The structure and activation of substrate water molecules in Sr²⁺-substituted photosystem II

Abstract

The mechanism of solar water oxidation by photosystem II (PSII) is of fundamental interest and it is the object of extensive studies both in the past and present. The solar water oxidation reaction of PSII occurs in the oxygen-evolving complex (OEC). The OEC consists of a tetranuclear manganese calcium-oxo (Mn4Ca-oxo) cluster that is surrounded by amino acid residues and inorganic cofactors. The role of the Ca(2+) ion in the water oxidation reaction is one of the most interesting questions that is yet to be answered. In this study, we probe the structural and functional differences induced by metal ion substitution in the Mn4Ca-oxo cluster by substituting the Ca(2+) ion in the OEC by a Sr(2+) ion. We apply two-dimensional (2D) hyperfine sublevel correlation (HYSCORE) spectroscopy to detect weak magnetic interactions between the paramagnetic Mn4Sr-oxo cluster and the surrounding protons in the S2 state of the OEC of Sr(2+)-substituted PSII. We identify three groups of protons that are magnetically interacting with the Mn4Sr-oxo cluster. Using the recently reported 1.9 Å resolution X-ray structure of the OEC in the S1 state [Umena et al.] and the high-resolution 2D HYSCORE spectroscopy studies of the S2 state of the OEC of Ca(2+)-containing PSII [Milikisiyants et al., Energy Environ. Sci., 2012, 5, 7747], we discuss the assignments of the three groups of protons that are magnetically coupled to the Mn4Sr-oxo cluster. Since hyperfine interactions are highly sensitive to small perturbations in the electronic and geometric structure of paramagnetic centers, a comparison of the 2D HYSCORE spectra of Sr(2+)-substituted and Ca(2+)-containing PSII allows us to draw important conclusions with respect to the structure of the substrate water molecules in the OEC and the role of the Ca(2+) ion in the water oxidation reaction. In addition, for the first time, we determine the experimental value of the spin projection factor for the Mn(III) ion of the Mn4Ca-oxo cluster as ρ1 = ±1.7 from the assignment of the hyperfine interaction of the paramagnetic cluster with the protons of the D1-His332 residue of PSII.

Proton Matrix ENDOR Studies on Ca2+-depleted and Sr2+-substituted Manganese Cluster in Photosystem II

“…The protons in the W3 and W4 molecules are in close proximity to each other, and the location of the protons in the DFT calculations is strongly dependent on the structural models employed (42,48,59,60). Lakshmi and co-workers (39,61) reported HYSCORE results of the S 2 state multiline signal, where similar proton signals to those of the proton matrix ENDOR were detected. However, the assignments of these signals are significantly different from those in the ENDOR assignments (37,39,61).…”

“…Lakshmi and co-workers (39,61) reported HYSCORE results of the S 2 state multiline signal, where similar proton signals to those of the proton matrix ENDOR were detected. However, the assignments of these signals are significantly different from those in the ENDOR assignments (37,39,61). The causes underlying these experimental differences and the assignments of these signals are unknown.…”

Computational Insights on Crystal Structures of the Oxygen-Evolving Complex of Photosystem II with Either Ca2+ or Ca2+ Substituted by Sr2+

“…The altered location of W5 upon Ca 2+ /Sr 2+ substitution might therefore be responsible for the 3-or 4-fold increase in the exchange rate of "slow" substrate water with bulk water when Sr 2+ is used to reconstitute Ca 2+ -depleted PSII 37 and for the reported differences in 2D hyperfine sublevel correlation (HYSCORE) spectra. 38,39 The new positions of W3 and W5 in Sr 2+ -substituted PSII also affect the hydrogen-bond network that connects the OEC to Y Z (reviewed in ref 40), which may account for the slower reduction of Y Z · in all S states, 41 and especially in S 3 . 42 The observed shift in the W3 position is also consistent with a recent DFT model of the Sr 2+ -OEC structure, optimized in the Mn 4 [III,III,III,III] state, 43 although our DFT-QM/MM analysis suggests that the OEC S −1 state is Mn 4 [III,IV,III,II] (Tables S1 and S2).…”

Structural Changes in the Acceptor Site of Photosystem II Upon Ca2+/Sr2+ Exchange in the Mn4CaO5 Cluster Site and the Possible Long-Range Interactions

“…1). It was reported previously that OEC perturbations by Ca 2+ /Sr 2+ exchange induces slight differences localized mainly in the OEC and nearby H- position of W3 -a water molecule binds to the Ca 2+ /Sr 2+ , which might be responsible from the O2 evolution reduction by ~60% comparing to the native PSII [2,3,12]. This is reasonable since the incorporation of Sr 2+ takes place in the OEC site and such conformational changes are expected to reduce the activity [3].…”