Convergence of QM/MM and Cluster Models for the Spectroscopic Properties of the Oxygen-Evolving Complex in Photosystem II

The latest crystal structure of photosystem II at 1.9 Å resolution, which resolves the topology of the Mn4CaO5 oxygen evolving complex (OEC) at atomistic detail, enables a better correlation between structural features and spectroscopic properties than ever before. Building on the refined crystallographic model of the OEC and the protein, we present combined quantum mechanical/molecular mechanical (QM/MM) studies of the spectroscopic properties of the natural catalyst embedded in the protein matrix. Focusing on the S2 state of the catalytic cycle, we examine the convergence of not only structural parameters but also of the intracluster magnetic interactions in terms of exchange coupling constants and of experimentally relevant 55Mn, 17O, and 14N hyperfine coupling constants with respect to QM/MM partitioning using five QM regions of increasing size. This enables us to assess the performance of the method and to probe second sphere effects by identifying amino acid residues that principally affect the spectroscopic properties of the OEC. Comparison between QM-only and QM/MM treatments reveals that whereas QM/MM models converge quickly to stable values, the QM cluster models need to incorporate significantly larger parts of the second coordination sphere and surrounding water molecules to achieve convergence for certain properties. This is mainly due to the sensitivity of the QM-only models to fluctuations in the hydrogen bonding network and ligand acidity. Additionally, a hydrogen bond that is typically omitted in QM-only treatments is shown to determine the hyperfine coupling tensor of the unique Mn(III) ion by regulating the rotation plane of the ligated D1-His332 imidazole ring, the only N-donor ligand of the OEC