Funneling energy through disorder

Light is the most important source of energy on the planet and, as such, the driver of several photochemical and photobiological processes such as photosynthesis—in which plants use solar energy to convert carbon dioxide and water into glucose and oxygen—vision, and human formation of vitamin D by exposure to sunlight, which are topics of high relevance nowadays.

However, in energizing certain biomolecules, excess light can also have adverse effects. For example, DNA can be cleaved by light, producing damaging free radicals. In plants, excess light can lead to photoinhibition, or photoinactivation of the reaction centers. Indeed, because oxygenic phototrophs generate O₂ as a by-product from the photocatalyzed splitting of water (H₂O), photosynthetic organisms have a particular risk of forming reactive oxygen species.

Over the course of evolution, nature has developed strategies to mitigate these adverse effects. Plants use a variety of photoreceptors to detect the intensity and direction of light and the duration of exposure to it. Some of these photoreceptors drive mechanisms that decrease the harm caused by excess light. Plants also produce enzymes that are essential for photoprotection. In humans, photoprotection of the skin is managed by very efficient internal conversion of energized DNA, proteins, and melanin. Specifically, the natural black-brown eumelanin pigment is the most widespread type of integumentary melanin. Its occurrence in large quantities gives the skin a brown color. It consists of a mixture of 5,6-dihydroxyindole molecules and 5,6-dihydroxyindole-2-carboxylic acid. Eumelanin has a high photoprotective power against ultraviolet photons by absorbing and rapidly dissipating their energy before they can cause damage to proteins and DNA. However, the description and understanding of the mechanism of photoprotection are rendered difficult by the extreme complexity of eumelanin that stems from its high degree of disorder and chemical diversity. Indeed, the two abovementioned indole monomers exist in different oxidation and protonation states and aggregate to form oligomers of different lengths and shapes. The π-conjugate oligomers stack into nanosized aggregates and larger particles.

This complexity is reflected in the absorption spectrum of the system, which is broad and featureless, continuously rising into the UV. Furthermore, the neighboring chromophores couple to each other, leading to the formation of collective excitonic states. This structural, chemical, and energetic disorder calls for a combination of tools to nail down the details of the photoprotection mechanism of eumelanin. Despite a number of foregoing studies with ultrafast spectroscopic tools, the description of the relaxation mechanism was still missing, and two opposing models for the critical molecular species were proposed: a) charge transfer excitons in solid-state aggregates or b) a molecular excited-state proton transfer in oligomers with the addition of excitonic coupling between electronic states. To solve this issue, Ilina et al. (1) used an impressive suite of advanced ultrafast spectroscopic tools and quantum chemical modeling.

In addition to steady-state absorption and resonance Raman spectroscopy, which helped characterize eumelanin as a heterogeneous ensemble of chromophores, they also used ultrafast spectroscopic tools such as transient absorption spectroscopy and ultrafast photoluminescence spectroscopy, which is needed because eumelanin fluorescence is characterized by a low yield (2). Indeed, if an emission occurs on a very short time scale, detection with a narrow temporal gate can capture the few photons that are emitted. As such, emissive states with quantum yields as low as 10⁻⁶ have been observed (3, 4). Furthermore, Ilina et al. (1) used femtosecond stimulated Raman spectroscopy, which is a powerful tool for observing changes in the vibrational structure of optically excited molecular systems (5).

From these studies, they conclude that light excites a distribution of chromophores that interconvert within 100 fs to states with energies in the visible range that rapidly localize. The role of excitonic coupling in this process is stressed. The localized excitations are confined within about 2 nm and are immobile, while they decay back to the ground state within a few picoseconds. Further to this, and in combination with pH- and solvent-dependent studies and quantum chemical calculations, they show that the early picosecond kinetics are consistent with a partial excited-state proton transfer from the catechol groups to the solvent.

Beyond elucidating the important photoprotective mechanisms of eumelanin, this study contains a number of broader conclusions. First, this work demonstrates the need for multispectroscopic approaches to understand how nature functions. It cannot be stressed how important this is, even when using the most advanced techniques. Examples of successful multispectroscopic approaches that include X-ray and optical domain methods are given in refs. 6 and 7. Second, the energy transfer and localization of the excitation are, to a certain extent, reminiscent of the processes occurring in photoexcited DNA strands (8, 9), for which in contrast to the present case, a charge transfer state is postulated, based on a combination of ultrafast TA and ultrafast linear dichroism studies (10). Third, despite the complexity of a chemically, energetically, and structurally disordered system, the energy dissipation pathway has been nailed down, showing how nature adopts a “reductive” approach in order to most efficiently funnel energy down a complex energy ladder. This seems to suggest that energy transport in this system does not undergo the generally assumed random walk approach in the transfer of electronic excitation energy (11). One may then raise the question as to whether the ultrafast (<100 fs) electronic relaxation down a significant energy gap (>1 eV) via energy transfer between chromophores is a coherent process? (12) A corollary to this question is: Over what distances does the energy travel prior to localization? Last but not least, a more fundamental question is: Does disorder matter in the present case? Is it part of the evolutionary design to optimize the funneling of energy?

Finally, this study sets an example of the strategy to adopt in elucidating electronic relaxation in disordered condensed phase molecular systems. One additional tool that could also greatly help in this respect is multidimensional spectroscopy (13), which holds great promise for the study of electronic energy transfer in partially (12, 14, 15) or fully disordered systems (16).

This study sets an example of the strategy to adopt in elucidating electronic relaxation in disordered condensed phase molecular systems.