Operando Spectroelectrochemical Characterization Shows that the Dynamic Flow of Electrons through Melanin Involves Its Redox-State Switching

Melanin is a group of heterogeneous polymeric pigments that has been proposed to perform various biological functions and is attracting increasing technological interest as a sustainable electronic material for energy storage and bioelectronics. Here, we prepared a semitransparent hydrogel film from a soluble melanin obtained from the black soldier fly (Hermetia illucens; BSF) and applied an operando spectroelectrochemical approach to investigate the molecular-level changes that occur when electrons are "flowing" through this melanin (i.e., while electron transfer processes are "in operation"). Like other natural and synthetic melanins, we observed that the BSF melanin has reversible redox activities in the mid-physiological redox potential range. We report that electron transfer can occur through an indirect (mediator-based) mechanism and also through a direct mechanism involving an extrinsic electron exchange with conducting graphene. In both mechanisms, we show that electron transfer is correlated to a reversible switching of the melanin's redox state. Finally, we provide evidence to support a chemical disorder model, which suggests that the properties of melanin may involve diverse structural and mechanistic features that occur over various length scales. Overall, we show that operando spectroelectrochemical measurements can bridge traditional bottom-up and top-down methods to facilitate the characterization of melanin.