Kα X-ray Emission Spectroscopy on the Photosynthetic Oxygen-Evolving Complex Supports Manganese Oxidation and Water Binding in the S₃ State

Abstract

The unique manganese-calcium catalyst in photosystem II (PSII) is the natural paragon for efficient light-driven water oxidation to yield O. The oxygen-evolving complex (OEC) in the dark-stable state (S) comprises a MnCaO core with five metal-bound water species. Binding and modification of the water molecules that are substrates of the water-oxidation reaction is mechanistically crucial but controversially debated. Two recent crystal structures of the OEC in its highest oxidation state (S) show either a vacant Mn coordination site or a bound peroxide species. For purified PSII at room temperature, we collected Mn Kα X-ray emission spectra of the S, S, S, and S intermediates in the OEC cycle, which were analyzed by comparison to synthetic Mn compounds, spectral simulations, and OEC models from density functional theory. Our results contrast both crystallographic structures. They indicate Mn oxidation in three S-transitions and suggest additional water binding at a previously open Mn coordination site. These findings exclude Mn reduction and render peroxide formation in S unlikely.

The S3 State of the Oxygen-Evolving Complex: Overview of Spectroscopy and XFEL Crystallography with a Critical Evaluation of Early-Onset Models for O–O Bond Formation

“…This type of structure with an oxo bridge between Mn3 and Mn4 and a terminal OH group on Mn1, in combination with its lower S i -state analogues, has been shown with time-dependent DFT calculations to reproduce successfully the measured Mn K-pre-edge X-ray absorption spectra of the OEC [30,56]. It is also consistent with Mn Kα X-ray emission spectroscopy that supports Mn oxidation in all three S 0 -S 1 , S 1 -S 2 , and S 2 -S 3 transitions along with binding of an additional water-derived ligand in the S 3 state at a previously open Mn coordination site [62].…”

“…Although in principle they are less sensitive to valence changes, they are an order of magnitude more intense than the Kβ1,3 line, enabling better XES signal quality. Schuth et al [62] reported room temperature Kα1 spectra of PSII in the S0, S1, S2, and S3 states and, by comparison of the data with model compounds in varying Mn oxidation states, they could reach the conclusion that Kα XES is consistent with the other XES results, supporting Mn oxidations in all transitions up to an all-Mn(IV) S3 state that likely features binding of an additional water ligand [62]. .…”

“…In terms of X-ray emission spectroscopy, Schuth et al [62] presented a comparison against experiment of S 3 minus S 1 Kα difference spectra, obtained from multiple-scattering theory calculations, for various DFT models of the S 3 state (Figure 9). Among the S 3 structural models tested was a structure that contained an O-O bond between atoms O5 and O6 in the form of hydroperoxide, with the two terminal Mn ions in the +III oxidation state (model labeled S 3 b in Figure 9).…”

“…Right: DFT models of the S 1 and the S 3 states used in the simulations: S 3 a assumes no extra ligand binding, S 3 b contains a hydroperoxide, and S 3 c assumes water binding at Mn1. Figures adapted with permission from Schuth et al[62]. Copyright 2018 American Chemical Society.…”

S = 3 Ground State for a Tetranuclear MnIV4O4 Complex Mimicking the S3 State of the Oxygen-Evolving Complex

“…[24][25][26][27][28][29][30][31][32][33][34][35][36][37][38] On the basis of EPR, MCD, and X-ray spectroscopic studies, the electronic structure of the S 3 state has been assigned to a homovalent Mn IV 4 core with an S = 3 spin ground state. 5,[39][40][41] Two structural isomers S 3 A (dimer-ofdimers) and S 3 B (trimer-monomer), both with S = 3 spin ground states, have been invoked for the S 3 state ( Figure 1a). 5,42 A similar structural isomerism has been proposed for the S 2 state.…”