Photosystem II (PSII) is a multisubunit pigment–protein complex that uses light-induced charge separation to power oxygenic photosynthesis. Its reaction center chromophores, where the charge transfer cascade is initiated, are arranged symmetrically along the D1 and D2 core polypeptides and comprise four chlorophyll (P D1 , P D2 , Chl D1 , Chl D2 ) and two pheophytin molecules (Pheo D1 and Pheo D2 ). Evolution favored productive electron transfer only via the D1 branch, with the precise nature of primary excitation and the factors that control asymmetric charge transfer remaining under investigation. Here we present a detailed atomistic description for both. We combine large-scale simulations of membrane-embedded PSII with high-level quantum-mechanics/molecular-mechanics (QM/MM) calculations of individual and coupled reaction center chromophores to describe reaction center excited states. We employ both range-separated time-dependent density functional theory and the recently developed domain based local pair natural orbital (DLPNO) implementation of the similarity transformed equation of motion coupled cluster theory with single and double excitations (STEOM-CCSD), the first coupled cluster QM/MM calculations of the reaction center. We find that the protein matrix is exclusively responsible for both transverse (chlorophylls versus pheophytins) and lateral (D1 versus D2 branch) excitation asymmetry, making Chl D1 the chromophore with the lowest site energy. Multipigment calculations show that the protein matrix renders the Chl D1 → Pheo D1 charge-transfer the lowest energy excitation globally within the reaction center, lower than any pigment-centered local excitation. Remarkably, no low-energy charge transfer states are located within the “special pair” P D1 –P D2 , which is therefore excluded as the site of initial charge separation in PSII. Finally, molecular dynamics simulations suggest that modulation of the electrostatic environment due to protein conformational flexibility enables direct excitation of low-lying charge transfer states by far-red light.

The ability to accurately compute low-energy excited states of chlorophylls is critically important for understanding the vital roles they play in light harvesting, energy transfer, and photosynthetic charge separation. The challenge for quantum chemical methods arises both from the intrinsic complexity of the electronic structure problem and, in the case of biological models, from the need to account for protein–pigment interactions. In this work, we report electronic structure calculations of unprecedented accuracy for the low-energy excited states in the Q and B bands of chlorophyll a . This is achieved by using the newly developed domain-based local pair natural orbital (DLPNO) implementation of the similarity transformed equation of motion coupled cluster theory with single and double excitations (STEOM-CCSD) in combination with sufficiently large and flexible basis sets. The results of our DLPNO–STEOM-CCSD calculations are compared with more approximate approaches. The results demonstrate that, in contrast to time-dependent density functional theory, the DLPNO–STEOM-CCSD method provides a balanced performance for both absorption bands. In addition to vertical excitation energies, we have calculated the vibronic spectrum for the Q and B bands through a combination of DLPNO–STEOM-CCSD and ground-state density functional theory frequency calculations. These results serve as a basis for comparison with gas-phase experiments.

Protein-embedded chromophores are responsible for light harvesting, excitation energy transfer, and charge separation in photosynthesis. A critical part of the photosynthetic apparatus are reaction centers (RCs), which comprise groups of (bacterio)chlorophyll and (bacterio)pheophytin molecules that transform the excitation energy derived from light absorption into charge separation. The lowest excitation energies of individual pigments (site energies) are key for understanding photosynthetic systems, and form a prime target for quantum chemistry. A major theoretical challenge is to accurately describe the electrochromic (Stark) shifts in site energies produced by the inhomogeneous electric field of the protein matrix. Here, we present large-scale quantum mechanics/molecular mechanics calculations of electrochromic shifts for the RC chromophores of photosystem II (PSII) using various quantum chemical methods evaluated against the domain-based local pair natural orbital (DLPNO) implementation of the similarity-transformed equation of motion coupled cluster theory with single and double excitations (STEOM-CCSD). We show that certain range-separated density functionals (ωΒ97, ωΒ97X-V, ωΒ2PLYP, and LC-BLYP) correctly reproduce RC site energy shifts with time-dependent density functional theory (TD-DFT). The popular CAM-B3LYP functional underestimates the shifts and is not recommended. Global hybrid functionals are too insensitive to the environment and should be avoided, while nonhybrid functionals are strictly nonapplicable. Among the applicable approximate coupled cluster methods, the canonical versions of CC2 and ADC(2) were found to deviate significantly from the reference results both for the description of the lowest excited state and for the electrochromic shifts. By contrast, their spin-component-scaled (SCS) and particularly the scale-opposite-spin (SOS) variants compare well with the reference DLPNO-STEOM-CCSD and the best range-separated DFT methods. The emergence of RC excitation asymmetry is discussed in terms of intrinsic and protein electrostatic potentials. In addition, we evaluate a minimal structural scaffold of PSII, the D1–D2–Cyt B559 RC complex often employed in experimental studies, and show that it would have the same site energy distribution of RC chromophores as the full PSII supercomplex, but only under the unlikely conditions that the core protein organization and cofactor arrangement remain identical to those of the intact enzyme.

Photosystem-II uses sunlight to trigger charge separation and catalyze water oxidation. Intrinsic properties of chlorophyll a pigments define a natural "red limit" of photosynthesis at � 680 nm. Nevertheless, charge separation can be triggered with far-red photons up to 800 nm, without altering the nature of lightharvesting pigments. Here we identify the electronic origin of this remarkable phenomenon using quantum chemical and multiscale simulations on a native Photosystem-II model. We find that the reaction center is preorganized for charge separation in the far-red region by specific chlorophyll-pheophytin pairs, potentially bypassing the light-harvesting apparatus. Charge transfer can occur along two distinct pathways with one and the same pheophytin acceptor (Pheo D1 ). The identity of the donor chlorophyll (Chl D1 or P D1 ) is wavelengthdependent and conformational dynamics broaden the sampling of the far-red region by the two charge-transfer states. The two pathways rationalize spectroscopic observations and underpin designed extensions of the photosynthetically active radiation limit.