Structural rearrangements preceding dioxygen formation by the water oxidation complex of photosystem II

Abstract

Photosynthetic water oxidation is catalyzed by the Mn 4 CaO 5 cluster of photosystem II. Recent studies implicate an oxo bridge atom, O5, of the Mn 4 CaO 5 cluster, as the "slowly exchanging" substrate water molecule. The D1-V185N mutant is in close vicinity of O5 and known to extend the lag phase and retard the O 2 release phase (slow phase) in this critical last S + 3 → S 0 transition of water oxidation. The pH dependence, hydrogen/deuterium (H/D) isotope effect, and temperature dependence on the O 2 release kinetics for this mutant were studied using time-resolved O 2 polarography, and comparisons were made with WT and two mutants of the putative proton gate D1-D61. Both kinetic phases in V185N are independent of pH and buffer concentration and have weaker H/D kinetic isotope effects. Each phase is characterized by a parallel or even lower activation enthalpy but a less favorable activation entropy than the WT. The results indicate new rate-determining steps for both phases. It is concluded that the lag does not represent inhibition of proton release but rather, slowing of a previously unrecognized kinetic phase involving a structural rearrangement or tautomerism of the S 3 + ground state as it approaches a configuration conducive to dioxygen formation. The parallel impacts on both the lag and O 2 formation phases suggest a common origin for the defects surmised to be perturbations of the H-bond network and the water cluster adjacent to O5.photosynthesis | water oxidation | oxygen release kinetics | photosystem II | activation energy O xygenic photosynthesis depends on the light-driven waterplastoquinone oxidoreductase, photosystem II (PSII), which catalyzes the complete oxidation of H 2 O molecules to O 2 . The electrons extracted from H 2 O oxidation are the reductant for autotrophic metabolism, and the liberated protons contribute to the transmembrane proton motive force powering ATP production (reviewed in refs. 1-4). The byproduct, O 2 , has transformed our Earth's atmosphere and makes heterotrophic life in the biosphere possible. A metal cluster, the Mn 4 CaO 5 , functions as the catalytic site of H 2 O oxidation and is buried in a protein domain of PSII referred to as the H 2 O oxidation complex (WOC). The primary photochemical electron donor of the reaction center (RC) complex is a dimeric chlorophyll moiety designated P 680 that is coordinated by the pseudosymmetrically arranged D1 and D2 polypeptides. Together, the D1/D2 heterodimer are responsible for the coordination of most of the photochemically active cofactors of the RC. Photoexcitation of P 680 initiates transmembrane charge separation with the activated electron moving to plastoquinone species, Q A and Q B , on the acceptor side of the RC. The resultant electron hole ðP +• 680 Þ functions as the powerful oxidant for the extraction of electrons from substrate H 2 O bound to the Mn 4 CaO 5 (Fig. 1A). However, the oxidation of the Mn 4 CaO 5 occurs through a redox active tyrosyl of the D1 protein, D1-Tyr161 (Y Z ), located between P 680 and the...

D1-Asn-298 in photosystem II is involved in a hydrogen-bond network near the redox-active tyrosine YZ for proton exit during water oxidation

“…Indeed, proton transfer as a lag phase (ϳ30 s) before electron transfer (42) or as a rate-limiting step (ϳ350 s) coupled to electron transfer (43) have been proposed in the S 2 3 S 3 transition, whereas a lag phase (ϳ200 s) before the electron transfer/O 2 evolution phase in the S 3 3 S 0 transfer has been attributed to a proton transfer process (58,(95)(96)(97). These putative proton transfer processes during the S 2 3 S 3 and S 3 3 S 0 transitions take place in the similar time regime of tens or hundreds of microseconds (42,43,58,(95)(96)(97), suggesting that they are performed by a similar proton transfer mechanism. However, the extent of inhibition by the D1-Asn-298 mutation was different between these transitions: the S 2 3 S 3 transition is only partially inhibited, whereas the S 3 3 S 0 transition is more significantly blocked.…”

“…Many mutants of amino acid residues in putative channels have been investigated so far (46 -60). Most of them are located on the Cl path; mutations of D1-Asp-61 to Ala and Asn significantly retarded the kinetic rate of O 2 release in the S 3 3 S 0 transition (47,53,58) and changed the property of a nearby water network (57). Mutations of D2-Lys-317 and D1-Asn-181, which are ligands to Cl-1, also retarded the O 2 kinetics or decreased the efficiency of the S 3 3 S 0 transition (54,55,59).…”

Structural models of the biological oxygen-evolving complex: achievements, insights, and challenges for biomimicry

“…1b) arising from many recent studies, but the details of the S 2 -S 3 transition and the precise nature of the S 3 state remain under active investigation. 74,77,[79][80][81][82][83][84][85][86][87][88][89][90][91][92][93][94][95][96][97][98] There is essentially no structural information about states past the S 3 and hence the identity of S 4 and of the intermediates involved in dioxygen formation and release remain debated. [99][100][101][102][103] A point that is important to clarify from the outset because it is highly relevant for the present review concerns the precise bonding topology in the inorganic core.…”

Across the Board: Licheng Sun on the Mechanism of O−O Bond Formation in Photosystem II

“…Regarding this unique observation, it has been suggested by different research groups that the S 3 ′Y Z . state must undergo some significant structural rearrangements before final oxidation of the Mn 4 CaO 5 cluster (over 1 ms) and subsequent O 2 evolution (within 50 μs) –…”