TY - JOUR
T1 - Theoretical evaluation of structural models of the S2 state in the oxygen evolving complex of photosystem II
T2 - protonation states and magnetic interactions
AU - Ames, William
AU - Pantazis, Dimitrios A.
AU - Krewald, Vera
AU - Cox, Nicholas
AU - Messinger, Johannes
AU - Lubitz, Wolfgang
AU - Neese, Frank
PY - 2011/12/14
Y1 - 2011/12/14
N2 - Protonation states of water ligands and oxo bridges are intimately involved in tuning the electronic structures and oxidation potentials of the oxygen evolving complex (OEC) in Photosystem II, steering the mechanistic pathway, which involves at least five redox state intermediates S n (n = 0-4) resulting in the oxidation of water to molecular oxygen. Although protons are practically invisible in protein crystallography, their effects on the electronic structure and magnetic properties of metal active sites can be probed using spectroscopy. With the twin purpose of aiding the interpretation of the complex electron paramagnetic resonance (EPR) spectroscopic data of the OEC and of improving the view of the cluster at the atomic level, a complete set of protonation configurations for the S 2 state of the OEC were investigated, and their distinctive effects on magnetic properties of the cluster were evaluated. The most recent X-ray structure of Photosystem II at 1.9 Å resolution was used and refined to obtain the optimum structure for the Mn 4O 5Ca core within the protein pocket. Employing this model, a set of 26 structures was constructed that tested various protonation scenarios of the water ligands and oxo bridges. Our results suggest that one of the two water molecules that are proposed to coordinate the outer Mn ion (Mn A) of the cluster is deprotonated in the S 2 state, as this leads to optimal experimental agreement, reproducing the correct ground state spin multiplicity (S = 1/2), spin expectation values, and EXAFS-derived metal-metal distances. Deprotonation of Ca 2+-bound water molecules is strongly disfavored in the S 2 state, but dissociation of one of the two water ligands appears to be facile. The computed isotropic hyperfine couplings presented here allow distinctions between models to be made and call into question the assumption that the largest coupling is always attributable to Mn III. The present results impose limits for the total charge and the proton configuration of the OEC in the S 2 state, with implications for the cascade of events in the Kok cycle and for the water splitting mechanism.
AB - Protonation states of water ligands and oxo bridges are intimately involved in tuning the electronic structures and oxidation potentials of the oxygen evolving complex (OEC) in Photosystem II, steering the mechanistic pathway, which involves at least five redox state intermediates S n (n = 0-4) resulting in the oxidation of water to molecular oxygen. Although protons are practically invisible in protein crystallography, their effects on the electronic structure and magnetic properties of metal active sites can be probed using spectroscopy. With the twin purpose of aiding the interpretation of the complex electron paramagnetic resonance (EPR) spectroscopic data of the OEC and of improving the view of the cluster at the atomic level, a complete set of protonation configurations for the S 2 state of the OEC were investigated, and their distinctive effects on magnetic properties of the cluster were evaluated. The most recent X-ray structure of Photosystem II at 1.9 Å resolution was used and refined to obtain the optimum structure for the Mn 4O 5Ca core within the protein pocket. Employing this model, a set of 26 structures was constructed that tested various protonation scenarios of the water ligands and oxo bridges. Our results suggest that one of the two water molecules that are proposed to coordinate the outer Mn ion (Mn A) of the cluster is deprotonated in the S 2 state, as this leads to optimal experimental agreement, reproducing the correct ground state spin multiplicity (S = 1/2), spin expectation values, and EXAFS-derived metal-metal distances. Deprotonation of Ca 2+-bound water molecules is strongly disfavored in the S 2 state, but dissociation of one of the two water ligands appears to be facile. The computed isotropic hyperfine couplings presented here allow distinctions between models to be made and call into question the assumption that the largest coupling is always attributable to Mn III. The present results impose limits for the total charge and the proton configuration of the OEC in the S 2 state, with implications for the cascade of events in the Kok cycle and for the water splitting mechanism.
UR - http://www.scopus.com/inward/record.url?scp=83055161471&partnerID=8YFLogxK
UR - http://dx.doi.org/10.1021/ja2041805
U2 - 10.1021/ja2041805
DO - 10.1021/ja2041805
M3 - Article
C2 - 22092013
AN - SCOPUS:83055161471
SN - 0002-7863
VL - 133
SP - 19743
EP - 19757
JO - Journal of the American Chemical Society
JF - Journal of the American Chemical Society
IS - 49
ER -
