The mechanism (s) that drive the organization of bone mineral throughout the bone extracellular matrix remain unclear. The long-standing theory implicates the organic matrix, namely specific non-collagenous proteins and/or collagen fibrils, while a recent theory proposes a self-assembly mechanism. Applying a combination of spectroscopic and microscopic techniques in wet and dry conditions to bone-like hydroxyapatite nanoparticles that were used as a proxy for bone mineral, we confirm that mature bone mineral particles have the capacity to self-assemble into organized structures. A large quantity of water is present at the surface of bone mineral due to the presence of a hydrophilic, amorphous surface layer that coats bone mineral nanoparticles. These water molecules must not only be strongly bound to the surface of bone mineral in the form of a rigid hydration shell, but they must also be trapped within the amorphous surface layer. Cohesive forces between these water molecules present at the mineral–mineral interface not only hold the mature bone mineral particles together, but also promote their oriented stacking. This intrinsic ability of mature bone mineral particles to organize themselves without recourse to the organic matrix forms the foundation for the development of the next generation of orthopedic biomaterials.
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