The Photosynthetic Oxygen Evolving Complex Requires Chloride for Its Redox State S2→S3 and S3→S0 Transitions But Not for S0→S1 or S1→S2 Transitions

Wincencjusz, Hanna; Gorkom, and Hans J. van; Yocum, Charles F.

doi:10.1021/bi9626719

Cited by 143 publications

(159 citation statements)

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“…This suggestion is in line with the observed strong retardation of electron transfer between Y Z and P 680 + in Ca-depleted PSII (29,83,110). On the contrary, in Cl --depleted centers where electron transfer from Y Z to P 680 + occurs as fast as in controls, i.e., in nanoseconds (8), the difference spectrum Y Z ox -Y Z (8,111) is similar to the one measured in oxygen-evolving centers in the whole spectral region. This indicates a more similar environment of Y Z in oxygen-evolving and Cl --depleted centers.…”

Section: Discussionmentioning

confidence: 87%

Tyrosine-Z in Oxygen-Evolving Photosystem II: A Hydrogen-Bonded Tyrosinate

1998

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In oxygen-evolving photosystem II (PSII), a tyrosine residue, D1Tyr161 (Y Z ), serves as the intermediate electron carrier between the catalytic Mn cluster and the photochemically active chlorophyll moiety P 680 . A more direct catalytic role of Y Z , as a hydrogen abstractor from bound water, has been postulated. That Y Z ox appears as a neutral (i.e. deprotonated) radical, Y Z • , in EPR studies is compatible with this notion. Data based on electrochromic absorption transients, however, are conflicting because they indicate that the phenolic proton remains on or near to Y Z ox . In Mn-depleted PSII the electron transfer between Y Z and P 680 + can be almost as fast as in oxygen-evolving material, however, only at alkaline pH. With an apparent pK of about 7 the fast reaction is suppressed and converted into an about 100-fold slower one which dominates at acid pH. In the present work we investigated the optical difference spectra attributable to the transition Y Z f Y Z ox as function of the pH. We scanned the UV and VIS range and used Mn-depleted PSII core particles and also oxygen-evolving ones. Comparing these spectra with published in vitro and in vivo spectra of phenolic compounds, we arrived at the following conclusions: In oxygen-evolving PSII Y Z resembles a hydrogen-bonded tyrosinate, Y Z (-) ‚‚‚H (+) ‚B. The phenolic proton is shifted toward a base B already in the reduced state and even more so in the oxidized state. The retention of the phenolic proton in a hydrogen-bonded network gives rise to a positive net charge in the immediate vicinity of the neutral radical Y Z • . It may be favorable both for the very rapid reduction by Y Z of P 680 + and for electron (not hydrogen) abstraction by Y Z • from the Mn-water cluster.Photosystem II (PSII) 1 produces molecular oxygen from water. It is located in photosynthetic membranes of plants and cyanobacteria. The inner core of PSII is a heterodimer of the D1D2 subunits which show homology with the L and M subunits of the purple bacterial RC (1). The primary electron donor of PSII, P 680 , is located close to the lumenal side of the membrane. The absorption of a quantum of light drives the charge separation between P 680 and the quinone acceptor at the stromal side (2). The very high redox potential of P 680 + drives water oxidation. It is a four-stepped process with at least four increasingly oxidized, metastable states S 0 to S 3 , plus a transient state S 4 that decays in milliseconds into S 0 under release of O 2 . P 680 + is reduced (in nanoseconds) by a redox-active tyrosine residue, Y Z (D1Tyr161 (3, 4)). Y Z ox is, in turn, reduced in microseconds by the oxygenevolving complex (OEC). The structure and exact location of the OEC is still ill-defined. It is formed by four manganese atoms (5, 6), possibly another redox cofactor, X (7-9), plus at least one Cl -ion (10) and one Ca 2+ (11, 12) ion. These cofactors serve various functions during water oxidation: The Mn cluster stores at least two of the oxidizing equivalents (namely on transitions S ...

