hard corals. In Vitro Cell Dev Biol Anim 35:616–624PubMedGoogle Scholar
  31. Kortschak RD, Samuel G, Saint R, Miller DJ (2003) EST analysis of the cnidarian Acropora millepora reveals extensive gene loss and rapid sequence divergence in the model invertebrates. Curr Biol 13:2190–2195PubMedGoogle Scholar
  32. Martindale MQ, Finnerty JR, Henry JQ (2002) The radiata and the evolutionary origins of the bilaterian body plan. Mol Phylogenet Evol 24:358–365CrossRefPubMedGoogle Scholar
  33. Mitterer RM (1978) Amino acid composition and metal binding capability of the skeleton proteins of corals. Bull Mar Sci 28:173–180Google Scholar
  34. Muscatine L, Cernichiari E (1969) Assimilation of photosynthetic products of zooxanthellae by a reef coral. Biol Bull 137:506–523Google Scholar
  35. Phillips JH (1961) Isolation and maintenance in tissue culture of coelenterate cell lines. In: Lenhoff HM, Loomis WF (eds) University of Miami Press, Coral Gables, pp 245–254 Google Scholar
  36. Poncet J, Serpentini A, Thiebot B, Villers C, Bocquet J, Boucaud-Camou E, Lebel J (2000) In vitro synthesis of proteoglycans and collagen in primary cultures of mantle cells from the nacreous mollusk, Haliotis tuberculata: a new model for study of molluscan extracellular matrix. Mar Biotechnol 2:387–398PubMedGoogle Scholar
  37. Reynaud-Vaganay S, Gattuso JP, Cuif JP, Jaubert J, Juillet-Leclerc A (1999) A novel culture technique for scleractinian corals: application to investigate changes in skeletal delta18O as a function of temperature. Mar Ecol Prog Ser 180:121–130Google Scholar
  38. Rinkevich B (1999) Cell cultures from marine invertebrates: obstacles, new approaches and recent improvements. J Biotechnol 70:133–153CrossRefGoogle Scholar
  39. Tambutté E, Allemand D, Bourge I, Gattuso JP, Jaubert J (1995) An improved 45Ca protocol for investigating physiological mechanisms in coral calcification. Mar Biol 122:453–459CrossRefGoogle Scholar
  40. Tambutté E, Allemand D, Mueller E, Jaubert J (1996) A compartmental approach to the mechanism of calcification in hermatypic corals. J Exp Biol 199:1029–1041PubMedGoogle Scholar
  41. Volpi N (2002) Influence of charge density, sulfate group position and molecular mass on adsorption of chondroitin sulfate onto coral. Biomaterials 23(14):3015–3022CrossRefPubMedGoogle Scholar
  42. Wainwright SA (1963) Skeletal organization in the coral Pocillopora damicornis. Q J Microsc Sci 104:169–183Google Scholar
  43. Weiner S (1984) Organization of organic matrix components in mineralized tissues. Amer Zool 24:945–951Google Scholar
  44. Wheeler AP, Sikes CS (1984) Regulation of carbonate calcification by organic matrix. Amer Zool 24:933–944Google Scholar
  45. Young SD (1971a) Organic matrices associated with CaCO3 skeletons of several species of hermatypic corals. In: Lenhoff HM, Muscatine L, Davis LV (eds) University Press of Hawaii, Honolulu, pp 260–264 Google Scholar
  46. Young SD (1971b) Organic material from scleractinian coral skeletons. I. Variation in composition between several species. Comp Biochem Physiol 40B:113–120Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Sandrine Puverel
    • 1
    • 2
  • Eric Tambutté
    • 1
  • Didier Zoccola
    • 1
  • Isabelle Domart-Coulon
    • 1
  • André Bouchot
    • 1
  • Séverine Lotto
    • 1
  • Denis Allemand
    • 1
    • 2
  • Sylvie Tambutté
    • 1
  1. 1.Centre Scientifique de Monacoav. St MartinMonaco
  2. 2.Faculté des sciencesUMR 1112 UNSA-INRANice cedex 2France

Personalised recommendations