Thermal site energy fluctuations in photosystem I: new insights from MD/QM/MM calculations

Cyanobacterial photosystem I (PSI) is one of the most efficient photosynthetic machineries found in nature. Due to the large scale and complexity of the system, the energy transfer mechanism from the antenna complex to the reaction center is still not fully understood. A central element is the accurate evaluation of the individual chlorophyll excitation energies (site energies). Such an evaluation must include a detailed treatment of site specific environmental influences on structural and electrostatic properties, but also their evolution in the temporal domain, because of the dynamic nature of the energy transfer process. In this work, we calculate the site energies of all 96 chlorophylls in a membrane-embedded model of PSI. The employed hybrid QM/MM approach using the multireference DFT/MRCI method in the QM region allows to obtain accurate site energies under explicit consideration of the natural environment. We identify energy traps and barriers in the antenna complex and discuss their implications for energy transfer to the reaction center. Going beyond previous studies, our model also accounts for the molecular dynamics of the full trimeric PSI complex. Via statistical analysis we show that the thermal fluctuations of single chlorophylls prevent the formation of a single prominent energy funnel within the antenna complex. These findings are also supported by a dipole exciton model. We conclude that energy transfer pathways may form only transiently at physiological temperatures, as thermal fluctuations overcome energy barriers. The set of site energies provided in this work sets the stage for theoretical and experimental studies on the highly efficient energy transfer mechanisms in PSI.