Thermodynamic Aspects of Molluscan Shell Ultrastructural Morphogenesis

Abstract

Over the years, molluscan shells have become an exemplar model system to study the process of mineral formation by living organisms, the process of biomineralization. Typically, the shells consist of a number of mineralized ultrastructural motifs, each exhibiting a specific mineral-organic composite architecture. These are made of calcium carbonate building blocks having a well-defined three-dimensional morphology that is significantly different from the shape of inorganically formed counterparts. Shell ultrastructures are known to form via a biologically controlled extracellular mineralization pathway in which the organism has no direct control over mineral formation. The cellular tissue, responsible for shell biomineralization, forms an organic framework and sets-up the physical conditions necessary for the deposition of a specific morphology, whereas the growth of the mineral part of the shell proceeds spontaneously via the process of self-assembly. In this feature article, the ability to employ thermodynamic models from classical materials science to describe the process of self-assembly and structural evolution of a variety of shell architectures is reviewed. Having the potential to offer an analytical framework to express ultrastructure formation in time and in space, these models not only provide a deeper insight into shell biomineralization, but also suggest tools for novel composite materials design.

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.…”

“…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.…”

A computational framework for the morpho-elastic development of molluskan shells by surface and volume growth

“…They have become exemplar model systems for studying the processes of biomineralization, a topic attracting a great deal of interest: from materials science to biomedical applications [5,6]. Recent studies have begun to identify genes involved in these complex processes and to analyse how they are developmentally regulated [7], although the physical mechanisms underlying the morphogenesis of the shell ultrastructures remain poorly understood [8]. Recent attention has also been given to the formation and differentiation of the shell-secreting mantle margin during development [9] and its morphological variations among classes [10,11].…”

Finite Element Analysis as a Method to Study Molluscan Shell Mechanics

“…An extensive body of research exists investigating the biomineralization and biomechanical properties of mollusc shells . An outcome of this research is the appreciation of how biological systems can take a simple, brittle mineral, and transform it into a robust composite many times stronger and tougher than the constituent ceramic phase through the simple inclusion of an organic phase and manipulation of the multi‐component geometry.…”

“…Mollusc diversification continued throughout the Cambrian, by the end of which the two major molluscan clades, Aculifera and Conchifera, had been established along with the three conchiferan classes that most contribute to biomechanical research: Bivalvia, Gastropoda, and Cephalopoda (Figure ) . All three groups share the presence of a shell composed of calcium carbonate polymorphs; primarily made of aragonite, calcite, or some combination thereof − with the rare inclusion of vaterite, embedded within an organic matrix . The conchiferan shell is formed by the mantle, extracellularly, in the extrapallial space between the mantle tissue and existing periostracum (an outer organic layer) or shell (Figure ) .…”