How carotenoid distortions determine optical properties: Lessons from the Orange Carotenoid Protein
Carotenoids in photosynthetic light-harvesting proteins carry out the dual function of harvesting light and defending against high light by quenching excess energy. The latter involves the low-lying, dark, excited electronic state labelled S1. Here "dark" means optically-forbidden, a property that is often (in the photosynthetic field at least) vaguely attributed to molecular symmetry, leading to speculation that its optical properties may be strongly-perturbed by structural distortions. This has been both explicitly and implicitly proposed as an important feature of excess energy quenching. Here we present a theoretical analysis of the relationship between structural distortions and S1 optical properties. We outline how S1 is dark not because of overall geometric symmetry but because of a topological symmetry related to bond length alternation in the conjugated backbone. Taking the carotenoid Echinenone as an example and using a combination of molecular dynamics, quantum chemistry, and the theory of spectral lineshapes, we show that distortions that break this symmetry are extremely "stiff". They are therefore absent in solution and only marginally present in even a very highly-distorted protein binding pocket such as in the Orange Carotenoid Protein (OCP). This means that, on average, S1 remains resolutely dark for reasons unrelated to any bulk symmetry (or lack thereof) of the molecule. However, we demonstrate that on short timescales the S1 transition dipole strength fluctuates strongly due to optically active C-C and C=C vibrations. We hypothesize that this is a possible reason for the observation of ultra-fast energy transfer involving S1 in time-resolved spectroscopy.