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Section: Discussionmentioning

confidence: 87%

Tyrosine-Z in Oxygen-Evolving Photosystem II: A Hydrogen-Bonded Tyrosinate

1998

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“…21 Recent studies have indicated that the presence of Cl is necessary only for the S 2 →S 3 and S 3 →S 0 transitions of the OEC, while the earlier steps of the cycle can proceed in its absence. 48,49 The amplitude and distance changes of Fourier peak III in the S 3 state are less obvious. Peak III appears substantially above the noise level in three of the six S 3 FTs and is readily distinguishable from the noise in two others.…”

Section: Exafs Of the S 3 Statementioning

confidence: 98%

Structural Change of the Mn Cluster during the S₂→S₃ State Transition of the Oxygen-Evolving Complex of Photosystem II. Does It Reflect the Onset of Water/Substrate Oxidation? Determination by Mn X-ray Absorption Spectroscopy

et al. 2000

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The oxygen-evolving complex of Photosystem II in plants and cyanobacteria catalyzes the oxidation of two water molecules to one molecule of dioxygen. A tetranuclear Mn complex is believed to cycle through five intermediate states (S 0 -S 4 ) to couple the four-electron oxidation of water with the one-electron photochemistry occurring at the Photosystem II reaction center. We have used X-ray absorption spectroscopy to study the local structure of the Mn complex and have proposed a model for it, based on studies of the Mn K-edges and the extended X-ray absorption fine structure of the S 1 and S 2 states. The proposed model consists of two di-μ-oxo-bridged binuclear Mn units with Mn-Mn distances of ~2.7 Å that are linked to each other by a mono-μ-oxo bridge with a Mn-Mn separation of ~3.3 Å. The Mn-Mn distances are invariant in the native S 1 and S 2 states. This report describes the application of X-ray absorption spectroscopy to S 3 samples created under physiological conditions with saturating flash illumination. Significant changes are observed in the Mn-Mn distances in the S 3 state compared to the S 1 and the S 2 states. The two 2.7 Å Mn-Mn distances that characterize the di-μ-oxo centers in the S 1 and S 2 states are lengthened to ~2.8 and 3.0 Å in the S 3 state, respectively. The 3.3 Å Mn-Mn and Mn-Ca distances also increase by 0.04-0.2 Å. These changes in Mn-Mn distances are interpreted as consequences of the onset of substrate/water oxidation in the S 3 state. Mn-centered oxidation is evident during the S 0 →S 1 and S 1 →S 2 transitions. We propose that the changes in Mn-Mn distances during the S 2 →S 3 transition are the result of ligand or water oxidation, leading to the Supporting Information Available: E-space S 3 state EXAFS spectrum; the data in k-space and the background that was removed to reduce the low-frequency contributions that show up as peaks at <1 Å in the Fourier transform; and the Fourier isolate of the k-space S 3 spectrum, shown overplotted on the S 3 EXAFS spectrum (PDF). This material is available free of charge via the Internet at http:// pubs.acs.org. NIH Public Access

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“…Additionally, it is possible that chloride depletion perturbs a proton exit pathway (37). Such disruption could give rise to long-lived higher S states (38,39) that may increase the probability of the release of partially oxidized water intermediates. These possibilities are not mutually exclusive.…”

Section: Psii Electron Donor Side Ros Production By Incomplete Water mentioning

confidence: 99%

Amino acid oxidation of the D1 and D2 proteins by oxygen radicals during photoinhibition of Photosystem II

