Autologous bone (AB) is the gold standard for bone-replacement surgeries¹, despite its limited availability and the need for an extra surgical site. Traditionally, competitive biomaterials for bone repair have focused on mimicking the mineral aspect of bone, as evidenced by the widespread clinical use of bioactive ceramics². However, AB also exhibits hierarchical organic structures that might substantially affect bone regeneration. Here, using a range of cell-free biomimetic-collagen-based materials in murine and ovine bone-defect models, we demonstrate that a hierarchical hybrid microstructure—specifically, the twisted plywood pattern of collagen and its association with poorly crystallized bioapatite—favourably influences bone regeneration. Our study shows that the most structurally biomimetic material has the potential to stimulate bone growth, highlighting the pivotal role of physicochemical properties in supporting bone formation and offering promising prospects as a competitive bone-graft material.

Significance: Disordered materials with heterogeneities at scales ranging from nano- to micrometers usually scatter visible light and become opaque beyond a certain thickness. However, transparent materials are found in nature. The physical origin of transparency in natural and artificial biopolymer materials is still not fully understood. Here, a gap of transparency is found in synthetic fibrillar collagen matrices within a very narrow range of concentration. The transparency results from structural partial order inhibiting light scattering, while preserving mechanical stability, stiffness, and nonlinearity. The potential to produce biomimetic hydrogels with such striking optical properties by self-assembly opens an interesting route in the study of photonic materials and provides new elements in the understanding of the appearance of transparency in natural materials.

The presence of phosphate from different origins (inorganic, bioorganic) is found more and more in calcium carbonate-based biominerals. Phosphate is often described as being responsible for the stabilization of the transient amorphous calcium carbonate phase. In order to specify the composition of the mineral phase deposited at the onset of carbonated shell formation, the present study investigates, down to the nanoscale, the growing shell from the European abalone Haliotis tuberculata, using a combination of solid state nuclear magnetic resonance, scanning transmission electron microscope and spatially-resolved electron energy loss spectroscopy techniques. We show the co-occurrence of inorganic phosphate with calcium and carbonate throughout the early stages of abalone shell formation. One possible hypothesis is that this first-formed mixed mineral phase represents the vestige of a shared ancestral mineral precursor that appeared early during Evolution. In addition, our findings strengthen the idea that the final crystalline phase (calcium carbonate or phosphate) depends strongly on the nature of the mineral-associated proteins in vivo.