Correlated Protein Environments Drive Quantum Coherence Lifetimes in Photosynthetic Pigment-Protein Complexes

摘要

SummaryEarly reports of long-lived quantum beating signals in photosynthetic pigment-protein complexes were interpreted to suggest that electronic coherence benefits from protection by the protein, but many subsequent studies have suggested instead that vibrational or vibronic contributions are responsible for the observed signals. Here, we devised two 2D-spectroscopy methods to observe how each exciton is perturbed by its nuclear environment in a photosynthetic complex. The first approach simultaneously monitors each exciton's energy fluctuations over time to obtain its time-dependent electronic-nuclear interactions. The second method isolates evidence of coupled interexcitonic environmental motions. The techniques are validated with Nile Blue A and subsequently used on the Fenna-Matthews-Olson (FMO) complex. The FMO data reveal that each exciton experiences nearly identical spectral motion after excitation and that spectral motion of one excited exciton induces similar motion on unpopulated neighboring excitonic states. These synchronized and correlated spectral dynamics prolong coherences in the FMO complex after femtosecond excitation.Graphical Display OmittedHighlights?Method of observing spectral motions directly after femtosecond excitation?Observed synchronized fluctuations among electronic states in a protein complex?Observed correlated spectral motion between occupied and unoccupied excited statesThe Bigger PictureObservations of quantum coherence in photosynthetic complexes spawned a new field of quantum biology for the study of how biology exploits quantum dynamics. However, theoretical models have suggested that these signals may not arise from electronic dynamics but rather from simple molecular vibrations. The key question is whether different excited electronic states evolve in a correlated fashion after excitation.Here, we have developed two spectroscopic methods to provide experimental evidence that electronic states within a photosynthetic protein-pigment complex experience correlated fluctuations after excitation. Surprisingly, we found that the excitonic transitions in the Fenna-Matthews-Olson complex all undergo the same spectral motion after excitation despite having different degrees of delocalization and different local environments, etc. Such correlated spectral motion explains how quantum coherence among electronic states can persist for so long after femtosecond excitation.Energy transfer in photosynthesis occurs as electronic excitations of coupled chromophores interact with their environment. The microscopic nature of these motions can enable novel energy-transfer mechanisms if the motions are not random. This study reveals synchronized and correlated fluctuations of the states within a photosynthetic pigment-protein complex, which explains prior observations of long-lived quantum coherence.