Interaction between tyrosineZ and substrate water in active photosystem II (original) (raw)
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Biochemistry, 1998
Photosynthetic water oxidation by photosystem II is mediated by a Mn 4 cluster, a cofactor X still chemically ill-defined, and a tyrosine, Y Z (D1-Tyr161). Before the final reaction with water proceeds to yield O 2 (transition S 4 f S 0 ), two oxidizing equivalents are stored on Mn 4 (S 0 w S 1 w S 2 ), a third on X (S 2 w S 3 ), and a forth on Y Z (S 3 w S 4 ). It has been proposed that Y Z functions as a pure electron transmitter between Mn 4 X and P 680 , or, more recently, that it acts as an abstractor of hydrogen from bound water. We scrutinized the coupling of electron and proton transfer during the oxidation of Y Z in PSII core particles with intact or impaired oxygen-evolving capacity. The rates of electron transfer to P 680 + , of electrochromism, and of pH transients were determined as a function of the pH, the temperature, and the H/D ratio. In oxygen-evolving material, we found only evidence for electrostatically induced proton release from peripheral amino acid residues but not from Y Z ox itself. The positive charge stayed near Y Z ox , and the rate of electron transfer was nearly independent of the pH. In core particles with an impaired Mn 4 cluster, on the other hand, the rate of the electron transfer became strictly dependent on the protonation state of a single base (pK ≈ 7). At pH <7, the rate of electron transfer revealed the same slow rate (t 1/2 ≈ 35 µs) as that of proton release into the bulk. The deposition of a positive charge around Y Z ox was no longer detected. A large H/D isotope effect (≈2.5) on these rates was also indicative of a steering of electron abstraction by proton transfer. That Y Z ox was deprotonated into the bulk in inactive but not in oxygen-evolving material argues against the proposed role of Y Z ox as an acceptor of hydrogen from water. Instead, the positive charge in its vicinity may shift the equilibrium from bound water to bound peroxide upon S 3 w S 4 as a prerequisite for the formation of oxygen upon S 4 f S 0 . † Financial support from the Deutsche Forschungsgemeinschaft (SFB 171/A2), the Fonds der Chemischen Industrie, and INTAS (INTAS-93-2852) is gratefully acknowledged. A.M. was supported by the Deutsche Forschungsgemeinschaft (Mu-1285/1-1, Mu-1285/1-2).
Tyrozine D oxidation and redox equilibrium in photosystem II
Biochimica et Biophysica Acta (BBA) - Bioenergetics, 2017
Tyrosine D (Tyr D) is an auxiliary redox active tyrosine residue in photosystem II (PSII). The mechanism of Tyr D oxidation was investigated by EPR spectroscopy, flash-induced fluorescence decay and thermoluminescence measurements in PSII enriched membranes from spinach. PSII membranes were chemically treated with 3 mM ascorbate and 1 mM diaminodurene and subsequent washing, leading to the complete reduction of Tyr D. Tyr D oxidation kinetics and competing recombination reactions were measured after a single saturating flash in the absence and presence of DCMU (inhibitor of the Q B-site) in the pH range of 4.7-8.5. Two kinetic phases of Tyr D oxidation were observed by the time resolved EPR spectroscopythe fast phase (msecsec time range) and the pH dependent slow phase (tens of seconds time range). In the presence of DCMU, Tyr D oxidation kinetics was monophasic in the entire pH range, i.e. only the fast kinetics was observed. The results obtained from the fluorescence and thermoluminescence analysis show that when forward electron transport is blocked in the presence of DCMU, the S 2 Q A recombination outcompetes the slow phase of Tyr D oxidation by the S 2 state. Modelling of the whole complex of these electron transfer events associated with Tyr D oxidation fitted very well with our experimental data. Based on these data, structural information and theoretical considerations we confirm our assignment of the fast and slow oxidation kinetics to two populations of PSII centers with different water positions (proximal and distal) in the Tyr D vicinity.
Water oxidation in PSII—H atom abstraction revisited
Biochimica et Biophysica Acta (BBA) - Bioenergetics, 2004
A model for the water oxidation reaction in Photosystem II (PSII) is presented, based on an H atom abstraction mechanism. The model rationalises the S-state dependence of observed substrate water exchange kinetics [Biochim. Biophys. Acta 1503 and assumes that H transfer occurs to an oxidised A-oxo bridge oxygen on the S 3 ! S 4 ! S 0 transition. The model requires that only one Mn-pair and a Ca ion be directly involved in the substrate binding and catalytic function. The multiline signal observed in the S 0 state is shown to plausibly arise from such a system. A detailed molecular model of the three-metal site, assuming ligation by those residues identified by mutagenesis as Ca/Mn ligands is presented. This bears a resemblance to the dinuclear Mn site in Mn catalase and is generally consistent with the electron density map of cyanobacterial PSII recently presented [Proc. Natl. Acad. Sci. U. S. A. 100 ].
Biochimica et Biophysica Acta (BBA) - Bioenergetics, 2017
The tyrosine residue D2-Tyr160 (Tyr D) in photosystem II (PSII) can be oxidized through charge equilibrium with the oxygen evolving complex in PSII. The kinetics of the electron transfer from Tyr D has been followed using timeresolved EPR spectroscopy after triggering the oxidation of pre-reduced Tyr D by a short laser flash. After its oxidation Tyr D is observed as a neutral radical (Tyr D •) indicating that the oxidation is coupled to a deprotonation event. The redox state of Tyr D was reported to be determined by the two water positions identified in the crystal structure of PSII [Saito et al. (2013) Proc. Natl. Acad. Sci. USA 110, 7690]. To assess the mechanism of the proton coupled electron transfer of Tyr D the oxidation kinetics has been followed in the presence of deuterated buffers, thereby resolving the kinetic isotope effect (KIE) of Tyr D oxidation at different H/D concentrations. Two kinetic phases of Tyr D oxidationthe fast phase (msec-sec time range) and the slow phase (tens of seconds time range) were resolved as was previously reported [Vass and Styring (1991) Biochemistry 30, 830]. In the presence of deuterated buffers the kinetics was significantly slower compared to normal buffers. Furthermore, although the kinetics were faster at both high pH and pD values the observed KIE was found to be similar (~2.4) over the whole pL range investigated. We assign the fast and slow oxidation phases to two populations of PSII centers with different water positions, proximal and distal respectively, and discuss possible deprotonation events in the vicinity of Tyr D .
