Nacre biomineralisation: A review on the mechanisms of crystal nucleation

The wide diversity of biogenic minerals that is found in nature, each with its own morphology, mechanical properties and composition, is remarkable. In order to produce minerals that are optimally adapted for their function, biomineralisation usually occurs under strict cellular control. This control is exerted by specialised proteins and polysaccharides that assemble into a 3-dimensional organic matrix framework, forming a microenvironment where mineral deposition takes place. Molluscs are unique in that they use a striking variety of structural motifs to build their shells, each made of crystals with different morphologies and different calcium carbonate polymorphs. Much of want is known about mollusc shell formation comes from studies on the nacreous layer, or mother-of-pearl. In this review, we discuss two existing models on the nucleation of aragonite crystals during nacre formation: heteroepitaxial nucleation and mineral bridges. The heteroepitaxial nucleation model is based on the identification of chemical functional groups and aragonite-nucleating proteins at the centre of crystal imprints. It proposes that during nacre formation, each aragonite tablet nucleates independently on a nucleation site that is formed by acidic proteins and/or glycoproteins adsorbed on the chitin scaffold. The mineral bridges model is based on the identification of physical connections between the crystals in a stack, which results in a large number of crystals across several layers sharing the same crystallographic orientation. These observations suggest that there is one nucleation event per stack of tablets. Once the first crystal nucleates and reaches the top interlamellar matrix, it continues growing through pores, giving rise to the next layer of nacre, subsequently propagating into a stack. We compare both models and propose that they work in concert to control crystal nucleation in nacre. De novo crystal nucleation has to occur at least once per stack of aligned crystals, and is induced by nucleation sites. We suggest that further growth is controlled both by mineral bridges and nucleation sites. Finally, we discuss the role of amorphous calcium carbonate precursor in nacre formation.