Abstract
Photosystem II (PSII), the principal enzyme of oxygenic photosynthesis, contains two integral light harvesting proteins (CP43 and CP47) that bind chlorophylls and carotenoids. The two intrinsic antennae play crucial roles in excitation energy transfer and photoprotection. CP43 interacts most closely with the reaction center of PSII, specifically with the branch of the reaction center (D1) that is responsible for primary charge separation and electron transfer. Deciphering the function of CP43 requires detailed atomic-level insights into the properties of the embedded pigments. To advance this goal, we employ a range of multiscale computational approaches to determine the site energies and excitonic profile of CP43 chlorophylls, using large all-atom models of a membrane-bound PSII monomer. In addition to time-dependent density functional theory (TD-DFT) used in the context of a quantum-mechanics/molecular-mechanics setup (QM/MM), we present a thorough analysis using the perturbed matrix method (PMM), which enables us to utilize information from long-timescale molecular dynamics simulations of native PSII-complexed CP43. The excited state energetics and excitonic couplings have both similarities and differences compared with previous experimental fits and theoretical calculations. Both static TD-DFT and dynamic PMM results indicate a layered distribution of site energies and reveal specific groups of chlorophylls that have shared contributions to low-energy excitations. Importantly, the contribution to the lowest energy exciton does not arise from the same chlorophylls at each system configuration, but rather changes as a function of conformational dynamics. An unexpected finding is the identification of a low-energy charge-transfer excited state within CP43 that involves a lumenal (C2) and the central (C10) chlorophyll of the complex. The results provide a refined basis for structure-based interpretation of spectroscopic observations and for further deciphering excitation energy transfer in oxygenic photosynthesis.