Temperature dependence of the oxidation kinetics of TyrZ and TyrD in oxygen-evolving photosystem II complexes throughout the range from 320K to 5K

Abstract

The photo-induced oxidation of TyrZ and TyrD by P680(•+), that involves both electron and proton transfer (PCET), has been studied in oxygen-evolving photosystem II from Thermosynechococcus elongatus. We used time-resolved absorption spectroscopy to measure the kinetics of P680(•+) reduction by tyrosine after the first flash given to dark-adapted PS II as a function of temperature and pH. The half-life of TyrZ oxidation by P680(•+) increases from 20ns at 300K to about 4μs at 150K. Analyzing the temperature dependence of the rate, one obtains a reorganization energy of about 770meV. Between 260K and 150K, the reduction of P680(•+) by TyrZ is increasingly replaced by charge recombination between P680(•+) and QA(•-). We propose that the driving force for TyrZ oxidation by P680(•+) decreases upon lowering the temperature. TyrZ oxidation cannot be excluded in a minority of PS II complexes at cryogenic temperatures. TyrD oxidation by P680(•+) with a half-life of about 30ns was observed at high pH. The pH dependence of the yield of TyrD oxidation can be described by a single protonable group with a pK of approximately 8.4. The rate of TyrD oxidation by P680(•+) is virtually identical upon substitution of solvent exchangeable protons with deuterons indicating that the rate is limited by electron transfer. The rate is independent of temperature between 5K and 250K. It is concluded that TyrD donates the electron to P680(•+) via PD2.

Redox transients of P680 associated with the incremental chlorophyll‐a fluorescence yield rises elicited by a series of saturating flashes in diuron‐treated photosystem II core complex of Thermosynechococcus vulcanus

“…1). This ultrafast phase is followed by an essentially biphasic decay, which can be well fitted in the time window from 1 to 800 ns by a bi-exponential decay with time constants of 16.6 ns (∼50%) and 167 ns (∼30%) and a constant (∼20%) that accounts for decay components on the microsecond time scale (Table 1), in good agreement with literature data for the reduction of P680 •+ by the donor side of PSII (van Best and Mathis 1978, Brettel et al 1984, Schlodder et al 2015. The fastest decay component (∼20 ns) has been clearly attributed to proton-coupled electron transport from TyrZ in the dark-adapted state (S 1 ) of the OEC (Tommos andBabcock 2000, Schlodder et al 2015).…”

“…The fastest decay component (∼20 ns) has been clearly attributed to proton‐coupled electron transport from TyrZ in the dark‐adapted state (S 1 ) of the OEC (Tommos and Babcock , Schlodder et al ). Slower decay components are thought to indicate relaxation processes involving hydrogen bond networks that shift the equilibrium P680 •+ TyrZ ↔ P680TyrZ • (H + ) to the right and reduction of TyrZ • (H + ) by the OEC (Schilstra et al , Christen and Renger , Schlodder et al ). Reduction of P680 •+ is also known to be slowed down in the presence of higher oxidation states (S 2 and S 3 ) of the OEC (Brettel et al , Schlodder et al ) and in PSII with inactive OEC (Conjeaud et al , Conjeaud and Mathis ).…”

Microsolvation of the Redox-Active Tyrosine-D in Photosystem II: Correlation of Energetics with EPR Spectroscopy and Oxidation-Induced Proton Transfer

“…Y D is known to outcompete Y Z in high-pH conditions; for example at pH 8.5 oxidation of Y D becomes extremely fast ( t 1/2 ≈ 190 ns), 22 and recent results from Schlodder et al report this rate to be even faster ( t 1/2 ≈ 30 ns) at pH 9. 138 These faster oxidation rates also depend on the location of the cation on the reaction center, and it is suggested 22,138 that in high-pH (8.5) conditions the major proportion of cation resides on the P D2 side of the reaction center, 138,139 unlike in low-pH conditions, where the cation is mainly localized on the P D1 side. 30 This charge shift presumably makes electron transfer faster from the reduced Y D to P 680 ( t 1/2 ≈ 30–190 ns).…”

Ultrafast Oxidation of a Tyrosine by Proton-Coupled Electron Transfer Promotes Light Activation of an Animal-like Cryptochrome

“…The absence of a KIE on the oxidation of tyrosine in PSII in ∼30 ns may point to a sequential PT/ET, where the hydroxyl proton of the tyrosine moves to a nearby histidine residue prior to rate-limiting ET. , A slower (few μs) tyrosine oxidation in PSII depleted of the oxygen-evolving complex, however, showed a normal KIE and was hence assigned to concerted PCET …”

“…Oxidation and back-reduction of tyrosyl residues has been discovered to be involved in the functioning of several enzymes, like prostaglandin H synthase, galactose oxidase, ribonucleotide reductase or photosystem II (PSII) . The case of PSII is of particular importance because the possibility to trigger the reactions by light allowed for detailed time-resolved studies of the reaction mechanism and is still a matter of discussion. − The one-electron reduction potential of tyrosine (YH •+ /YH couple) is as high as ∼1.35 V (vs NHE) in aqueous solution . However, the oxidant of tyrosine in PSII, the chlorophyll cation P680 + , provides only ∼1.25 V, so that a simple ET from YH to P680 + would be uphill (endergonic).…”