Oxidation-State-Controlled Janus Behavior in Eumelanin: Nonadiabatic Branching between Photoprotection and Photoreactivity

Eumelanin exhibits a Janus character, functioning as both a highly efficient photoprotectant and, under certain conditions, a source of photochemical reactivity. The molecular origins of this dual behavior remain incompletely understood, particularly regarding the role of oxidation state in excited-state branching. In this work, we investigate the nonadiabatic excited-state dynamics of three representative eumelanin monomers─hydroquinone (DHI), semiquinone (MKI), and fully oxidized quinone (DKI)─using MRSF-TDDFT-based surface-hopping molecular dynamics simulations. Our results reveal a clear oxidation-state-dependent modulation of excited-state relaxation pathways. DHI exhibits extensive branching, with only 26% of trajectories returning intact to the ground state, while the majority (62%) undergo radical formation via N-H and O-H bond dissociation. MKI, in contrast, displays predominantly nonreactive ultrafast internal conversion, with 79.9% of trajectories restoring the original structure and 20.1% forming a tautomer via excited-state intramolecular proton transfer (ESIPT), but without radical formation. Fully oxidized DKI shows the most restricted behavior: relaxation proceeds exclusively through a single conical intersection channel, with 100% structural recovery and no proton transfer or radical pathways. These findings demonstrate that oxidation state governs the balance between photoprotective internal conversion and photoreactive radical branching. Reduced forms favor radical-generating channels, whereas oxidized forms promote structurally conservative decay. This oxidation-controlled nonadiabatic branching provides a microscopic basis for the intrinsic Janus behavior of eumelanin and suggests that pigment redox composition critically regulates its photobiological function.