Comprehensive Evaluation of Models for Ammonia Binding to the Oxygen Evolving Complex of Photosystem II

The identity and
insertion pathway of the substrate oxygen atoms
that are coupled to dioxygen by the oxygen-evolving complex (OEC)
remains a central question toward understanding Nature’s water
oxidation mechanism. In several studies, ammonia has been used as
a small “water analogue” to elucidate the pathway of
substrate access to the OEC and to aid in determining which of the
oxygen ligands of the tetramanganese cluster are substrates for O–O
bond formation. On the basis of structural and spectroscopic investigations,
five first-sphere binding modes of ammonia have been suggested, involving
either substitution of an existing H2O/OH–/O2– group or addition as an extra ligand to a
metal ion of the Mn4CaO5 cluster. Some of these
modes, specifically the ones involving substitution, have already
been subject to spectroscopy-oriented quantum chemical investigations,
whereas more recent suggestions that postulate the addition of ammonia
have not been examined so far with quantum chemistry for their agreement
with spectroscopic data. Herein, we use a common structural framework
and theoretical methodology to evaluate structural models of the OEC
that represent all proposed modes of first-sphere ammonia interaction
with the OEC in its S2 state. Criteria include energetic,
magnetic, kinetic, and spectroscopic properties compared against available
experimental EPR, ENDOR, ESEEM, and EDNMR data. Our results show that
models featuring ammonia replacing one of the two terminal water ligands
on Mn4 align best with experimental data, while they definitively
exclude substitution of a bridging μ-oxo ligand as well as incorporation
of ammonia as a sixth ligand on Mn1 or Mn4.