Skip to main content
SpringerLink
Log in

On the ultrastructure and the supposed function of the mineralizing matrix coat of sea urchins (Echinodermata, Echinoida)

  • Published:
Zoomorphology Aims and scope Submit manuscript

Summary

Echinoderm ossicles are part of the mesenchyme. Their formation and growth, with respect to the underlying tissues, is studied using echinoid spines and teeth and applying different methods of fixation. The calcification process in echinoderms is strictly intracellular and needs (1) syncytial sclerocytes which completely enclose (2) a vacuolar cavity which in turn contains (3) an organic matrix coat. Strictly speaking, each ossicle is nothing but the calcified vacuolar space of a single syncytium of sclerocytes. In fully grown parts, however, the continuous sheath may split open and the matrix-coated mineral may come into contact with the extracellular space. According to biochemical analyses the matrix consists of insoluble components, but most (95%) of its constituents are soluble in EDTA or weak acids. If routine transmission electron microscope methods are used the soluble components are lost and the matrix at best looks electron light. If tannic acid is added to the fixative the soluble matrix components are preserved and reveal further ultrastructural details of the biomineralization process in echinoderms. The matrix coat looks extremely electron dense. Further soluble material is to be found within the vacuolar space or attached to the vacuolar surface of the cytoplasmic sheath. The results lead to the opinion that the matrix coat consists of a hydrophobic framework of insoluble components that contains soluble components which guide the Ca through pores in the hydrophobic layers into the interior of the matrix-coated space. It is only within this space that the mineral is deposited.

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

  • Behnke O, Zelander T (1970) Preservation of intercellular substances by the cationic dye alcian blue in preparative procedures for electron microscopy. J Ultrastruct Res 31:424–438

    Google Scholar 

  • Benson S, Jones EME, Crise-Benson N, Wilt F (1983) Morphology of the organic matrix of the spicule of the sea urchin larva. Exp Cell Res 148:249–253

    Google Scholar 

  • Benson SC, Crise-Benson N, Wilt F (1986) The organic matrix of the skeletal spicule of sea urchin embryos. J Cell Biol 102:1878–1886

    Google Scholar 

  • Chen CP, Lawrence JM (1986) Localization of carbonic anhydrase in the plumula of the tooth of Lytechinus variegatus (Echinodermata: Echinoidea). Acta Zool 67 (1):27–32

    Google Scholar 

  • Futaesaku Y, Mizuhira V, Nakamura H (1972) A new fixation method using tannic acid for electron microscopy and some observations of biological specimens. Proc Int Congr Histochem Cytochem 4:155–156

    Google Scholar 

  • Gibbins JR, Tilney LG, Porter KR (1969) Microtubules in the formation and development of the primary mesenchyme in Arbacia punctulata. I. The distribution of microtubules. J Cell Biol 41:201–226

    Google Scholar 

  • Goldberg WM, Benayahu Y (1987) Spicule formation in the gorgonian coral Pseudoplexaura flagellosa. 2: Calcium localization by antimonate precipitation. Bull Mar Sci 40:304–310

    Google Scholar 

  • Goldberg WM (1988) Chemistry, histochemistry and microscopy of the organic matrix of spicules from a gorgonian coral. Relationship to alcian blue staining and calcium binding. Histochemistry 89:163–170

    Google Scholar 

  • Heatfield BM (1971) Origin of calcified tissue in regenerating spines of the sea urchin, Strongylocentrotus purpuratus (Stimpson): A quantitative radioautographic study with tritiated thymidine. J Exp Zool 178:233–246

    Google Scholar 

  • Heatfield BM, Travis DF (1975) Ultrastructural studies of regenerating spines of the sea urchin Strongylocentrotus purpuratus. I. Cell types without spherules. J Morphol 145:13–27 pls 1–11

    Google Scholar 

  • Karnovsky MJ (1971) Use of ferrocyanide-reduced osmium tetroxide in electron microscopy. Abstracts of the Am Soc of Cell Biol. Rockefeller University Press, New York, New Orleans, p 146

