Coherent steering of photosynthetic excitons with redox-dependent vibronic coupling

Photosynthetic pigment-protein complexes can capture and transport solar energy with high efficiency. It has been shown that the Fenna-Matthews-Olson (FMO) complex can quench excitations in oxidizing redox environments via a cysteine-mediated mechanism to prevent the generation of reactive oxygen species. In this study, we use two-dimensional electronic spectroscopy to map the excited state dynamics of wild-type and cysteine-mutated FMO complexes in both oxidizing and reducing conditions. We find that FMO steers excitations toward quenching sites in oxidizing conditions by modulating the vibronic coupling of its chromophores. Specifically, the oxidized cysteines shift the pigment energies to detune the resonant coupling between excitons and a vibrational mode in bacteriochlorophyll-a. This vibronically-enhanced energy transfer correlates with increased quantum beating signatures in the two-dimensional spectra. We assign these beating signals to excited state vibrational coherences that maintain their phase relationship through the energy transfer process. These results show that the vibronic energy transfer process proceeds through a coherent mechanism and that photosynthesis has evolved to exploit the quantum mechanics of vibronic coupling for photoprotection.