Morphogenesis of Biomineralized Calcitic Prismatic Tissue in Mollusca Fully Described by Classical Hierarchical Grain Boundary Motion

Abstract

Biomineralization of complex composite architectures comprising the shells of molluscs is known to proceed via self-assembly and in accordance with thermodynamic boundary conditions set by an organic macromolecular framework that is regulated by the organism. Hence, theoretically, the formation of these ultrastructures can be reproduced using the analytical backbone of various physical theories that are commonly employed to express crystal growth of man-made materials. Using a two-dimensional Monte Carlo Potts model simulation, we quantitatively describe and fully predict the structural evolution of the prismatic assembly in the shell of Pinctada nigra. The model, based on hierarchical motion of different types of grain boundaries that are involved in structural formation, has the capacity to describe the morphogenesis of various other biogenic and synthetic polycrystalline composite systems.

Crystal growth kinetics as an architectural constraint on the evolution of molluscan shells

“…Whereas the existence of this space and its size are still under debate, the majority of experimental evidence points toward its crucial role in shell biomineralization (17). Here, the different ultrastructures were hypothesized to form via self-assembly and grow in thickness from the periostracum toward the mantle cells, which guide their morphogenesis by changing the physical boundary conditions (e.g., saturation level, pH, and viscosity) and the chemistry of the solidifying medium by using a repertoire of organic and inorganic precursors (8, 18–20). For example, specific interactions of biomolecules with mineral precursors were shown to affect nucleation, polymorph selection, crystallization pathway, and the growth process of the mineral phase (21–25).…”

Biomineralized tissue formation as an archetype of ideal grain growth

“…Indeed, such a coarsening of the prismatic ultrastructure with the direction of growth has already been shown in a variety of bivalve shells. [9][10][11] To obtain a complete history of microstructural evolution of the prismatic layer in A. vexillum, we performed a microtomography experiment at beamline ID19 of the European Synchrotron Radiation Facility (ESRF). The organic interfaces, having the thickness of approximately 1 mm, were easily resolved using an effective voxel size of 0.649 mm.…”

“…Here we assume a linear correlation between the two and, essentially, reduce the three-dimensional growth in space into a twodimensional temporal process. [9][10][11] Average growth law…”

“…1a), and the other layer is a nacreous ultrastructure composed of flat platelets made of aragonite. Earlier studies were successful in demonstrating that physical models have the capacity to describe the morphogenesis of the prismatic architecture in a variety of bivalves [9][10][11] and ideal behaviour in A. vexillum was recently suggested. 12 However, ideal growth that perfectly adheres to all principal theoretical predictions has not yet been shown.…”

Insights into the Exceptional Crystallographic Order of Biominerals Using Dark-Field X-ray Microscopy

“…Like nature, materials science aims to produce function-optimised materials. Bio-inspired structures are growing increasingly common as scientists seek to understand and replicate natural growth processes [3]. Nonetheless, many aspects of biomineralization remain that are not fully understood.…”