Studies on molluscan shells: contributions from microscopic and analytical methods.

Molluscan shells have always attracted the interest of researchers, from biologists to physicists, from paleontologists to materials scientists. Much information is available at present, on the elaborate architecture of the shell, regarding the various Mollusc classes. The crystallographic characterization of the different shell layers, as well as their physical and chemical properties have been the subject of several investigations. In addition, many researches have addressed the characterization of the biological component of the shell and the role it plays in the hard exoskeleton assembly, that is, the biomineralization process. All these topics have seen great advances in the last two or three decades, expanding our knowledge on the shell properties, in terms of structure, functions and composition. This involved the use of a range of specialized and modern techniques, integrating microscopic methods with biochemistry, molecular biology procedures and spectroscopy. However, the factors governing synthesis of a specific crystalline carbonate phase in any particular layer of the shell and the interplay between organic and inorganic components during the biomineral assembly are still not widely known. This present survey deals with microstructural aspects of molluscan shells, as disclosed through use of scanning electron microscopy and related analytical methods (microanalysis, X-ray diffraction, electron diffraction and infrared spectroscopy). These already published data provide relevant information on shells and also contribute for better understanding the biomineralization process.

[1]  H. Liao,et al.  Tissue responses to natural aragonite (Margaritifera shell) implants in vivo. , 2000, Biomaterials.

[2]  R. Dreele Multipattern Rietveld refinement of protein powder data: an approach to higher resolution , 2006 .

[3]  H. Ozawa,et al.  Organic components of crystal sheaths in bones. , 2001, Journal of electron microscopy.

[4]  A. Howie,et al.  Electron Microscopy of Thin Crystals , 1977, Nature.

[5]  Marc A. Meyers,et al.  Growth and structure in abalone shell , 2005 .

[6]  Edmund Buerlein Handbook of Biomineralization , 2007 .

[7]  J. Marxen,et al.  Carbohydrates of the Organic Shell Matrix and the Shell-Forming Tissue of the Snail Biomphalaria glabrata (Say). , 1998, The Biological bulletin.

[8]  H. Nakahara,et al.  An electron microscope study of the formation of the periostracum of Macrocallista maculata. , 1967, Calcified tissue research.

[9]  A. W. Martin,et al.  Shell repair in Nautilus macromphalus , 1974 .

[10]  Y. Dauphin,et al.  Lipids from the nacreous and prismatic layers of two Pteriomorpha mollusc shells. , 2009, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[11]  O. Delattre,et al.  Use of mother of pearl as a bone substitute - Experimental study in sheep , 1997, European Journal of Orthopaedic Surgery & Traumatology.

[12]  D. Rhoads,et al.  Skeletal Growth of Aquatic Organisms , 1980 .

[13]  S. Valiyaveettil,et al.  CaCO3 biomineralization: acidic 8-kDa proteins isolated from aragonitic abalone shell nacre can specifically modify calcite crystal morphology. , 2005, Biomacromolecules.

[14]  K. Simkiss 14 – Molluscs—Epithelial Control of Matrix and Minerals , 1989 .

[15]  A. Wierzbicki,et al.  Oyster Shell Protein and Atomic Force Microscopy of Oyster Shell Folia. , 1998, The Biological bulletin.

[16]  M. Silveira,et al.  Microstructural characacterization of shell components in the mollusc Physa sp. , 2006, Scanning.

[17]  M. Mansur,et al.  Ultrastructural analysis of the shells of Anodontites trapesialis (Lamarck) and Anodontites elongatus (Swaison) (Mollusca, Bivalvia, Etherioidea) from the Mato Grosso Pantanal Region, Brazil , 2005 .

[18]  Sebastian Doniach,et al.  Synchrotron radiation research , 1981 .

[19]  M. José-Yacamán,et al.  Crystal structure characterization of nautilus shell at different length scales. , 2006, Biomaterials.

[20]  J. Susini,et al.  In situ chemical speciation of sulfur in calcitic biominerals and the simple prism concept. , 2003, Journal of structural biology.

[21]  J. Susini,et al.  Structure and composition of the nacre–prisms transition in the shell of Pinctada margaritifera (Mollusca, Bivalvia) , 2008, Analytical and bioanalytical chemistry.

[22]  P. D. Reynolds The Scaphopoda. , 2002, Advances in marine biology.

[23]  H David Sheets,et al.  Comparison of geometric morphometric outline methods in the discrimination of age-related differences in feather shape , 2006, Frontiers in Zoology.

[24]  J. G. Carter Skeletal biomineralization : patterns, processes, and evolutionary trends , 1991 .

