Combined Multireference-Multiscale Approach to the Description of Photosynthetic Reaction Centers.

A first-principles description of the primary photochemical processes that drive photosynthesis and sustain life on our planet remains one of the grand challenges of modern science. Recent research established that explicit incorporation of protein electrostatics in excited-state calculations of photosynthetic pigments, achieved for example with quantum-mechanics/molecular-mechanics (QM/MM) approaches, is essential for a meaningful description of the properties and function of pigment-protein complexes. Although time-dependent density functional theory has been used productively so far in QM/MM approaches for the study of such systems, this methodology has limitations. Here we pursue for the first time a QM/MM description of the reaction center in the principal enzyme of oxygenic photosynthesis, Photosystem II, using multireference wave function theory for the high-level QM region. We identify best practices and establish guidelines regarding the rational choice of active space and appropriate state-averaging for the efficient and reliable use of complete active space self-consistent field (CASSCF) and the N-electron valence state perturbation theory (NEVPT2) in the prediction of low-lying excited states of chlorophyll and pheophytin pigments. Given that the Gouterman orbitals are inadequate as a minimal active space, we define specific minimal and extended active spaces for the NEVPT2 description of electronic states that fall within the Q and B bands. Subsequently, we apply our multireference-QM/MM protocol to the description of all pigments in the reaction center of Photosystem II. The calculations reproduce the electrochromic shifts induced by the protein matrix and the ordering of site energies consistent with the identity of the primary donor (Chl) and the experimentally known asymmetric and directional electron transfer. The optimized protocol sets the stage for future multireference treatments of multiple pigments, and hence for multireference studies of charge separation, while it is transferable to the study of any photoactive embedded tetrapyrrole system.