Crystallographic control on the substructure of nacre tablets.

Nacre tablets of mollusks develop two kinds of features when either the calcium carbonate or the organic portions are removed: (1) parallel lineations (vermiculations) formed by elongated carbonate rods, and (2) hourglass patterns, which appear in high relief when etched or in low relief if bleached. In untreated tablets, SEM and AFM data show that vermiculations correspond to aligned and fused aragonite nanogloblules, which are partly surrounded by thin organic pellicles. EBSD mapping of the surfaces of tablets indicates that the vermiculations are invariably parallel to the crystallographic a-axis of aragonite and that the triangles are aligned with the b-axis and correspond to the advance of the {010} faces during the growth of the tablet. According to our interpretation, the vermiculations appear because organic molecules during growth are expelled from the a-axis, where the Ca-CO3 bonds are the shortest. In this way, the subunits forming nacre merge uninterruptedly, forming chains parallel to the a-axis, whereas the organic molecules are expelled to the sides of these chains. Hourglass patterns would be produced by preferential adsorption of organic molecules along the {010}, as compared to the {100} faces. A model is presented for the nanostructure of nacre tablets. SEM and EBSD data also show the existence within the tablets of nanocrystalline units, which are twinned on {110} with the rest of the tablet. Our study shows that the growth dynamics of nacre tablets (and bioaragonite in general) results from the interaction at two different and mutually related levels: tablets and nanogranules.

[1]  H. Xin,et al.  Calcite Prisms from Mollusk Shells (Atrina Rigida): Swiss‐cheese‐like Organic–Inorganic Single‐crystal Composites , 2011 .

[2]  B. Schöne,et al.  Mutvei's solution: An ideal agent for resolving microgrowth structures of biogenic carbonates , 2005 .

[3]  Y. Dauphin,et al.  Nanostructures of the aragonitic otolith of cod (Gadus morhua). , 2008, Micron.

[4]  Yuh J. Chao,et al.  Nanoscale Structural and Mechanical Characterization of a Natural Nanocomposite Material: The Shell of Red Abalone , 2004 .

[5]  B. Maier,et al.  Homoepitaxial meso- and microscale crystal co-orientation and organic matrix network structure in Mytilus edulis nacre and calcite. , 2013, Acta biomaterialia.

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

[7]  E. Dessilly,et al.  The Devonian Bryozoa of Belgium. The discovery of the Hemitrypa and Semicoscinium genera in the Devonian of Belgium , 1962 .

[8]  J. Cartwright,et al.  Calcium carbonate polyamorphism and its role in biomineralization: how many amorphous calcium carbonates are there? , 2012, Angewandte Chemie.

[9]  H. Mutvei,et al.  Crystalline structure, orientation and nucleation of the nacreous tablets in the cephalopod Nautilus , 2010 .

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

[11]  M. Burghammer,et al.  Structure-property relationships of a biological mesocrystal in the adult sea urchin spine , 2012, Proceedings of the National Academy of Sciences.

[12]  M. Fritz,et al.  Correlation of the orientation of stacked aragonite platelets in nacre and their connection via mineral bridges. , 2009, Ultramicroscopy.

[13]  Y. Kauffmann,et al.  Inhomogeneity of Nacre Lamellae on the Nanometer Length Scale , 2012 .

[14]  Y. Dauphin The nanostructural unity of Mollusc shells , 2008, Mineralogical Magazine.

[15]  A. Baronnet,et al.  Crystallization in organo-mineral micro-domains in the crossed-lamellar layer of Nerita undata (Gastropoda, Neritopsina). , 2012, Micron.

[16]  H. Mutvei Ultrastructural Characteristics of the Nacre in Some Gastropods , 1978 .

[17]  Y. Dauphin Nanostructures de la nacre des tests de céphalopodes actuels , 2001 .

[18]  S. Weiner,et al.  Crystallization Pathways in Biomineralization , 2011 .

[19]  H. Mutvei The nacreous layer inMytilus, Nucula, andUnio (Bivalvia) , 1977, Calcified Tissue Research.

[20]  Martin R. Lee,et al.  Crystallography and chemistry of the calcium carbonate polymorph switch in M. edulis shells , 2006 .

[21]  M. Kunz,et al.  Crystal lattice tilting in prismatic calcite. , 2013, Journal of structural biology.

[22]  K. Wada Crystal growth of molluscan shells , 1961 .

[23]  A. Baronnet,et al.  Crystallization of biogenic Ca-carbonate within organo-mineral micro-domains. Structure of the calcite prisms of the Pelecypod Pinctada margaritifera (Mollusca) at the submicron to nanometre ranges , 2008, Mineralogical Magazine.

