Structure, ligands and substrate coordination of the oxygen-evolving complex of photosystem II in the S2 state: a combined EPR and DFT study

Abstract

The S2 state of the oxygen-evolving complex of photosystem II, which consists of a Mn4O5Ca cofactor, is EPR-active, typically displaying a multiline signal, which arises from a ground spin state of total spin ST = 1/2. The precise appearance of the signal varies amongst different photosynthetic species, preparation and solvent conditions/compositions. Over the past five years, using the model species Thermosynechococcus elongatus, we have examined modifications that induce changes in the multiline signal, i.e. Ca(2+)/Sr(2+)-substitution and the binding of ammonia, to ascertain how structural perturbations of the cluster are reflected in its magnetic/electronic properties. This refined analysis, which now includes high-field (W-band) data, demonstrates that the electronic structure of the S2 state is essentially invariant to these modifications. This assessment is based on spectroscopies that examine the metal centres themselves (EPR, (55)Mn-ENDOR) and their first coordination sphere ligands ((14)N/(15)N- and (17)O-ESEEM, -HYSCORE and -EDNMR). In addition, extended quantum mechanical models from broken-symmetry DFT now reproduce all EPR, (55)Mn and (14)N experimental magnetic observables, with the inclusion of second coordination sphere ligands being crucial for accurately describing the interaction of NH3 with the Mn tetramer. These results support a mechanism of multiline heterogeneity reported for species differences and the effect of methanol [Biochim. Biophys. Acta, Bioenerg., 2011, 1807, 829], involving small changes in the magnetic connectivity of the solvent accessible outer MnA4 to the cuboidal unit Mn3O3Ca, resulting in predictable changes of the measured effective (55)Mn hyperfine tensors. Sr(2+) and NH3 replacement both affect the observed (17)O-EDNMR signal envelope supporting the assignment of O5 as the exchangeable μ-oxo bridge and it acting as the first site of substrate inclusion.

Artificial photosynthesis: understanding water splitting in nature

“…This hypothesis comes from correlation to MIMS results which show that Ca 2þ /Sr 2þ replacement perturbs the rate at which W s exchanges with bulk water [38,67,74]. As Ca 2þ /Sr 2þ replacement similarly affects the electronic properties of O5 (but no other exchangeable oxygen ligand) [57], this result can again be easily understood. We note that the fast rate of exchange of O5 when compared with that of m-oxo bridges in simple synthetic model systems is likely due to the unusual flexibility of its metal coordination (figures 4-6) [52,53].…”

“…W1 displacement as opposed to other binding modes (m-oxo bridge displacement) is also preferred based on energetic considerations and an analysis of available vibrational data [71][72][73]. In samples where NH 3 is added, the hyperfine coupling of the exchangeable m-oxo bridge is strongly perturbed (ca 30%) [57,72]. This result is readily understood as due to a trans effect: the W1 ligand is trans to the O5 bridge.…”

QM/MM study of the S2 to S3 transition reaction in the oxygen-evolving complex of photosystem II

“…have examined the electronic structures of S2 and S3 based on their QM models, and they suggested cluster structures and protonation states in comparison to the electron paramagnetic resonance (EPR) results [11][12][13]. We have performed quantum mechanics/molecular mechanics (QM/MM) calculations to elucidate the hydrogen-bonding networks in the PSII-OEC [14,15].…”

Structural Analysis of High-Spin States of S0-S4 at OEC Complex: A Theoretical Approach of Small Models

“…However, there are several variables to be considered in this disagreement between experimental and theoretical data. The protonation state of oxygen atoms in OEC, 6,34 the number of water molecules surrounding OEC 23,[35][36][37] and the oxidation and spin state of manganese atoms 38,39 are the main issues. In the models studied here all these structural details were considered.…”

“…5,6,36 It is mainly explained by the μ-oxobridge MnD1---O5---MnA4 that is high sensitive to oxidation and spin state of manganese atoms as reported in literature. 13,14,[36][37][38]40,41 The standard structural deviations (σ) observed between HS regarding experimental structure is around 10.0% (see Table S2, Supplementary Information section).The HS calculated models were also compared to reference structure (Ref) of structural parameters. The bigger percentage deviation from Ref structure was for MnA4−O4 parameter, −9.1% for S2-HS.…”