Not all bone nanocomposites are equal: structure-water-micromechanics of osteocytic and anosteocytic fishbone material

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The skeletons of vertebrates are made of bone, a nanocomposite material comprising mineralized collagen fibrils and water, as well as small amounts of non-collagenous proteins. Bone can withstand recurrent mechanical loads over a long period of time without failing due to the existence of a mechanism of self-repair of accumulated microdamage and by being able to adapt to changing loads (re/modeling). In widely studied mammalian bone, re/modeling is thought to be regulated and activated by bone cells (osteocytes) residing in lacunae within the bone matrix, communicating via canaliculi. It is therefore intriguing that the bone material of a large group of advanced teleosts is totally devoid of osteocytes (anosteocytic bone). In the previously funded period, we found several differences between the two bone types that might help understand how they may be able to re/model with and without osteocytes. We propose to further explore and understand the differences in the structure-mechanical function relations between medaka and zebrafish bone types, studied in-vivo in the first funding period. To this end, new computer-based experiments will explore data already collected in the first part of the study. We will quantify differences in composition, microstructure and water permeability, and their mechanical deformation response will be compared by 3D in situ loading experiments along with FE analysis. In the first funding period, we observed an unexpected difference between water diffusion across the ECM regions in anosteocytic and osteocytic bone, despite a very similar composition of mineralized collagen fibers. We will investigate the cause of this difference, as well as the hypothesis that water diffusion is the likely agent of stress transduction in osteocytic bone. Stress generated by bone dehydration will also be used to study crack propensity differences. By combining all the proposed methods, we expect to provide insights into the interplay between geometry, texture, and hydration state of the anosteocytic and osteocytic bone and, therefore, give a new perspective of how bones cope with mechanical stress, circumventing damage.