Theoretical reflections on the structural polymorphism of the oxygen-evolving complex in the S2 state and the correlations to substrate water exchange and water oxidation mechanism in photosynthesis

Abstract

The structural polymorphism of the oxygen-evolving complex is of great significance to photosynthetic water oxidation. Employing density functional theory calculations, we have made further advisement on the interconversion mechanism of O5 transfer in the S state, mainly focusing on the potentiality of multi-state reactivity and spin transitions. Then, O5 protonation is proven impossible in S for irreversibility of the interconversion, which serves as an auxiliary judgment for the protonation state of O5 in S. Besides, the structural polymorphism could also be archived by alternative mechanisms involving Mn3 ligand exchange, one of which with Mn3(III) makes sense to substrate water exchange in S, although being irresponsible for the derivations of the observed EPR signals. During the water exchange, high-spin states would prevail to facilitate electron transfer between the ferromagnetically coupled Mn centers. In addition, water exchange in S could account for the closed-cubane structure as the initial form entering S at cryogenic temperatures. With regard to water oxidation, the structural flexibility and variability in both S and S guarantee smooth W2-O5 coupling in S, according to the substrate assignments from water exchange kinetics. Within this theoretical framework, the new XFEL findings on S-S can be readily rationalized. Finally, an alternative mechanistic scenario for OO bond formation with ·OH radical near O4 is presented, followed by water binding to the pivot Mn4(III) from O4 side during S-S. This may diversify the substrate sources combined with the Ca channel in water delivery for the forthcoming S-cycle.

Thermodynamics of the S2-to-S3 state transition of the oxygen-evolving complex of photosystem II

“…This suggests the advancement of the OEC to the S3 state through the S2 g = 2 state is energetically unfavorable, which agrees with earlier studies. 8,19,32,53,[55][56][57] Thus, for the OEC to advance from the S2 g = 2 state to the S3 state, it has to transit through the S2 g = 4.1 state. [58][59][60] Experimental studies using EPR spectroscopy 58,59 also indicates the formation of the S3 state from the S2 state g = 4.1 isomer at lower temperatures in both Ca-PSII and Sr-PSII.…”

Fourier Transform Infrared Analysis of the S-State Cycle of Water Oxidation in the Microcrystals of Photosystem II

“…The fourth flash converts the S 0 state to the initial S 1 state to complete the S-state cycle. It is generally accepted that the transitions other than the S 1 → S 2 transition (S 0 → S 1 , S 2 → S 3 , and S 3 → S 0 ) are accompanied by proton release, − and the S 2 → S 3 and S 3 → S 0 (after S 4 formation) transitions involve the insertion of water molecules into the WOC. − …”

The exchange of the fast substrate water in the S2 state of photosystem II is limited by diffusion of bulk water through channels – implications for the water oxidation mechanism

“…[44][45][46]49 For all S states, the S A structures dominate under most conditions, except for the S 3 state, where S 3 AW is most stable. 19,29 Identication of the two substrate water binding sites in the four discrete intermediates of the reaction cycle would provide a solid basis for decoding the mechanism of biological water oxidation. While there are several ways to identify water molecules bound to or near the Mn 4 CaO 5/6 cluster, only the determination of the isotopic composition of the O 2 produced aer a rapid enrichment of the sample with H 2…”

“…[11][12][13][14][15][16][17] The next light-induced charge separation triggers the S 3 / S 4 / S 0 transition, which not only involves the O-O bond formation, but also O 2 release and the concomitant lling of the open coordination site by one of the terminal water ligands (W3 or W2) as well as the binding of a new water molecule (W N2 ). 9,12,18,19 All S state transitions, with the exception of S 1 / S 2 , are coupled to proton release into the bulk, keeping the total charge of the cluster at 0 or +1, respectively. 20 Proton release is facilitated by an intricate H-bonding network that is pivotal to the function of PSII and its earth-abundant water oxidation catalyst.…”

“… 44–46,49 For all S states, the S A structures dominate under most conditions, except for the S 3 state, where S 3 AW is most stable. 19,29 …”