The first tyrosyl radical intermediate formed in the S2–S3 transition of photosystem II

Abstract

The EPR "split signals" represent key intermediates of the S-state cycle where the redox active D1-Tyr161 (YZ) has been oxidized by the reaction center of the photosystem II enzyme to its tyrosyl radical form, but the successive oxidation of the Mn4CaO5 cluster has not yet occurred (SiYZ˙). Here we focus on the S2YZ˙ state, which is formed en route to the final metastable state of the catalyst, the S3 state, the state which immediately precedes O-O bond formation. Quantum chemical calculations demonstrate that both isomeric forms of the S2 state, the open and closed cubane isomers, can form states with an oxidized YZ˙ residue without prior deprotonation of the Mn4CaO5 cluster. The two forms are expected to lie close in energy and retain the electronic structure and magnetic topology of the corresponding S2 state of the inorganic core. As expected, tyrosine oxidation results in a proton shift towards His190. Analysis of the electronic rearrangements that occur upon formation of the tyrosyl radical suggests that a likely next step in the catalytic cycle is the deprotonation of a terminal water ligand (W1) of the Mn4CaO5 cluster. Diamagnetic metal ion substitution is used in our calculations to obtain the molecular g-tensor of YZ˙. It is known that the gx value is a sensitive probe not only of the extent of the proton shift between the tyrosine-histidine pair, but also of the polarization environment of the tyrosine, especially about the phenolic oxygen. It is shown for PSII that this environment is determined by the Ca(2+) ion, which locates two water molecules about the phenoxyl oxygen, indirectly modulating the oxidation potential of YZ.

Strong Coupling between the Hydrogen Bonding Environment and Redox Chemistry during the S2 to S3 Transition in the Oxygen-Evolving Complex of Photosystem II

“…The structural and electronic features of S 2 Y Z •+ are intimately related to those of the precursor S 2 state because of weak magnetic interaction between the Mn 4 CaO 5 core and Tyr Z •+ . 39 Assuming that the oxidation state of the inorganic cluster is Mn IV 3 Mn III in the S 2 Y Z •+ state, the structural relaxation results in a shift of the central μ-oxo bridge (O5) toward either Mn A or Mn D with the IV oxidation state, forming a Mn IV −O bond and leaving behind a unique five-coordinate Mn D or Mn A site with the III oxidation state. This bifurcation gives rise to structural and redox isomers: an open cubane with an oxidation state of (4443) and a closed cubane with an oxidation state of (3444) in Figure 1 •+ and a closed cubane structure B with 5(7) {↓↑↑↑···↓(↑)} in S 2 (closed)Y Z •+ are separated by a barrier of about 14 kcal mol −1 , with the former being 1.3 kcal mol −1 more stable than the latter.…”

Removal of Ca2+ from the Oxygen-Evolving Complex in Photosystem II Has Minimal Effect on the Mn4O5 Core Structure: A Polarized Mn X-ray Absorption Spectroscopy Study

“…(iii) A crucial role of the Ca 2+ ion in proton-coupled electron transfer from the OEC to the Y Z • residue is strongly supported by recent studies. 52,53,74,76 (iv) A direct adverse effect of Ca 2+ depletion on the oxidation of Mn D1 during the S 2 ′-to-S 3 ′ transition has recently been put forward in theoretical studies. 75,76 (v) Experimental 45,82,84 and computational 85 evidence that the first (early binding), slowly exchanging substrate is O5 suggests that the Lewis acidity of the Ca 2+ ion may also be critical for providing the specific electropositive environment for this ligand discussed above.…”

“…26,49 (iii) The fact that Sr 2+ is the only metal ion able to functionally replace Ca 2+41,50,51 leads to the conclusion that their property as strong Lewis acids with similar electronegativities, giving rise to similar p K a values of H 2 O ligands, may be critical for substrate deprotonation during catalysis 52 and (iv) proton-coupled electron transfer from the OEC to Y Z • . 52,53 …”

Artificial photosynthesis: understanding water splitting in nature

“…These are listed below with reference to design criteria for the development of biomimetic and bioinspired water splitting catalysts using manganese. also may act to tune the redox/magnetic properties of the cuboidal (Mn 3 Ca) unit [83], or of the tyrosine radical [36] or both. The inclusion of calcium has been correlated with enhanced water splitting activity of manganese oxide water oxidation catalysts [82,84].…”