Insect cuticle is a widespread yet poorly-understood biological composite material with diverse and specialized mechanical properties. The main structural components, chitin and proteins, form a complex, fiber-reinforced network, while additional components such as catechols, enzymes and water modulate the interactions between the structural materials. We performed a comprehensive study of the mechanical properties of elytra from Tribolium castaneum and Tenebrio molitor as a function of maturation time. As the insects mature, the cuticle changes from a soft (E=44±8MPa) and ductile material to a stiff (E=2400±1100MPa) and brittle material. To understand the origin of such changes in mechanical properties, we have used dynamic mechanical analysis to examine the material interactions within this multicomponent biomaterial. Our results are consistent with the hypothesis that cuticle components become more cross-linked over time, given that the frequency dependence of the storage modulus decreases significantly. Dehydration also stiffens the cuticle and introduces additional physical interactions, but does not account for all the changes in mechanical properties seen upon tanning. Treating the fully mature cuticle with physical bond-breaking solvents does not completely reverse the properties to those of the immature state, suggesting that permanent, covalent interactions develop over time. RNA interference has also been used to support the hypothesized mechanism of enzymatic cross-linking leading to the development of mechanical properties.
In the design of bio-inspired composite materials, it is important to understand which features of the complex biological structures need to be replicated. Often, biomaterials have many layers of hierarchical structure from the macroscale to the molecular scale. For technological applications, the synthesis of biomimetic materials would be simplified if we knew exactly which features were essential for a particular function. For example, we have determined that molecular interactions such as protein cross-linking serve to increase the elastic response of cuticle over a broad range of frequencies. However, on a macroscale, the cuticle has rib structures that confer additional toughness by stopping the propagation of cracks. Knowledge of such structure-function relationships will allow for precise control over synthetic material properties. Our understanding of the structure-function properties of beetle elytral cuticle has inspired the design of high strength, biocompatible polymer networks made of agarose and polyethylene glycol (PEG) to be used as tissue engineering scaffolds. The structure of the interpenetrating hydrogel networks (IPNs) mimics the cuticle’s combination of chitin fibers embedded in a protein matrix. The IPN has significantly greater toughness than either PEG or agarose alone. Structure-function characterization of other naturally efficient biological materials has the potential to improve the design of new bio-based composites by determining which aspects of the biological material are most essential to an analogous technological material.
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