Reaction Center Excitation in Photosystem II: From Multiscale Modeling to Functional Principles

[Image: see text] Oxygenic photosynthesis is the fundamental energy-converting process that utilizes sunlight to generate molecular oxygen and the organic compounds that sustain life. Protein–pigment complexes harvest light and transfer excitation energy to specialized pigment assemblies, reaction centers (RC), where electron transfer cascades are initiated. A molecular-level understanding of the primary events is indispensable for elucidating the principles of natural photosynthesis and enabling development of bioinspired technologies. The primary enzyme in oxygenic photosynthesis is Photosystem II (PSII), a membrane-embedded multisubunit complex, that catalyzes the light-driven oxidation of water. The RC of PSII consists of four chlorophyll a and two pheophytin a pigments symmetrically arranged along two core polypeptides; only one branch participates in electron transfer. Despite decades of research, fundamental questions remain, including the origin of this functional asymmetry, the nature of primary charge-transfer states and the identity of the initial electron donor, the origin of the capability of PSII to enact charge separation with far-red photons, i.e., beyond the “red limit” where individual chlorophylls absorb, and the role of protein conformational dynamics in modulating charge-separation pathways. In this Account, we highlight developments in quantum-chemistry based excited-state computations for multipigment assemblies and the refinement of protocols for computing protein-induced electrochromic shifts and charge-transfer excitations calibrated with modern local correlation coupled cluster methods. We emphasize the importance of multiscale atomistic quantum-mechanics/molecular-mechanics and large-scale molecular dynamics simulations, which enabled direct and accurate modeling of primary processes in RC excitation at the quantum mechanical level. Our findings show how differential protein electrostatics enable spectral tuning of RC pigments and generate functional asymmetry in PSII. A chlorophyll pigment on the active branch (Chl(D1)) has the lowest site energy in PSII and is the primary electron donor. The complete absence of low-lying charge-transfer states within the central pair of chlorophylls excludes a long-held assumption about the initial charge separation. Instead, we identify two primary charge separation pathways, both with the same pheophytin acceptor (Pheo(D1)): a fast pathway with Chl(D1) as the primary electron donor (short-range charge-separation) and a slow pathway with P(D1)P(D2) as the initial donor (long-range charge separation). The low-energy spectrum is dominated by two states with significant charge-transfer character, Chl(D1)(δ+)Pheo(D1)(δ−) and P(D1)(δ+)Pheo(D1)(δ−). The conformational dynamics of PSII allows these charge-transfer states to span wide energy ranges, pushing oxygenic photosynthesis beyond the “red limit”. These results provide a quantum mechanical picture of the primary events in the RC of oxygenic photosynthesis, forming a solid basis for interpreting experimental observations and for extending photosynthesis research in new directions.