Self-similar mesostructure evolution of the growing mollusc shell reminiscent of thermodynamically driven grain growth

Abstract

Significant progress has been made in understanding the interaction between mineral precursors and organic components leading to material formation and structuring in biomineralizing systems. The mesostructure of biological materials, such as the outer calcitic shell of molluscs, is characterized by many parameters and the question arises as to what extent they all are, or need to be, controlled biologically. Here, we analyse the three-dimensional structure of the calcite-based prismatic layer of Pinna nobilis, the giant Mediterranean fan mussel, using high-resolution synchrotron-based microtomography. We show that the evolution of the layer is statistically self-similar and, remarkably, its morphology and mesostructure can be fully predicted using classical materials science theories for normal grain growth. These findings are a fundamental step in understanding the constraints that dictate the shape of these biogenic minerals and shed light on how biological organisms make use of thermodynamics to generate complex morphologies.

Natural Pearls

“…Hartling's might have been a simpler, texture agnostic cellular segregation pattern -see Bayerlein et al [32] for this formalization; or approach the texture of prismatic shell -"dendritic prisms" in Checa et al [33]. Raman points to Clément & Rivière [34] for their controlled packing of dendritic calcium carbonate crystallization in a gel.…”

“…The transition between prismatic aragonite and nacre needs closer inspection. 32 Another mollusk provides a hint: Pododesmus macrocysma volunteers a handy marker for its muscle pearls -the myostracum is the only aragonite in this calcitic shell, and the small muscle pearls of Podo's are indeed of fibrous aragonite [ Fig. 1 e and 2 g,h,i].…”

Two‐Dimensional Hybrid Materials: Transferring Technology from Biology to Society

“…[25] In particular, from an application point of view it is interesting to point out that the formation of ordered assemblies of crystals with near-uniform sizes, shapes, and orientation as observed in the prismatic layer of the mollusk shell does not require a very precise templating structure. [26] Rather, these well-defined crystal assemblies are formed in a minimalistic approach in which uniformity results from competition driven by thermodynamic principles and which would relax the requirements for the bioinspired synthesis of advanced 2D hybrid materials. [27] In addition to the growth of 2D materials by several organisms, we can point out that 2D minerals are now thought to have possibly played a key role in the development of organisms in the early life evolution period.…”

Organic membranes determine the pattern of the columnar prismatic layer of mollusc shells

“…They constitute important functional materials acting in bending, their high degree of flexibility being provided by the organic envelopes. The growth in depth of the calcitic prisms of the outer layer of the pen shell Pinna nobilis has recently been explained by normal grain growth theory [11], according to which those prisms that initially exhibited lower transverse surface area or a lesser number of sides were more prone to be outcompeted during growth. In this view, the organic sheaths should passively adjust to the changes in dimensions of the prisms perpendicular to the growth axis [12].…”