Untangling the Mechanisms of Lattice Distortions in Biogenic Crystals across Scales

Biomineralized structures are complex functional hierarchical assemblies composed of biomineral building blocks joined together by an organic phase. The formation of individual mineral units is governed by the cellular tissue component that orchestrates the process of biomineral nucleation, growth, and morphogenesis. These processes are imprinted in the structural, compositional, and crystallographic properties of the emerging biominerals on all scales. Measurement of these properties can provide crucial information on the mechanisms that are employed by the organism to form these complex 3D architectures and to unravel principles of their functionality. Nevertheless, so far, this has only been possible at the macroscopic scale, by averaging the properties of the entire composite assembly, or at the mesoscale, by looking at extremely small parts of the entire picture. In this study, the newly developed synchrotron-based dark-field X-ray microscopy method is employed to study the link between 3D crystallographic properties of relatively large calcitic prisms in the shell of the mollusc Pinna nobilis and their local lattice properties with extremely high angular resolution down to 0.001°. Mechanistic links between variations in local lattice parameters and spacing, crystal orientation, chemical composition, and the deposition process of the entire mineral unit are unraveled.