    Google Scholar 

  • Kniprath E (1974) Ultrastructure and growth of the sea urchin tooth. Calcif Tiss Res 14:211–228

    Google Scholar 

  • Krampitz G, Drolshagen H, Häusle J, Hof-Irmscher K (1983) Organic matrices of mollusc shells. In: Westbroek P, de Jong FW (eds) Biomineralization and biological metal accumulation. Reidel Publishing Company, Dordrecht, pp 231–247

    Google Scholar 

  • Luft JH (1971a) Ruthenium red and violet. I. Chemistry, purification, methods of use for electron microscopy and mechanisms of action. Anat Rec 171:347–368

    Google Scholar 

  • Luft JH (1971b) Ruthenium red and violet. II. Fine structural localization in animal tissue. Anat Rec 171:369–416

    Google Scholar 

  • Märkel K, Titschack H (1969) Morphologie der Seeigelzähne. I. Der Zahn von Stylocidaris affinis. Z Morphol Tiere 64:179–200

    Google Scholar 

  • Märkel K, Gorny P, Abraham K (1977) Microarchitecture of sea urchin teeth. Fortschr Zool 24:103–114

    Google Scholar 

  • Märkel K, Röser U (1983a) The spine tissues in the echinoid Eucidaris tribuloides. Zoomorphology 103:25–41

    Google Scholar 

  • Märkel K, Röser U (1983b) Calcite resorption in the spine of the echinoid Eucidaris tribuloides. Zoomorphology 103:43–58

    Google Scholar 

  • Märkel K, Röser U (1985) Comparative morphology of echinoderm calcified tissues: Histology and ultrastructure of ophiuroid scales. Zoomorphology 105:197–207

    Google Scholar 

  • Märkel K, Röser U, Mackenstedt U, Klostermann M (1986) Ultrastructural investigation of matrix-mediated biomineralization in echinoids (Echinodermata, Echinoida). Zoomorphology 106:232–243

    Google Scholar 

  • Merker E (1916) Studien am Skelet der Echinodermen. Zool Jahrb Abt Allg Zool Physiol Tiere 36:25–205

    Google Scholar 

  • Millonig G (1970) A study on the formation and structure of the sea urchin spicule. J Submicrosc Cytol 2:157–165

    Google Scholar 

  • Okazaki K (1975) Spicule formation by isolated micromeres of the sea urchin embryo. Am Zool 15:567–581

    Google Scholar 

  • Okazaki K, Inoué S (1976) Crystal property of the larval sea urchin spicule. Dev Growth Differ 18:413–434

    Google Scholar 

  • Prouho H (1887) Recherches sur le Dorocidaris papillata et quelques autres echinides de la mediterrannee. Arch Zool Exp Gen 5, Ser 2:213–380

    Google Scholar 

  • Ruggeri A, Dell'Orbo C, Quacci D (1975) Electron microscopic visualization of proteoglycans with alcian blue. Histochem J 7:187–197

    Google Scholar 

  • Scott JE, Quintarelli G, Dellovo M (1964) The chemical and histochemical properties of alcian blue. I. The mechanism of alcian blue staining. Histochemie 4:73–85

    Google Scholar 

  • Simionescu N, Simionescu M (1975) Digallic acid as mordant in electron microscopy. J Cell Biol 67 (2, Pt. 2): 401a (Abstr.)

