A microscopically motivated model for the swelling-induced drastic softening of hydrogen-bond dominated biopolymer networks.

The penetration of water into rubber-like protein networks such as cross-linked resilin, which is found in insects, can lead to changes in stiffness that range over several orders of magnitude. This softening effect cannot be explained by the volumetric changes associated with pure swelling/deswelling used to describe networks with covalent bonds. Rather, this property stems from the reversible swelling-induced breaking of hydrogen cross-linking bonds that connect the chains in the network. This work presents a model for the swelling and the mechanical response of hydrogen-bond dominated biopolymer networks. It is shown that the penetration of water molecules into the network leads to the breaking of non-covalent cross-linking sites. In turn, the network experiences a reduction in the effective chain-density, an increase in entropy, and a consequent decrease in free energy, thus explaining the dramatic softening. Additionally, the breaking of hydrogen bonds alters the micro-structure and changes the quantitative elastic behavior of the network. The proposed model is found to be in excellent agreement with several experimental findings. The merit of the work is twofold in that it (1) accounts for the number and the strength of non-covalent cross-linking bonds, thus explaining the drastic reduction in stiffness upon water uptake, and (2) provides a method to characterize the micro-structural evolution of hydrogen-bond dominated networks. Consequently, the model can be used as a micro-structural design-guide to program the response of synthetic polymers. STATEMENT OF SIGNIFICANCE: Hydrogen-bond dominated biopolymer networks are found in insects and have a unique structure that allows a dramatic reduction of several orders of magnitude in stiffness upon hydration. Understanding the micro-structure of such networks is key in the fabrication of new biomimetic polymers with tunable mechanical properties. This work introduces a microscopically motivated model that explains the dramatic reduction in stiffness and quantifies the influence of key micro-structural quantities on the overall response. The model is validated through several experimental findings. The insights from this work motivate further attempts at the fabrication of new biomimetic polymers and serve as a micro-structural design guide that enables the programming of the elastic swelling-induced response.