Biogenic plate-like guanine crystals form via templated nucleation of thin crystal leaflets on amyloid scaffolds

The nanoscale morphologies of crystalline materials determine their optical, electrical and mechanical properties and, thus, their potential applications. However, producing crystals with particular shapes requires overriding their strong tendency to adopt thermodynamically stable structures. Nevertheless, many organisms form crystals with distinct morphologies, such as the plate-like guanine crystals formed by a large variety of terrestrial and aquatic species for vision, camouflage, body temperature regulation, and kin recognition. The control over crystal morphogenesis was hypothesized to involve physical growth restriction by the delimiting crystal chamber membrane, combined with fine-tuned interactions between organic molecules and the growing crystals. Using cryo-electron tomography, we followed crystal formation in developing zebrafish larvae in three dimensions. We find that initially, crystals form in the lumen of the crystal-forming organelle, with no contact with the delimiting membrane. Only later in development the elongating crystals reach the membrane and eventually push against it, deforming the organelle shape. We further show that crystals form via templated nucleation of multiple thin leaflets on preassembled, 20 nm thick, amyloid protein scaffolds. The initial thin leaflets then merge and coalesce into a single platelet crystal, with no obvious reminiscence of the initial leaflets. Our findings provide new insights into how organisms control the morphology and, thereby, optical properties of crystals, setting the stage for studying the interaction between proteins and molecular crystals.