Unraveling the electronic origin of a special feature in the triplet-minus-singlet spectra of carotenoids in natural photosystems

Abstract

The influence of carotenoid triplet states on the Q_y electronic transitions of chlorophylls has been observed in experiments on light-harvesting complexes over the past three decades, but the interpretation of the resulting spectral feature in the triplet minus singlet (T–S) absorption spectra of photosystems is still debated, as the physical–chemical explanation of this feature has been elusive. Here, we resolve this debate, by explaining the T–S spectra of pigment complexes over the Q_y-band spectral region through a comparative study of chlorophyll–carotenoid model dyads and larger pigment complexes from the main light harvesting complex of higher plants (LHCII). This goal is achieved by combining state-of-the-art time-dependent density functional theory with analysis of the relationship between electronic properties and nuclear structure, and by comparison to the experiment. We find that the special signature in the T–S spectra of both model and natural photosystems is determined by singlet-like triplet excitations that can be described as effective singlet excitations on chlorophylls influenced by a stable electronic triplet on the carotenoid. The comparison with earlier experiments on different light-harvesting complexes confirms our theoretical interpretation of the T–S spectra in the Q_y spectral region. Our results indicate an important role for the chlorophyll–carotenoid electronic coupling, which is also responsible for the fast triplet–triplet energy transfer, suggesting a fast trapping of the triplet into the relaxed carotenoid structure. The gained understanding of the interplay between the electronic and nuclear structures is potentially informative for future studies of the mechanism of photoprotection by carotenoids.