Electronic Structural Changes of Mn in the Oxygen-Evolving Complex of Photosystem II during the Catalytic Cycle

Abstract

The oxygen evolving complex (OEC) in Photosystem II (PS II) was studied in the S0 through S3 states using 1s2p direct resonant inelastic X-ray scattering (RIXS) spectroscopy. The spectral changes of the OEC during the S-state transitions are subtle, indicating that the electrons are strongly delocalized throughout the cluster. The result suggests that in addition to the Mn ions ligands are also playing an important role in the redox reactions. A series of MnIV coordination complexes with different protonation states, nuclearity, and with and without the presence of Ca were compared, particularly with the PS II S3 state spectrum to understand its oxidation state. We find strong variations of the electronic structure within the series of MnIV model systems. The spectrum of the S3 state best resembles the MnIV complexes, Mn3IVCa2 and saplnMn2IV(OH)2, i.e. the oxo-bridge protonation of Mn dimer complexes and the presence of Ca in one corner of a Mn cubane structure show a similar spectroscopic response, suggesting that Ca in PS II and protonation of the oxo-bridge may give rise to analogous modifications of the electronic structure at the Mn sites. The current result emphasizes that the assignment of formal oxidation states alone is not sufficient for understanding the detailed electronic structural changes that govern the catalytic reaction in the OEC.

X-ray Emission Spectroscopy as an in Situ Diagnostic Tool for X-ray Crystallography of Metalloproteins Using an X-ray Free-Electron Laser

“…35 However, for PS II, RIXS experiments have demonstrated that the electron density is delocalized throughout the cluster compared to model complexes. 22, 40 This illustrates the need to go beyond the simple representation of formal oxidation states to explain the differences in first moments observed between model complexes and PS II, but this discussion is beyond the scope of this study.…”

Structural changes correlated with magnetic spin state isomorphism in the S2 state of the Mn4CaO5 cluster in the oxygen-evolving complex of photosystem II

“…However, formal oxidation states does not necessarily coincide with effective number of electrons in the metal valence shells because of important factors like metal–ligand covalency 13,14. A recent resonant inelastic X-ray scattering spectroscopy (RIXS) study indicate increasing delocalization of positive charge on to the ligands during the S-state transitions 15. Among the S-states, the S 2 state is the most studied state due to the presence of rich EPR signals and nearly 100% conversion by illumination starting from the dark stable S 1 state.…”

Metalloprotein structures at ambient conditions and in real-time: biological crystallography and spectroscopy using X-ray free electron lasers

“…One step further would be the collection of L-edge resonant inelastic X-ray scattering data (RIXS), where one can map the energy levels and occupation of the valence orbitals. At present only K-edge RIXS studies have been conducted on metalloenzymes [57,58], but a first demonstration experiment at LCLS showed that it is possible to collect time resolved L-edge RIXS on a solution of an Fe compound in the ~100s mM concentration range [59]. …”