Assigning the Low-Energy Excitons in Far-Red Photosystem II through Atomistic Modeling

Abstract

Far-red light photoacclimation of cyanobacteria extends the spectral range of oxygenic photosynthesis through the incorporation of chlorophylls (Chls) d and f into natural photosystems, but the energetic organization of these pigments remains poorly understood. Here, we combine electronic-structure calculations with atomistic QM/MM and polarizable QM/MM approaches to determine the site energies, electronic couplings, and excitonic structure of the far-red PSII from Synechococcus sp. PCC 7335. In particular, we use benchmark calculations against spin-component-scaled CC2 to assess the accuracy of long-range corrected density functionals for describing the relative energetics of Chls a, d, and f. Our calculations reveal that the energetic tuning of the far-red pigments is governed primarily by protein electrostatics, whereas structural distortions and environmental polarization make comparatively minor contributions. We find significant excitonic interactions within the subset of CP47 chlorophylls, while the reaction-center Chl d remains largely localized. The resulting excitonic Hamiltonian quantitatively reproduces both the far-red absorption spectrum and the sequence of exciton energies extracted from two-dimensional electronic spectroscopy, enabling a first-principles assignment of the low-energy excitons to specific Chl f and Chl d pigments. These results provide an atomistic picture of the far-red excitonic landscape and establish a quantitative basis for future simulations of excitation energy transfer and charge separation in far-red photosystems.