Molecular Principles of Redox-Coupled Protonation Dynamics in Photosystem II

Abstract

Photosystem II (PSII) catalyzes light-driven water oxidization, releasing O 2 into the atmosphere and transferring the electrons for the synthesis of biomass. However, despite decades of structural and functional studies, the water oxidation mechanism of PSII has remained puzzling and a major challenge for modern chemical research. Here, we show that PSII catalyzes redox-triggered proton transfer between its oxygen-evolving Mn 4 O 5 Ca cluster and a nearby cluster of conserved buried ion-pairs, which are connected to the bulk solvent via a proton pathway. By using multi-scale quantum and classical simulations, we find that oxidation of a redox-active Tyr z (Tyr161) lowers the reaction barrier for the water-mediated proton transfer from a Ca 2+ -bound water molecule (W3) to Asp61 via conformational changes in a nearby ion-pair (Asp61/Lys317). Deprotonation of this W3 substrate water triggers its migration toward Mn1 to a position identified in recent X-ray free-electron laser (XFEL) experiments [Ibrahim et al. Proc. Natl. Acad. Sci. USA 2020, 117, 12,624–12,635]. Further oxidation of the Mn 4 O 5 Ca cluster lowers the proton transfer barrier through the water ligand sphere of the Mn 4 O 5 Ca cluster to Asp61 via a similar ion-pair dissociation process, while the resulting Mn-bound oxo/oxyl species leads to O 2 formation by a radical coupling mechanism. The proposed redox-coupled protonation mechanism shows a striking resemblance to functional motifs in other enzymes involved in biological energy conversion, with an interplay between hydration changes, ion-pair dynamics, and electric fields that modulate the catalytic barriers.

Peroxy Intermediate Drives Carbon Bond Activation in the Dioxygenase AsqJ

“…Although the present O 2 end -on configuration differs from the typical side -on coordination in Ni-O 2 complexes of other dioxygenases, the proposed O 2 – splitting process resembles a Criegee rearrangement in non-heme iron intradiol dioxygenases, as well as an alkylperoxo-intermediate observed in extradiol-ring cleaving dioxygenases . Moreover, similar peroxo-intermediates have been proposed for O–O bond splitting in oxidoreductases like cytochrome c oxidase or apocarotenoid oxygenase (see Figure S10 for comparison to AsqJ), as well as in enzymatic and molecular H 2 O-splitting catalysts, such as photosystem II , and Ru-catalysts, respectively.…”

Roles of the Flexible Primary Coordination Sphere of the Mn4CaOx Cluster: What Are the Immediate Decay Products of the S3 State?

“…Structural elucidation and mechanistic investigations over the past decade have made remarkable progress in understanding the underlying chemical principles of water oxidation occurring in the OEC. − A tight coupling of the Kok–Joliot cycle with ligand acid–base chemistry and metal valence/structural isomerism has been found to be crucial for the highly regulated progression of a S i state to a higher oxidation state ( S i +1 ). For example, an extended, seven-step catalytic cycle has been proposed in which ligand deprotonation and metal oxidation events are strictly alternating to prevent a significant increase of the redox potential of the Mn cluster. , At least two isomers with different spin states are likely to be involved in the S 1 , S 2 , and S 3 states, − . − Two S 1 isomers ( g = 4.8 and 12 in parallel mode) observed by electron paramagnetic resonance (EPR) spectroscopy − may differ in a crucial electronic structure feature that is relevant for catalytic progression to the next S 2 state .…”

“…The redox isomerism in H + -depleted S 2 state results in either Mn oxidation state (4443) for the open cubane ( S 2 Y Z • ) or (4444) for the closed cubane ( S 3 Y Z ) . The cluster can, therefore, pick up a new water molecule at either Mn D III of the open cubane or Mn A IV of the closed cubane, leading to two mutually exclusive propositions: water binding first (open cubane) ,, and Mn oxidation first (closed cubane) ,, mechanisms for the S 2 to S 3 transition. Because of its mechanistic significance, we set out to perform a detailed mechanistic study using broken-symmetry (BS) density functional theory (DFT) followed by the generalized spin projection technique, , with an aim of comprehending the functional roles of the flexible primary coordination sphere in the H + -depleted S 2 state and in the decay of the S 3 state to a modified S 2 state.…”

The impact of secondary coordination sphere engineering on water oxidation reactivity catalysed by molecular ruthenium complexes: a next-generation approach to develop advanced catalysts

“…[8][9][10] The quantum chemical simulations by Kaila and coworkers on PS II revealed that the electric field generated during the oxidation of redoxactive Tyr161 has a significant effect on lowering the energy barrier for the water-mediated proton transfer from the cluster-bound water molecule to the Asp61 residue, leading to the facile generation of the reactive state. 11 Thus, taking a lesson from nature, it can be perceived that the secondary coordination sphere might play an essential role in developing efficient artificial WOCs.…”