Computational studies of the O2-evolving complex of photosystem II and biomimetic oxomanganese complexes

Abstract

In recent years, there has been considerable interest in studies of catalytic metal clusters in metalloproteins based on Density Functional Theory (DFT) quantum mechanics/molecular mechanics (QM/MM) hybrid methods. These methods explicitly include the perturbational influence of the surrounding protein environment on the structural/functional properties of the catalytic centers. In conjunction with recent breakthroughs in X-ray crystallography and advances in spectroscopic and biophysical studies, computational chemists are trying to understand the structural and mechanistic properties of the oxygen-evolving complex (OEC) embedded in photosystem II (PSII). Recent studies include the development of DFT-QM/MM computational models of the Mn(4)Ca cluster, responsible for photosynthetic water oxidation, and comparative quantum mechanical studies of biomimetic oxomanganese complexes. A number of computational models, varying in oxidation and protonation states and ligation of the catalytic center by amino acid residues, water, hydroxide and chloride have been characterized along the PSII catalytic cycle of water splitting. The resulting QM/MM models are consistent with available mechanistic data, Fourier-transform infrared (FTIR) spectroscopy, X-ray diffraction data and extended X-ray absorption fine structure (EXAFS) measurements. Here, we review these computational efforts focused towards understanding the catalytic mechanism of water oxidation at the detailed molecular level.

Possible mechanisms of water splitting reaction based on proton and electron release pathways revealed for CaMn4O5 cluster of PSII refined to 1.9 Å X‐ray resolution

“…The present computational result is consistent with our previous conclusion [57]. Brudvig-Batista and their collaborators [111][112][113][114] have performed extensive QM/ MM simulations starting from the London structure [15], proposing the nucleophilic attack of hydroxide on Ca(II) to the oxyl radical Mn 4(d) (IV)¼ ¼O at the S 4 stage. Wydrzynski and his collaborators [105][106][107] and Pace et al [115,116] have also proposed the nucleophilic attack of HO-anion to the Mn¼ ¼O for the OAO bond formation.…”

A Possible Evolutionary Origin for the Mn4 Cluster in Photosystem II: From Manganese Superoxide Dismutase to Oxygen Evolving Complex

“…Oxygen evolution occurs through a "Kok cycle" of five "S-state" intermediates, S 0 through S 4 , where the subscript represents the number of oxidizing equivalents abstracted from the PSII OEC by the photoxidized chlorophyll species (Kok et al 1970) (Scheme 1). Many mechanistic models of oxygen evolution in photosystem II have been proposed (McEvoy and Brudvig 2006;Dau and Haumann 2008;Sproviero et al 2008;Liu et al 2008;Siegbahn 2008).…”

From natural to artificial photosynthesis

“…In fact, they are the only water molecules directly ligated to the metal cluster. One well-championed mechanism suggests that the substrate water, associated with Mn 4 , is deprotonated during the S-state cycle and converted into a highly electrophilic oxo (figure 5a) [36][37][38][39][40].…”

“…These studies, coupled with quantum mechanical analyses, have provided a refinement of the structure of the WOC [33][34][35] and given detailed schemes for the water-splitting chemistry leading to O -O bond formation [36][37][38][39][40][41][42][43].…”