Microstructural Variation of Biogenic Calcite with Intracrystalline Organic Macromolecules

Abstract

The influence of intracrystalline organic macromolecules on the microstructure and properties of host crystals has been investigated by micro-and macroscopic analyses for several biogenic calcites: prisms in the outer layers of pearl oysters (Pinctada fucata), oysters (Crassostrea nippona), and pen shells (Atrina pectinata); folia in the inner layers of C. nippona and scallops (Patinopecten yessoensis); and coccoliths of Pleurochrysis carterae. Thermogravimetric analysis showed that the three prisms contain more intracrystalline organic matter than the folia and coccolith. Transmission electron microscopy (TEM) revealed that Fresnel contrasts, which probably correspond to the intracrystalline organic macromolecules, are distributed inhomogeneously and partition the calcite crystals into subgrains with small misorientations in the prisms of P. f ucata and C. nippona. From peak broadening in powder X-ray diffraction (XRD), we found a large variance of lattice spacing (Δd/d) in the two prisms. On the other hand, intracrystalline macromolecules in the prisms of A. pectinata are distributed rather homogeneously and do not influence the crystal structure, as revealed by diffraction contrast in TEM. XRD of the prisms in A. pectinata indicates significantly smaller Δd/d than that for the other two prisms. In the folia and coccolith, intracrystalline macromolecules were scarcely observed in TEM, and the estimated Δd/d is small. ■ INTRODUCTIONBiominerals often possess well-regulated structures with superior properties. 1,2 Such superiority may be ascribed to the fact that biominerals are not pure inorganic crystals because they contain a certain amount of organic matter. Mollusk shells, for example, contain organic components of up to 5% of the entire weight, 3 which may influence the polymorph selection, 4,5 morphology, 6 and mechanical properties 1 of biominerals.Calcium carbonate crystals are the most abundant biominerals. Calcite, one of the polymorphs of calcium carbonate, is the most thermodynamically stable polymorph under ambient conditions, but it is mechanically weak because of the perfect {104} cleavage planes. Biogenic calcite is, however, much more resistant to fractures than abiotic calcite because {104} cleavage planes generally do not develop at the fractures. This is attributed to the existence of organic matter within the crystals, 7 but it has not been elucidated at the atomic scale how organic matter modifies the calcite crystals to prevent the cleavages.The relationships between intracrystalline organic matter and calcium carbonate crystals have been investigated using X-ray diffraction (XRD). High-resolution synchrotron XRD analysis indicated that anisotropic lattice distortion and crystallite size exist in the calcite prismatic layers of bivalves, and the anisotropy has been ascribed to intracrystalline organic matter. 8 However, although XRD techniques can quantitatively estimate such anisotropy in the whole specimens, they do not tell us the actual interaction between organic matter and crystals at...

Crystallographic orientation inhomogeneity and crystal splitting in biogenic calcite

“…A similar pattern has been recently observed in the nacre of the mussel Perna [33]. Organic molecules occluded within the crystals and distributed around the boundaries of 200-300 nm crystalline domains (similar to the ones which we report here; figure 6a-c,e-i) were imaged with TEM in the calcites of the pterioidean Pinctada and in the ostreoidean Crassostrea [13,34]; the boundaries are characterized by small misorientations, in coincidence with small distortions of the crystal lattice. The same authors failed to find such patterns of misoriented domains in the calcite of the pinnoidean Atrina.…”

“…They are anisotropic in shape, extending differently along diverse crystallographic directions [11]. These findings are in good agreement with the TEM observations [8,13] of intracrystalline submicrometre partitions with different diffraction contrasts, which were limited by discontinuously aligned biomacromolecules. Up to now, no data on the misorientation between adjacent nanodomains have been provided, although values less than 28 can be inferred from fig.…”

“…Unfortunately, neither data from the literature nor our TEM data directly revealed the existence of dislocation lines on the material. Okumura et al [13], with TEM, noted similar rsif.royalsocietypublishing.org J R Soc Interface 10: 20130425…”

“…Pokroy et al [35,36] revealed that in biological calcite and aragonite the crystal lattices are anisotropically distorted, attributing this to the action of intracrystalline biomolecules. Okumura et al [13] reported significant differences in their calculated variances of lattice spacing, the values for Pinctada and Crassostrea being well above that for Atrina. This certainly correlates with the gradients and crystal-splitting processes recorded with EBSD in Pinctada and Ostrea, and with their absence in Pinna (see paragraph above).…”

Studies on the Chemical Structures of Organic Matrices and Their Functions in the Biomineralization Processes of Molluscan Shells

“…Crystallization in the shell, including that of organic matrices, produces an elaborate microstructure with micro-or nano-scale structures (Boggild 1930;Taylor and Kennedy 1969;Carter 1990;Carter and Hall 1990). Organic-inorganic microstructures reduce the area of the cleavage plane in the crystals and impart high mechanical strength and toughness to the shell (Kamat et al 2000;Okumura et al 2012). Previous reports have suggested that the organic matrices in the shell play key roles in regulating crystal nucleation, polymorphy, growth, morphology, and orientation in the calcification process (Lowenstam and Weiner 1989).…”