A Spotlight on the Compatibility between XFEL and Ab Initio Structures of the Oxygen Evolving Complex in Photosystem II

Abstract

The Mn CaO cluster of photosystem II promotes a crucial step in the oxygenic photosynthesis, namely, the water-splitting reaction. The structure of such cluster in the S state of the Kok-Joliot's cycle has been recently resolved by femtosecond X-ray free-electron laser (XFEL) measurements. However, the XFEL results are characterized by appreciable discrepancies with previous X-ray diffraction (XRD), as well as with S models based on ab initio calculations. We provide here a unifying picture based on a combined set of DFT-based structures and molecular dynamics simulations of the S and S states. Our findings indicate that the XFEL results cannot be interpreted on the grounds of a single structure. A combination of two S stable isomers together with a minority contribution of the S state is necessary to reproduce XFEL results within 0.16 Å.

Explaining the Different Geometries of the Water Oxidising Complex in the Nominal S3 State Crystal Structures of Photosystem II at 2.25 Å and 2.35 Å

“…As noted above, with the 1.9 Å structure, these discrepancies were initially attributed to X‐ray ‘photo‐reduction’ during XRD data collection (subsequently argued against,) . The appearance of the 1.95 Å structure made photo‐reduction untenable and it was then proposed that this structure must contain a mixture of S 1 and S 0 species,– although specific precautions were taken by Suga et al. to avoid this …”

On the comparison between differential vibrational spectroscopy spectra and theoretical data in the carboxyl region of photosystem II

“…Additionally, the 10 water molecules closest to the cluster and the chloride anion close to Glu333 were also treated at DFT level. For all the S 1 state models, we used oxidation states (III, IV, IV, III) and ↑↓↑↓ spin configuration (Narzi et al ). For the S 2 state, we simulated the open cubane conformer (named S) proposed by Patanzis et al as the most stable one (Pantazis et al , Bovi et al ) with oxidation and spin state in agreement with the EPR results [(III, IV, IV, IV) ↑↓↓↑].…”

“…The catalytic process is divided in five steps (from S 0 to S 4 ), which have been largely studied by several spectroscopic techniques, such as extended X‐ray absorption fine structure (Robblee et al , Yano et al , Dau et al , Pushkar et al , Kusunoki , Li et al ), X‐ray crystallography (Zouni et al , Loll et al , Guskov et al , Umena et al , Suga et al , , Kern et al , ) and electron paramagnetic resonance (EPR) (Boussac et al , Sjöholm et al , Lohmiller et al , Boussac et al ). Additionally, in the last years, several theoretical studies have been carried out with the aim to interpret and rationalizing the huge amount of experimental data and ultimately to shed light on the catalytic mechanism of PSII (Ames et al , Isobe et al , Siegbahn , , Askerka et al , , Capone et al , , Narzi et al , ). A detailed characterization of the structural, electronic and magnetic features for each step of the Kok‐Joliot's cycle would represent an important source of inspiration for developing new efficient artificial devices performing the water splitting reaction (Nocera , Faunce et al ).…”

Tracing the Pathways of Waters and Protons in Photosystem II and Cytochrome c Oxidase

“…S 3 [38] is primed for reaction. The growing agreement about the structure of this state comes from a dialog between QM/MM simulation and XFEL experiment [20,22,30,[39][40][41]. In the S 3 state, a new water (or hydroxyl) is added.…”