Sequential Proton-Coupled Electron Transfer Mediates Excited-State Deactivation of a Eumelanin Building Block

Abstract

Skin photoprotection is commonly believed to rely on the photochemistry of 5,6-dihydroxyindole (DHI)- and 5,6-dihydroxyindole-2-carboxylic acid (DHICA)-based eumelanin building blocks. Attempts to elucidate the underlying excited-state relaxation mechanisms have been partly unsuccessful due to the marked instability to oxidation. We report a study of the excited-state deactivation of DHI using steady-state and time-resolved fluorescence accompanied by high-level quantum-chemistry calculations including solvent effects. Spectroscopic data show that deactivation of the lowest excited state of DHI in aqueous buffer proceeds on the 100 ps time scale and is 20 times faster than in methanol. Quantum-chemical calculations reveal that the excited-state decay mechanism is a sequential proton-coupled electron transfer, which involves the initial formation of a solvated electron from DHI, followed by the transfer of a proton to the solvent. This unexpected finding would prompt a revision of current notions about eumelanin photophysics and photobiology.

Dynamics of electronically excited states in the eumelanin building block 5,6-dihydroxyindole

“…The 5,6-DHI absorption features seen in both water and methanol appear red-shifted by as much as 30 nm with respect to the gas phase. 8,11…”

“…Although 5,6-DHI and 5,6-DHICA have been studied extensively in solution, [8][9][10][11][12][13][14][15] our work is, to the best of our knowledge, the first gas phase excited state dynamics study to be conducted on either system. Gas phase measurements are an important "bottom-up" starting point that provide critical new benchmarks for advanced theory under conditions that are free from solvent perturbations.…”

Ultrafast spectral hole burning reveals the distinct chromophores in eumelanin and their common photoresponse

“…The desire to uncover structure-function relationships in eumelanin has inspired studies of the DHI and DHICA precursors along with oligomers formed from them. [11][12][13][14][15][16][17][18] This bottom-up approach has provided insight into the decay pathways of these putative eumelanin subunits, but the lack of agreement between their absorption spectra and that of eumelanin indicates that these studies cannot capture the full set of eumelanin chromophores. Additionally, these studies do not capture excitonic interactions between different kinds of chromophores, which are hypothesized to play a central role in the excited state dynamics of eumelanin.…”

Computational Study of Absorption Spectra of Eumelanin Constituents: Key Role of Oxidized Species in the Red Edge Absorption

“…The charge transfer character may trigger excited state proton-coupled electron transfer mechanisms that have been postulated to play an important role in the radiationless excited-state deactivation of melanin constituents. [17][18][19][20][21][22]…”