Heterogeneous Composition of Oxygen-Evolving Complexes in Crystal Structures of Dark-Adapted Photosystem II

Abstract

Photosystem II (PSII) is a homodimeric protein complex that catalyzes water oxidation at the oxygen-evolving complex (OEC), a heterocubanoid calcium−tetramanganese cluster. Here, we analyze the omit electron density peaks of the OEC's metal ions in five X-ray free-electron laser PSII structures at resolutions between 2.15 and 1.95 Å. The omit peaks can be described by the total number of electrons and approximated by the variance of electron density distribution when the distributions are spherically symmetric. We show that the number of electrons of metal centers is different in the two OECs of PSII dimers, implying that the oxidation states and/or occupancies of individual metal ions are different in the two monomers. In either case, we find that the two OECs of dark-adapted PSII dimers in crystals are not fully synchronized in the S 1 state. Differences in redox states of the OEC in PSII only partially account for the observation that the electron densities integrate to a smaller number of electrons than expected. Differences between the determined and expected relative electron numbers are much larger than the estimated errors, indicating heterogeneity in the OEC composition.

High-resolution cryo-electron microscopy structure of photosystem II from the mesophilic cyanobacterium, Synechocystis sp. PCC 6803

“…The map ambiguity is most likely a consequence of the C terminus being flexible, found in different orientations within individual particles used to create the ensemble cryo-EM map. It is unclear whether this flexibility is an intrinsic characteristic of Synechocystis 6803 PSII or whether it is a result of isolation procedures or experimental conditions as discussed recently ( 37 ). Kato et al.…”

Proteomic analysis demonstrates that Bidens pilosa root exudates differentially impact Pteris multifida gametophyte growth

“…Importantly, the data show the potential structural domains impacted by undecane-induced toxicity. The oxygen-evolving complex in the PsbP of Photosystem II was signi cantly downregulated; this system has two critical roles: electron denotation to P680 + and the release of oxygen molecules (Wang et al, 2021a).…”

Probing the proton release by Photosystem II in the S1 to S2 high-spin transition

“…19.476895 doi: bioRxiv preprint O5. After a further refinement of the electron density maps some works could indicate an heterogeneity in the valence of Mn ions between the two PSII monomers and/or show a lower than expected oxidation state of some Mn ions [15][16][17]. However, other groups [18][19][20] do not share such a conclusion mainly by taking into account the Jahn-Teller effect on the orientation of the bondings of the Mn III .…”

“…The Mn 4 CaO 5 structure resemble a distorted chair including a μ-oxo-bridged cuboidal Mn 3 O 4 Ca unit with a fourth Mn attached to this core structure via two μ-oxo bridges involving the two oxygen’s O4 and O5. After further refinement of the electron density maps, some works could indicate an heterogeneity in the valence of Mn ions between the two PSII monomers and/or could show a lower than expected oxidation state of some Mn ions [15–17]. However, other groups [18–20] do not share such a conclusion mainly by taking into account the Jahn–Teller effect on the orientation of the bondings of the Mn III .…”