WEB A Structural Investigation into the Hydration Behaviour and Mechanical Adaptation of Brachiopod Shells
For hundreds of millions of years, nature has evolved a large assortment of organic-inorganic hybrid materials that are optimally adapted for a wide range of functions, including navigation, protection, mechanical support and protection. These materials not only exhibit exceptional material properties but also display multifunctionality, including features such as adapting, sensing and self-healing.2, 3 Among the most remarkable biominerals found in nature are the shells of the phosphatic brachiopods Discinisca tenuis and Lingulla anatina. We empirically observed, for the first time, that the mechanical properties of these shells vary according to their water content. While they are hard and stiff when dry, they become flexible when hydrated, to the point that the shell can be folded in 2 without fracturing. Such capability of an organic-inorganic composite to switch reversibly between stiff and flexible and in real time, adapting to changes in the environment that demand a different set of mechanical properties, is truly unique among both biological and synthetic materials. The aim of this research was to characterise how the structure the brachiopod shells changes as a function of hydration, leading to changes in mechanical properties.
We used cryo-ptychographic X-ray computed tomography (PXCT) on dry, partially hydrated (exposed to 70 % relative humidity) and fully hydrated shells (exposed to 100 % relative humidity) to characterise how the structure of the shell at the sub-micron and micron levels changed as a function of hydration. Solid-state NMR (SSNMR) was used to determine the effect of hydration on the molecular conformation of the organic components.
PXCT measurements demonstrated the organic-rich layers in the shell expanded in thickness, increasing from ~160 nm in the dry sample to ~180 nm in the partially hydrated and ~340 nm in the fully hydrated sample. Using SSNMR, we identified that the macromolecular chains of proteins, and in particular the methyl groups in proximity to the mineral, become more mobile with hydration.
Our results show that the changes in the mechanical properties of the shell as it absorbs water arise from modifications in the mobility of the organic components and structural changes, at the sub-micron and micrometer levels, caused by the swelling of the organic layers.