[25]  S. Weiner,et al.  X‐ray diffraction study of the insoluble organic matrix of mollusk shells , 1980 .

[26]  Y. Dauphin Structure and composition of the septal nacreous layer of Nautilus macromphalus L. (Mollusca, Cephalopoda). , 2006, Zoology.

[27]  S. Weiner,et al.  Lamellar bone: structure-function relations. , 1999, Journal of structural biology.

[28]  Steve Weiner,et al.  Mollusk shell formation: mapping the distribution of organic matrix components underlying a single aragonitic tablet in nacre. , 2006, Journal of structural biology.

[29]  S. Popović,et al.  X-ray diffraction study of calcification processes in embryos and larvae of the brooding oyster Ostrea edulis , 1997 .

[30]  N. Watabe Dahllite Identified as a Constituent of Prodissoconch I of Pinctada martensii (Dunker) , 1956, Science.

[31]  C. Grégoire STRUCTURE OF THE CONCHIOLIN CASES OF THE PRISMS IN MYTILUS EDULIS LINNE , 1961, The Journal of biophysical and biochemical cytology.

[32]  J. Marxen,et al.  The Organic Shell Matrix of the Freshwater Snail Biomphalaria glabrata , 1997 .

[33]  W. K. Emerson A classification of the scaphopod mullusks , 1962 .

[34]  R. Asaro,et al.  Macromolecular structure of the organic framework of nacre in Haliotis rufescens: implications for growth and mechanical behavior. , 2008, Journal of structural biology.

[35]  M. Epple,et al.  Calcium carbonate modifications in the mineralized shell of the freshwater snail Biomphalaria glabrata. , 2000, Chemistry.

[36]  A. Veis Mineralization in Organic Matrix Frameworks , 2003 .

[37]  B. Runnegar Crystallography of the foliated calcite shell layers of bivalve molluscs , 1984 .

[38]  Xavier Bourrat,et al.  Multiscale structure of sheet nacre. , 2005, Biomaterials.

[39]  P. Hansma,et al.  Inorganic Overgrowth of Aragonite on Molluscan Nacre Examined by Atomic Force Microscopy. , 1995, The Biological bulletin.

[40]  A. Bubel An electron-microscope study of periostracum formation in some marine bivalves. I. The origin of the periostracum , 1973, Marine Biology.

[41]  F. Marin,et al.  Unusually Acidic Proteins in Biomineralization , 2008 .

[42]  Hans-Rudolf Wenk,et al.  Combined texture and structure analysis of deformed limestone from time-of-flight neutron diffraction spectra , 1997 .

[43]  E. R. Trueman The Structure, Development, and Operation of the Hinge Ligament of Ostrea edulis , 1951 .

[44]  J. Pais de Barros,et al.  The shell matrix of the freshwater mussel Unio pictorum (Paleoheterodonta, Unionoida) , 2007, The FEBS journal.

[45]  Lei Jiang,et al.  Morphology and crystalline characterization of abalone shell and mimetic mineralization , 2003 .

[46]  N. Watabe Crystal growth of calcium carbonate in the invertebrates , 1981 .

[47]  K. Wilbur CHAPTER 8 – Shell Formation and Regeneration , 1964 .

[48]  M. Marsh,et al.  Aragonite Twinning in the Molluscan Bivalve Hinge Ligament , 1980, Science.

[49]  Brian H. Toby,et al.  EXPGUI, a graphical user interface for GSAS , 2001 .

[50]  Joanna Aizenberg,et al.  Interactions of various skeletal intracrystalline components with calcite crystals , 1993 .

[51]  H. Rietveld A profile refinement method for nuclear and magnetic structures , 1969 .

[52]  J. Bereiter-Hahn,et al.  Biology of the Integument , 1984, Springer Berlin Heidelberg.

[53]  J. Currey 8 – Shell Form and Strength , 1988 .

[54]  H. Nakahara,et al.  An electron microscope study of the formation and structure of the periostracum of a gastropod,Littorina littorea , 2005, Calcified Tissue Research.

[55]  F. Marin,et al.  Molluscan biomineralization: The proteinaceous shell constituents of Pinna nobilis L. , 2005 .

[56]  M. Farina,et al.  Microstructure of Monoplacophora (Mollusca) shell examined by low-voltage field emission scanning electron and atomic force microscopy. , 2006, Scanning.

[57]  P. Reynolds The phylogeny and classification of Scaphopoda (Mollusca): an assessment of current resolution and cladistic reanalysis , 1997 .

[58]  H. Liao,et al.  Tissue responses to nacreous implants in rat femur: an in situ hybridization and histochemical study. , 2002, Biomaterials.

