Delocalized electronic excitations and their role in directional charge transfer in the reaction center of...

In purple bacteria, the fundamental charge-separation step that drives the conversion of radiation energy into chemical energy proceeds along one branch-the A branch-of a heterodimeric pigment-protein complex, the reaction center. Here, we use first principles time-dependent density functional theory (TDDFT) with an optimally-tuned range-separated hybrid functional to investigate the electronic and excited-state structure of the six primary pigments in the reaction center of Rhodobacter sphaeroides. By explicitly including amino-acid residues surrounding these six pigments in our TDDFT calculations, we systematically study the effect of the protein environment on energy and charge-transfer excitations. Our calculations show that a forward charge transfer into the A branch is significantly lower in energy than the first charge transfer into the B branch, in agreement with the unidirectional charge transfer observed experimentally. We further show that the inclusion of the protein environment redshifts this excitation significantly, allowing for energy transfer from the coupled Qx excitations. Through analysis of transition and difference densities, we demonstrate that most of the Q-band excitations are strongly delocalized over several pigments and that both their spatial delocalization and charge-transfer character determine how strongly affected they are by thermally-activated molecular vibrations. Our results suggest a mechanism for charge-transfer in this bacterial reaction center and pave the way for further first-principles investigations of the interplay between delocalized excited states, vibronic coupling, and the role of the protein environment in this and other complex light-harvesting systems.