Mineralization of Bouligand-structured collagen matrices derived from fish scales with enhanced mechanical properties and biocompatibility

Abstract

Biological materials often combine both high strength and toughness, with their exceptional mechanical properties relying on multi-scale hierarchical architectures. Investigating the biomineralization processes of such materials provides valuable inspiration for designing artificial composites. The scales of the jiangjunjia (Sargocentron rubrum), known for their armor-like hardness, feature an internal collagen layer arranged in a 75° staggered pattern, characteristic of a Bouligand structure. Needle-shaped hydroxyapatite crystals are embedded within the interstices of collagen fibrils, with their c-axis aligned parallel to the longitudinal axis of the collagen. During remineralization, mineralized spots gradually evolve from irregular shapes into well-defined rhombic morphologies, growing and coalescing at an approximate rate of 60 µm²/h. The long axis of these rhombic regions aligns with the orientation of the collagen fibrils. Interestingly, throughout the remineralization process, the external waxy layer of the scale remains almost non-participatory in mineralization. However, the region adjacent to the waxy layer exhibits enhanced mineral growth. Remarkably, after 14 days of remineralization, the regenerated scale achieves mechanical properties comparable to those of the original scale-despite having a mineral content of only 26.0%-while also demonstrating superior biocompatibility. This makes it a promising candidate for developing novel bone repair materials.