Chemical and structural disorder in eumelanins: a possible explanation for broadband absorbance

Abstract

We report the results of an experimental and theoretical study of the electronic and structural properties of a key eumelanin precursor-5,6,-dihydroxyindole-2-carboxylic acid (DHICA)-and its dimeric forms. We have used optical spectroscopy to follow the oxidative polymerization of DHICA to eumelanin and observe red shifting and broadening of the absorption spectrum as the reaction proceeds. First principles density functional theory calculations indicate that DHICA oligomers (possible reaction products of oxidative polymerization) have the gap between the highest occupied molecular orbital and the lowest unoccupied molecular orbital red-shifted gaps with respect to the monomer. Furthermore, different bonding configurations (leading to oligomers with different structures) produce a range of gaps. These experimental and theoretical results lend support to the chemical disorder model where the broadband monotonic absorption characteristic of all melanins is a consequence of the superposition of a large number of nonhomogeneously broadened Gaussian transitions associated with each of the components of a melanin ensemble. These results suggest that the traditional model of eumelanin as an amorphous organic semiconductor is not required to explain its optical properties and should be thoroughly reexamined. These results have significant implications for our understanding of the physics, chemistry, and biological function of these important biological macromolecules. Indeed, one may speculate that the robust functionality of melanins in vitro is a direct consequence of its heterogeneity, i.e., chemical disorder is a "low cost" natural resource in these systems.

FIGURE 1

Characteristic broadband absorbance of eumelanin (dashed line) and pheomelanin (solid line). The spectra are featureless from the UV to the near infra-red and are more characteristic of an inorganic semiconductor than an organic pigment.

FIGURE 2

Schematic representation of DHICA (1a), DHI (1b), and the four dimers (2a–2d), which we also consider here.

FIGURE 3

¹H NMR of DHICA in DMSO-d6.

FIGURE 4

¹³C NMR of DHICA in DMSO-d6.

FIGURE 5

XPS spectra of DHICA. (a), C 1s region,( b), O 1s region, and (c) N 1s region. See text and Table 2 for assignments of individual components.

FIGURE 6

UV-visible absorption spectra DHICA in NaOH solution at t = 0 (a) and at various times (b) (legend represents hours).

FIGURE 7

Absorption versus time plots of the DHICA solution at 328 nm and 250 nm.

FIGURE 8

Electron density in the highest occupied molecular orbital (HOMO, left) and lowest unoccupied molecular orbital (LUMO, right) of 2a–d.