  • Simionescu N, Simionescu M (1976a) Gallolylglucoses of low molecular weight as mordant in electron microscopy. I. Procedure, and evidence for mordanting effect. J Cell Biol 70:608–621

    Google Scholar 

  • Simionescu N, Simionescu M (1976b) Gallolylglucoses of low molecular weight as mordant in electron microscopy. II. The moiety and functional groups possibly evolved in mordanting effect. J Cell Biol 70:622–633

    Google Scholar 

  • Slocum RD, Roux SJ, (1982) An improved method for the subcellular localization of calcium using a modification of the antimonate precipitation technique. J Histochem Cytochem 30:617–629

    Google Scholar 

  • Stricker SA (1985) The ultrastructure and formation of the calcareous ossicles in the body wall of the sea cucumber Leptosynapta clarki. Zoomorphology 105:209–222

    Google Scholar 

  • Swift DM, Sikes CS, Wheeler AP (1986) Analysis and function of organic matrix from sea urchin tests. J Exp Zool 240:65–73

    Google Scholar 

  • Thyberg CJO (1984) Electron microscopy of proteoglycans. In: Ruggeri A, Motta PM (eds) Ultrastructure of the connective tissue matrix. Martinus Nijhoff Publishers, Boston, pp 95–112

    Google Scholar 

  • Veis DJ, Albinger TM, Clohisy J, Rahima M, Sabsay B, Veis A (1986) Matrix proteins of the teeth of the sea urchin Lytechinus variegatus. J Exp Zool 240:35–46

    Google Scholar 

  • Wagner RC (1976) The effect of tannic acid on electron images of capillary endothelial cell membranes. J Ultrastruct Res 57:132–139

    Google Scholar 

  • Weiner S, Traub W, Lowenstam HA (1983) Organic matrix in calcified exoskeletons. In: Westbroek P, de Jong EW (eds) Biomineralization and biological metal accumulation. Reidel Publishing Company, Dordrecht, pp 205–224

    Google Scholar 

  • Weiner S (1984) Organization of organic matrix components in mineralized tissue. Am Zool 24:945–951

    Google Scholar 

  • Weiner S, Traub W (1984) Macromolecules in mollusc shells and their functions in biomineralization. Philos Trans R Soc London Ser B 304:425–434

    Google Scholar 

  • Weiner S (1985) Organic matrixlike macromolecules associated with the mineral phase of sea urchin skeletal plates and teeth. J Exp Zool 234:7–15

    Google Scholar 

  • Wheeler AP, Sikes CS (1984) Regulation of carbonate calcification by organic matrix. Am Zool 24:933–944

    Google Scholar 

  • Wheeler AP, Rusenko KW, Swift DM, Sikes CS (1988) Regulation of in vitro and in vivo CaCO3 crystallization by fractions of oyster shell organic matrix. Mar Biol 98:71–80

    Google Scholar 

  • Wilbur KM, Simkiss K (1979) Carbonate turnover and deposition by metazoa. In: Trudinger PA, Swaine DJ (eds) Biogeochemical cycling of mineral-forming elements. Elsevier, Amsterdam, pp 69–106

    Google Scholar 

  • Wilbur KM, Saleuddin ASM (1983) Shell formation. In: Saleuddin ASM, Wilbur KM (eds) The Mollusca. Academic Press, New York, pp 235–287

    Google Scholar 

  • Wilbur KM (1984) Many minerals, several phyla, and a few considerations. Am Zool 24:839–845

    Google Scholar 

  • Wilbur KM, Bernhardt AM (1984) Effects of amino acids, magnesium, and molluscan extrapallial fluid on crystallization of calcium carbonate: In vitro experiments. Biol Bull 166:251–259

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Lehrstuhl für Spezielle Zoologie und Parasitologie (Arbeitsgruppe Funktionelle Morphologie), Ruhr-Universität Bochum, D-4630, Bochum 1, Federal Republic of Germany

    Konrad Märkel, Ursula Röser & Michael Stauber

Authors
  1. Konrad Märkel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ursula Röser
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michael Stauber
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Märkel, K., Röser, U. & Stauber, M. On the ultrastructure and the supposed function of the mineralizing matrix coat of sea urchins (Echinodermata, Echinoida). Zoomorphology 109, 79–87 (1989). https://doi.org/10.1007/BF00312313

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00312313

Keywords

Search

Navigation