Kale

Hebert

Frankel

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

133

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The Photosystem II reaction center is vulnerable to photoinhibition. The D1 and D2 proteins, lying at the core of the photosystem, are susceptible to oxidative modification by reactive oxygen species that are formed by the photosystem during illumination. Using spin probes and EPR spectroscopy, we have determined that both O 2 . The identification of specific amino acid residues oxidized by reactive oxygen species provides insights into the mechanism of damage to the D1 and D2 proteins under light stress.photosynthesis | Photosystem II | reactive oxygen species | photo inhibition | mass spectrometry P hotosystem II (PSII) functions as a water-plastoquinone oxidoreductase (1, 2) and is a thylakoid membrane pigmentprotein complex present in all oxygenic photosynthetic organisms (cyanobacteria, algae, and higher plants). Current high-resolution structures of thermophilic cyanobacterial PSII (3, 4), and lower resolution structures of the red algal (5) and higher plant photosystems (6), have been critically important in furthering our understanding of the molecular organization of PSII. Structurally, the PSII reaction center core is composed of five proteins: D1, D2, the α-and β-subunits of cytochrome b 559 , and PsbI. These components bind all of the redox-active cofactors of PSII.Excitation energy transfer and electron transport within PSII are unavoidably associated with production of reactive oxygen species (ROS) when the absorption of light by the chlorophyll antenna exceeds the capacity for energy utilization. Many mechanisms for ROS production have been proposed (for reviews, see refs. 7 and 8). Briefly, singlet oxygen ( 1 O 2 ) may be formed by excitation energy transfer from triplet chlorophylls (formed either by the change in orientation of the spin of an excited electron in the PSII antenna complex, or via charge recombination of the primary radical pair 3 [P 680 •+ Pheo •− ]) to O 2 (9, 10). ROS production by electron transport involves either the two-electron oxidation of water or the one-electron reduction of O 2 on the PSII electron donor and acceptor sides, respectively. On the PSII electron donor side, a twoelectron oxidation of water leads to the formation of hydrogen peroxide (H 2 O 2 ), which may be oxidized to the superoxide anion radical (O 2•−

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The Photosynthetic Oxygen Evolving Complex Requires Chloride for Its Redox State S₂→S₃ and S₃→S₀ Transitions But Not for S₀→S₁ or S₁→S₂ Transitions

Cited by 143 publications

References 32 publications

Tyrosine-Z in Oxygen-Evolving Photosystem II: A Hydrogen-Bonded Tyrosinate

Tyrosine-Z in Oxygen-Evolving Photosystem II: A Hydrogen-Bonded Tyrosinate

Structural Change of the Mn Cluster during the S₂→S₃ State Transition of the Oxygen-Evolving Complex of Photosystem II. Does It Reflect the Onset of Water/Substrate Oxidation? Determination by Mn X-ray Absorption Spectroscopy

Amino acid oxidation of the D1 and D2 proteins by oxygen radicals during photoinhibition of Photosystem II

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The Photosynthetic Oxygen Evolving Complex Requires Chloride for Its Redox State S2→S3 and S3→S0 Transitions But Not for S0→S1 or S1→S2 Transitions

Cited by 143 publications

References 32 publications

Tyrosine-Z in Oxygen-Evolving Photosystem II: A Hydrogen-Bonded Tyrosinate

Tyrosine-Z in Oxygen-Evolving Photosystem II: A Hydrogen-Bonded Tyrosinate

Structural Change of the Mn Cluster during the S2→S3 State Transition of the Oxygen-Evolving Complex of Photosystem II. Does It Reflect the Onset of Water/Substrate Oxidation? Determination by Mn X-ray Absorption Spectroscopy

Amino acid oxidation of the D1 and D2 proteins by oxygen radicals during photoinhibition of Photosystem II

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The Photosynthetic Oxygen Evolving Complex Requires Chloride for Its Redox State S₂→S₃ and S₃→S₀ Transitions But Not for S₀→S₁ or S₁→S₂ Transitions

Structural Change of the Mn Cluster during the S₂→S₃ State Transition of the Oxygen-Evolving Complex of Photosystem II. Does It Reflect the Onset of Water/Substrate Oxidation? Determination by Mn X-ray Absorption Spectroscopy