Electron diffraction and solid-state NMR reveal the structure and exciton coupling in a eumelanin precursor

Abstract

Eumelanin, a versatile biomaterial found throughout the animal kingdom, performs essential functions like photoprotection and radical scavenging. The diverse properties of eumelanin are attributed to its elusive and heterogenous structure with DHI (5,6-dihydroxyindole) and DHICA (5,6-dihydroxyindole-2-carboxylic acid) precursors as the main constituents. Despite DHICA being recognized as the key eumelanin precursor, its crystal structure and functional role in the assembled state remain unknown. Herein, we employ a synthesis-driven, bottom-up approach to elucidate the structure and assembly-specifics of DHICA, a critical building block of eumelanin. We introduce an interdisciplinary methodology to analyse the nanocrystalline assembly of DHICA, employing three-dimensional electron diffraction (3D ED), solid-state NMR and density functional theory (DFT), while correlating the structural aspects with the electronic spectroscopic features. The results underscore charge-transfer exciton delocalization as the predominant energy transfer mechanism within the π–π stacked and hydrogen-bonded crystal network of DHICA. Additionally, extending the investigation to the ¹³C-labelled DHICA-based polymer improves our understanding of the chemical heterogeneity across the eumelanin pigment, providing crucial insights into the structure of eumelanin.