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 (ChlD1) 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.