[59]  E. R. Trueman Observations on the ligament of Mytilus edulis. , 1950, The Quarterly journal of microscopical science.

[60]  S. Mann Mineralization in biological systems , 1983 .

[61]  Luc Ortlieb,et al.  Microstructure, nanostructure and composition of the shell of Concholepas concholepas (Gastropoda, Muricidae) , 2003 .

[62]  J. Currey The design of mineralised hard tissues for their mechanical functions. , 1999, The Journal of experimental biology.

[63]  T. Okamoto,et al.  Organization pattern of nacre in Pteriidae (Bivalvia: Mollusca) explained by crystal competition , 2006, Proceedings of the Royal Society B: Biological Sciences.

[64]  A. Saleuddin,et al.  The Mode of Formation and the Structure of the Periostracum , 1983 .

[65]  Michael B. Cortie,et al.  Fracture mechanics of mollusc shells , 2006 .

[66]  T. Samata,et al.  Bivalve shell structure and organic matrix , 2006 .

[67]  Jiming Hu,et al.  Meretrix lusoria--a natural biocomposite material: in situ analysis of hierarchical fabrication and micro-hardness. , 2006, Micron.

[68]  F. Cui,et al.  Crystallographic alignment of calcite prisms in the oblique prismatic layer of Mytilus edulis shell , 2000 .

[69]  Young Ha Kim,et al.  Effects of organic matrix proteins on the interfacial structure at the bone-biocompatible nacre interface in vitro. , 2002, Biomaterials.

[70]  E. Vieira,et al.  Amyloid–β-Sheet Formation at the Air-Water Interface , 1999 .

[71]  H. Toraya Crystal structure refinement of α‐Si3N4 using synchrotron radiation powder diffraction data: unbiased refinement strategy , 2000 .

[72]  L. Bédouet,et al.  The in vitro osteoclastic degradation of nacre. , 2007, Biomaterials.

[73]  Steve Weiner,et al.  Mollusk Shell Formation: A Source of New Concepts for Understanding Biomineralization Processes , 2006 .

[74]  Regine Herbst-Irmer,et al.  Crystal Structure Refinement , 2006 .

[75]  A. Checa A new model for periostracum and shell formation in Unionidae (Bivalvia, Mollusca). , 2000, Tissue & cell.

[76]  H. Nakahara,et al.  An electron microscope study of the formation of the ligament ofMytilus edulis andPinctada radiata , 2005, Calcified Tissue Research.

[77]  P. Grégoire SUR LA STRUCTURE DES MATRICES ORGANIQUES DES COQUILLES DE MOLLUSQUES , 1967 .

[78]  C. Yonge,et al.  Physiology of Mollusca , 1964 .

[79]  D. Medaković Carbonic anhydrase activity and biomineralization process in embryos, larvae and adult blue mussels Mytilus edulis L. , 2000, Helgoland Marine Research.

[80]  Daniel Chateigner,et al.  Mollusc shell microstructures and crystallographic textures , 2000 .

[81]  A. Saleuddin,et al.  Cellular mechanisms of periostracum formation in Physa spp. (Mollusca: Pulmonata) , 1978 .

[82]  S. Weiner,et al.  Control and Design Principles in Biological Mineralization , 1992 .

[83]  I. Weiss,et al.  The distribution of chitin in larval shells of the bivalve mollusk Mytilus galloprovincialis. , 2006, Journal of structural biology.

[84]  Rongqing Zhang,et al.  Matrix Proteins in the Outer Shells of Molluscs , 2006, Marine Biotechnology.

[85]  P. E. Hare,et al.  Amino acid compositions of normal and regenerated shell of Helix , 1970 .

[86]  M. Lamghari,et al.  Conservation of signal molecules involved in biomineralisation control in calcifying matrices of bone and shell , 2004 .

[87]  The protonephridial system of the tusk shell, Antalis entalis (Mollusca, Scaphopoda) , 2001, Zoomorphology.

[88]  J. Quintana,et al.  Anisotropic lattice distortions in the mollusk-made aragonite: a widespread phenomenon. , 2006, Journal of structural biology.

[89]  J. G. Carter,et al.  Environmental and biological controls of bivalve shell mineralogy and microstructure , 1980 .

[90]  Stephen Mann,et al.  Flat pearls from biofabrication of organized composites on inorganic substrates , 1994, Nature.

[91]  C. Grégoire Further studies on structure of the organic components in mother-of-pearl, especially in pelecypods. Part 1 , 1960 .