[24]  Frédéric Marin,et al.  Merging models of biomineralisation with concepts of nonclassical crystallisation: is a liquid amorphous precursor involved in the formation of the prismatic layer of the Mediterranean Fan Mussel Pinna nobilis? , 2012 .

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

[26]  Julyan H E Cartwright,et al.  Mineral bridges in nacre. , 2011, Journal of structural biology.

[27]  A. Sánchez-Navas,et al.  Crystal Growth in the Foliated Aragonite of Monoplacophorans (Mollusca) , 2009 .

[28]  L. Holt,et al.  Phase transitions in biogenic amorphous calcium carbonate , 2012, Proceedings of the National Academy of Sciences.

[29]  S. Weiner,et al.  Transformation mechanism of amorphous calcium carbonate into calcite in the sea urchin larval spicule , 2008, Proceedings of the National Academy of Sciences.

[30]  Y. Nelyubina,et al.  From "loose" to "dense" crystalline phases of calcium carbonate through "repulsive" interactions: an experimental charge-density study. , 2012, Chemistry.

[31]  Xiaodong Li,et al.  Uncovering Aragonite Nanoparticle Self-assembly in Nacre—A Natural Armor , 2012 .

[32]  H. Nagasawa,et al.  Characteristics of biogenic calcite in the prismatic layer of a pearl oyster, Pinctada fucata. , 2010, Micron.

[33]  H. Nagasawa,et al.  Microstructural Variation of Biogenic Calcite with Intracrystalline Organic Macromolecules , 2012 .

[34]  S. Weiner,et al.  Spiers Memorial Lecture. Lessons from biomineralization: comparing the growth strategies of mollusc shell prismatic and nacreous layers in Atrina rigida. , 2003, Faraday discussions.

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

[36]  H. Mutvei The nacreous layer in Mytilus, Nucula, and Unio (Bivalvia). Crystalline composition and nucleation of nacreous tablets. , 1977, Calcified tissue research.

[37]  A. Putnis,et al.  Nano-cluster composite structure of calcitic sponge spicules--a case study of basic characteristics of biominerals. , 2006, Journal of inorganic biochemistry.

[38]  M. Cusack,et al.  Comparison of the crystallographic structure of semi nacre and nacre by electron backscatter diffraction , 2007 .

[39]  Xiaodong Li,et al.  Order-disorder transition of aragonite nanoparticles in nacre. , 2012, Physical review letters.

[40]  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.

[41]  P. Fratzl,et al.  Nanostructure of biogenic calcite crystals : a view by small-angle X-ray scattering , 2011 .

[42]  Robert M. Panas,et al.  Nanoscale Morphology and Indentation of Individual Nacre Tablets from the Gastropod Mollusc Trochus Niloticus , 2005 .

[43]  J. Stolarski,et al.  Hierarchically structured scleractinian coral biocrystals. , 2008, Journal of structural biology.

[44]  Xiaodong Li,et al.  Unveiling the formation mechanism of pseudo-single-crystal aragonite platelets in nacre. , 2009, Physical review letters.

[45]  Christopher J. Johnson,et al.  Architecture of columnar nacre, and implications for its formation mechanism. , 2007, Physical review letters.

[46]  Xiaodong Li,et al.  In situ observation of nanograin rotation and deformation in nacre. , 2006, Nano letters.

[47]  Andreas Scholl,et al.  Gradual ordering in red abalone nacre. , 2008, Journal of the American Chemical Society.

[48]  P. Gilbert Polarization-dependent Imaging Contrast (PIC) mapping reveals nanocrystal orientation patterns in carbonate biominerals , 2012 .

[49]  W. Schmidt Die Bausteine des Tierkörpers in polarisiertem Lichte , 1924 .

[50]  A. Freer,et al.  Aragonite Prism−Nacre Interface in Freshwater Mussels Anodonta anatina (Linnaeus, 1758) and Anodonta cygnea (L. 1758) , 2010 .

[51]  J. Gómez‐Herrero,et al.  WSXM: a software for scanning probe microscopy and a tool for nanotechnology. , 2007, The Review of scientific instruments.

[52]  J. Valley,et al.  Mollusk shell nacre ultrastructure correlates with environmental temperature and pressure. , 2012, Journal of the American Chemical Society.

[53]  H. Mutvei,et al.  Structural relationship between interlamellar organic sheets and nacreous tablets in gastropods and the cephalopodNautilus , 2008 .

[54]  C. Grégoire On submicroscopic structure of the Nautilus shell , 1962 .