Latest advances in PSII features and mechanism of water oxidation
Coordination Chemistry Reviews, 2018
The evolution of aerobic life on earth is depended on proceeding water splitting accomplished through photosynthesis in plants, algae, and cyanobacteria. Photosystem II (PSII), with a catalytic center CaMn 4 O 5 located on the lumenal surface, is responsible for water splitting and generating molecular oxygen through a four-step photocatalytic cycle. So far, the structure of the catalytic center and its ligation environments have been studied by different methods mostly relied on various spectroscopic techniques, disclosing unknowing aspects of the PSII components. Over the last half-decade, the experimental methods have extensively been coupled with quantum mechanics/molecular mechanics (QM/MM) methods to explore diverse aspects of PSII structure and water oxidation mechanism. However, despite the progress made in the past years, distinguishing a generally accepted mechanism on the O-O bond formation is still a challenge. This substantial challenge, if resolved, would provide a widespread criterion for development of globally deployable biomimetic model systems for water splitting catalysts. Here, we highlight some latest studies performed on the structure and function of PSII, the information that tells us how to establish new artificial catalytic systems to deliver maximum performance through water splitting in research labs.
2012
Photosystem II (PSII), the thylakoid membrane enzyme which uses sunlight to oxidize water to molecular oxygen, holds many organic and inorganic redox cofactors participating in the electron transfer reactions. Among them, two tyrosine residues, Tyr-Z and Tyr-D are found on the oxidizing side of PSII. Both tyrosines demonstrate similar spectroscopic features while their kinetic characteristics are quite different. Tyr-Z, which is bound to the D1 core protein, acts as an intermediate in electron transfer between the primary donor, P 680 and the CaMn 4 cluster. In contrast, Tyr-D, which is bound to the D2 core protein, does not participate in linear electron transfer in PSII and stays fully oxidized during PSII function. The phenolic oxygens on both tyrosines form well-defined hydrogen bonds to nearby histidine residues, His Z and His D respectively. These hydrogen bonds allow swift and almost activation less movement of the proton between respective tyrosine and histidine. This proton movement is critical and the phenolic proton from the tyrosine is thought to toggle between the tyrosine and the histidine in the hydrogen bond. It is found towards the tyrosine when this is reduced and towards the histidine when the tyrosine is oxidized. The proton movement occurs at both room temperature and ultra low temperature and is sensitive to the pH. Essentially it has been found that when the pH is below the pK a for respective histidine the function of the tyrosine is slowed down or, at ultra low temperature, halted. This has important consequences for the function also of the CaMn 4 complex and the protonation reactions as the critical Tyr-His hydrogen bond also steer a multitude of reactions at the CaMn 4 cluster. This review deals with the discovery and functional assignments of the two tyrosines. The pH dependent phenomena involved in oxidation and reduction of respective tyrosine is covered in detail. This article is part of a Special Issue entitled: Photosystem II. (S. Styring). 1 CaMn 4 cluster, the catalytic center consisting of four Mn-ions and one Ca-ion; D1 and D2, the core protein subunits in PSII; EPR, electron paramagnetic resonance; His D , histidine 189 (cyanobacterial numbering) on the D2 protein that participates in hydrogen bonding to Tyr-D; His Z , histidine 190 on the D1 protein that participates in hydrogen bonding to Tyr-Z; OEC, oxygen evolving complex consisting if the CaMn 4 cluster and surrounding amino acid ligands; P 680 , primary electron donor chlorophylls in PSII; PSII, photosystem II; Q A and Q B , primary and secondary plastoquinone acceptors of PSII; S states, intermediates in the cyclic turnover of the OEC; Tyr-D (Y D ), tyrosine 160 on the D2 protein; Tyr-Z (Y Z ), tyrosine 161 on the D1 protein.
Biochimica et Biophysica Acta (BBA) - Bioenergetics, 2010
Chloride is an essential cofactor for photosynthetic water oxidation. However, its location and functional roles in active photosystem II are still a matter of debate. We have investigated this issue by studying the effects of Cl − replacement by Br − in active PSII. In Br − substituted samples, Cl − is effectively replaced by Br − in the presence of 1.2 M NaBr under room light with protection of anaerobic atmosphere followed by dialysis. The following results have been obtained. i) The oxygen-evolving activities of the Br −-PSII samples are significantly lower than that of the Cl −-PSII samples; ii) The same S 2 multiline EPR signals are observed in both Br − and Cl −-PSII samples; iii) The amplitudes of the visible light induced S 1 Tyr Z • and S 2 Tyr Z • EPR signals are significantly decreased after Br − substitution; the S 1 Tyr Z • EPR signal is up-shifted about 8 G, whereas the S 2 Tyr Z • signal is down-shifted about 12 G after Br − substitution. These results imply that the redox properties of Tyr Z and spin interactions between Tyr Z • and Mn-cluster could be significantly modified due to Br − substitution. It is suggested that Cl − /Br − probably coordinates to the Ca 2+ ion of the Mn-cluster in active photosystem II.