[92]  Y. Dauphin Soluble Organic Matrices of the Calcitic Prismatic Shell Layers of Two Pteriomorphid Bivalves , 2003, The Journal of Biological Chemistry.

[93]  M. Barthélémy,et al.  Soluble silk-like organic matrix in the nacreous layer of the bivalve Pinctada maxima. , 2002, European journal of biochemistry.

[94]  Gang-sheng Zhang,et al.  Photonic crystal type structure in bivalve ligament of Pinctada maxima , 2007 .

[95]  A K Soh,et al.  Structural and mechanical properties of the organic matrix layers of nacre. , 2003, Biomaterials.

[96]  S. Weiner,et al.  On how proteins interact with crystals and their effect on crystal formation , 2001, Zeitschrift für Kardiologie.

[97]  Z. Jiang,et al.  Infrared Spectroscopy , 2022 .

[98]  T. Tan,et al.  Iridescence of a shell of mollusk Haliotis Glabra. , 2004, Optics express.

[99]  O. Bøggild The shell structure of the Mollusks , 1930 .

[100]  N. Watabe,et al.  STUDIES ON SHELL FORMATION , 1961, The Journal of biophysical and biochemical cytology.

[101]  R. Glauber,et al.  The Theory of Electron Diffraction , 1953 .

[102]  A. Rodríguez-Navarro,et al.  The nature and formation of calcitic columnar prismatic shell layers in pteriomorphian bivalves. , 2005, Biomaterials.

[103]  N. Watabe,et al.  EXPERIMENTAL STUDIES ON CALCIFICATION IN MOLLUSCS AND THE ALGA COCCOLITHUS HUXLEYI , 1963, Annals of the New York Academy of Sciences.

[104]  S. Wise,et al.  NOTES ON THE MICROSTRUCTURE OF THE NAUTILUS SHELL. DISCUSSION , 1995 .

[105]  S. Weiner,et al.  Chitin-Silk Fibroin Interactions: Relevance to Calcium Carbonate Formation in Invertebrates , 2003, Calcified Tissue International.

[106]  Y. Dauphin Infrared Spectra and Elemental Composition in Recent Biogenic Calcites: Relationships between the ν4 Band Wavelength and Sr and Mg Concentrations , 1999 .

[107]  David L. Kaplan,et al.  Mollusc shell structures: novel design strategies for synthetic materials , 1998 .

[108]  J. Wishart,et al.  The effect of an oral calcium load on plasma ionized calcium and parathyroid hormone concentrations in osteoporotic postmenopausal women , 1987, Calcified Tissue International.

[109]  Q. Feng,et al.  Crystal orientation preference and formation mechanism of nacreous layer in mussel , 2003 .

[110]  Jiming Hu,et al.  In situ analysis of the organic framework in the prismatic layer of mollusc shell. , 2002, Biomaterials.

[111]  Patricia M. Dove,et al.  An Overview of Biomineralization Processes and the Problem of the Vital Effect , 2003 .

[112]  Frédéric Marin,et al.  A marriage of bone and nacre , 1998, Nature.

[113]  T. Sterry Hunt International Geological Congress , 1876 .

[114]  Y. Dauphin,et al.  Structure and composition of the aragonitic crossed lamellar layers in six species of Bivalvia and Gastropoda. , 2000, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[115]  Karl M. Wilbur,et al.  The chemical composition of the periostracum of the molluscan shell , 1969 .

[116]  R. Dreele Combined Rietveld and stereochemical restraint refinement of a protein crystal structure , 1999 .

[117]  S. Weiner,et al.  Design strategies in mineralized biological materials , 1997 .

[118]  E. DiMasi,et al.  Synchrotron x-ray microbeam diffraction from abalone shell , 2004 .

[119]  O. Delattre,et al.  Nacre/bone interface changes in durable nacre endosseous implants in sheep. , 2005, Biomaterials.

[120]  J. Cartwright,et al.  The dynamics of nacre self-assembly , 2007, Journal of The Royal Society Interface.

[121]  B. Hannoyer,et al.  Fourier transform infrared spectroscopy (FTIR) and X-ray diffraction analyses of mineral and organic matrix during heating of mother of pearl (nacre) from the shell of the mollusc Pinctada maxima. , 1999, Journal of biomedical materials research.

[122]  B. Warren,et al.  X-Ray Diffraction , 2014 .

[123]  C. Palmer A SUPRASPECIFIC CLASSIFICATION OF THE SCAPHOPOD MOLLUSCA , 1974 .

[124]  S. Berland,et al.  Bioactivity of nacre water-soluble organic matrix from the bivalve mollusk Pinctada maxima in three mammalian cell types: fibroblasts, bone marrow stromal cells and osteoblasts. , 2002, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[125]  F. Cui,et al.  Crystal orientation, toughening mechanisms and a mimic of nacre , 2000 .

[126]  A. Rodríguez-Navarro,et al.  Geometrical and crystallographic constraints determine the self-organization of shell microstructures in Unionidae (Bivalvia: Mollusca) , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[127]  S. Weiner,et al.  Mollusc larval shell formation: amorphous calcium carbonate is a precursor phase for aragonite. , 2002, The Journal of experimental zoology.

[128]  L. Salvini-Plawen A reconsideration of systematics in the Mollusca (phylogeny and higher classification) , 1980 .

[129]  A. Bubel An electron-microscope study of periostracum formation in some marine bivalves. II. The cells lining the periostracal groove , 1973, Marine Biology.

[130]  H. Nakahara,et al.  The formation and growth of the prismatic layer ofPinctada radiata , 2005, Calcified Tissue Research.

[131]  K. Simkiss,et al.  Biomineralization : cell biology and mineral deposition , 1989 .

[132]  F. Meldrum Calcium carbonate in biomineralisation and biomimetic chemistry , 2003 .

[133]  J. Desbrières,et al.  An infrared investigation in relation with chitin and chitosan characterization , 2001 .

[134]  G. Cadée,et al.  HYDRAULIC BURROWING IN THE BIVALVE MYA ARENARIA LINNAEUS (MYOIDEA) AND ASSOCIATED LIGAMENTAL ADAPTATIONS , 1997 .

[135]  M. Antonietti,et al.  Amorphous layer around aragonite platelets in nacre. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[136]  Diane M. Griffiths,et al.  THE REGENTS OF THE UNIVERSITY OF CALIFORNIA , 2007 .

[137]  A. Lutts,et al.  X-ray diffraction patterns from the prisms of mollusk shells , 1960 .

[138]  A. Saleuddin Fine structure of normal and regenerated shell of Helix. , 1971, Canadian journal of zoology.

[139]  Steve Weiner,et al.  THE MATERIAL BONE: Structure-Mechanical Function Relations , 1998 .

[140]  A. Heuer,et al.  Tissue Regeneration in the Shell of the Giant Queen Conch, Strombus gigas , 2004 .

[141]  M. Marsh,et al.  Structure of the molluscan bivalve hinge ligament, a unique calcified elastic tissue. , 1976, Journal of ultrastructure research.

[142]  J. M. Bates,et al.  Determination of calcite: aragonite ratios in mollusc shells by infrared spectra1 , 1973 .

[143]  M. Epple,et al.  Early mineralization in Biomphalaria glabrata: Microscopic and structural results , 2003 .

[144]  M. Fritz,et al.  A Simple and Reliable Method for the Determination and Localization of Chitin in Abalone Nacre , 2002 .

[145]  S. Wise Microstructure and mode of formation of nacre (mother-of-pearl) in pelecypods, gastropods, and cephalopods , 1970 .

[146]  Frédéric Marin,et al.  Molluscan shell proteins , 2004 .

[147]  G. Falini,et al.  Crystallization of calcium carbonate salts into beta-chitin scaffold. , 2002, Journal of inorganic biochemistry.

[148]  E. Vieira,et al.  Amyloid – b-Sheet Formation at the Air-Water Interface , 1999 .

[149]  C. Hickman The problem of similarity: analysis of repeated patterns of microsculpture on gastropod larval shells , 2005 .

[150]  S. Mann Biomineralization and biomimetic materials chemistry , 1995 .

[151]  S. Weiner,et al.  Structure of the nacreous organic matrix of a bivalve mollusk shell examined in the hydrated state using cryo-TEM. , 2001, Journal of structural biology.

[152]  R. Ballarini,et al.  Structural basis for the fracture toughness of the shell of the conch Strombus gigas , 2000, Nature.

[153]  S. Weiner,et al.  Soluble protein of the organic matrix of mollusk shells: a potential template for shell formation , 1975, Science.

[154]  K. Bandel Shell Structure of the Gastropoda Excluding Archaeogastropoda , 1991 .

[155]  Himadri S. Gupta,et al.  Nanoscale Mechanisms of Bone Deformation and Fracture , 2008 .

[156]  F. Fisher,et al.  The fine structure and crystallography of the hinge ligament ofSpisula solidissima (Mollusca: Bivalvia: Mactridae) , 2004, Journal of comparative physiology.

[157]  Antonio G Checa,et al.  Self-organisation of nacre in the shells of Pterioida (Bivalvia: Mollusca). , 2005, Biomaterials.