Properties of the Chloride-Depleted Oxygen-Evolving Complex of Photosystem II Studied by Electron Paramagnetic Resonance

Vliet, Pieter van; Rutherford, A. William

doi:10.1021/bi9514471

Cited by 82 publications

(72 citation statements)

References 60 publications

(133 reference statements)

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“…All of these factors affect the hydrogen-bonding network surrounding the OEC, thereby stabilizing one of the two isomers. Also, it has been observed that depletion of Cl -favors the S = 5/2 spin isomer in the S 2 state of spinach PSII (10,11). This observation, however, has not been seen in cyanobacterial PSII indicating that the Cl --binding site and its associated hydrogen-bonding network affects the spin isomer distribution differently in the two species (12).…”

Section: Introductionmentioning

confidence: 99%

Substitution of the D1-Asn87 site in photosystem II of cyanobacteria mimics the chloride-binding characteristics of spinach photosystem II

Banerjee

Ghosh

Kim

et al. 2018

Journal of Biological Chemistry

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Photoinduced water oxidation at the O 2 -evolving complex (OEC) of photosystem II (PSII) is a complex process involving a tetramanganesecalcium cluster that is surrounded by a hydrogenbonded network of water molecules, chloride ions, and amino-acid residues. Although the structure of the OEC has remained conserved over eons of evolution, significant differences in the chloride-binding characteristics exist between cyanobacteria and higher plants. An analysis of amino-acid residues in and around the OEC has identified residue 87 in the D1 subunit as the only significant difference between PSII in cyanobacteria and higher plants. We substituted the D1-N87 residue in the cyanobacterium Synechocystis sp. PCC 6803 (wild-type) with alanine, present in higher plants, or with aspartic acid. We studied PSII core complexes purified from D1-N87A and D1-N87D variant strains to probe the function of the D1-N87 residue in the water-oxidation mechanism. EPR spectra of the S 2 state and flash-induced FTIR spectra of both D1-N87A and D1-N87D PSII core complexes exhibited characteristics similar to those of wildtype Synechocystis PSII core complexes. However, flash-induced O 2 -evolution studies revealed a decreased cycling efficiency of the D1-N87D variant, whereas the cycling efficiency of the D1-N87A PSII variant was similar to that of wild-type PSII. Steady-state O 2 -evolution activity assays revealed that substitution of the D1-87 residue with alanine perturbs the chloridebinding site in the proton-exit channel. These findings provide new insight into the role of the D1-N87 site in the water-oxidation mechanism and explain the difference in the chloride-binding properties of cyanobacterial and higher-plant PSII.Photosystem II (PSII) is a 700 kDa pigmentprotein complex responsible for water oxidation in photoautotrophic organisms. The site of water oxidation, known as the oxygen-evolving complex (OEC), consists of a µ-oxo-bridged tetramanganese-calcium cluster ligated by a number of amino-acid residues and water molecules (1). The OEC is surrounded by a network of hydrogen-bonded amino-acid residues and water molecules that, along with Cl -ions, play a pivotal role in water oxidation (2,3). This process is initiated by photoinduced charge separation via a chlorophyll molecule called P 680 . The P 680 ⦁ + species thus formed is reduced by oxidation of the tetramanganese cluster, thereby building up oxidizing equivalents that are used for water oxidation (4). The process of water oxidation has been shown to proceed via a fourflash cycle called the Kok cycle with the intermediates formed at each step being referred to as S i states (i = 0 -4) (5). has remained elusive so far while the remaining S states have been studied using many experimental methods, especially electron paramagnetic resonance (EPR), Fourier transform infrared (FTIR), and extended X-ray absorption fine structure (EXAFS) spectroscopy. Information about the S 0 -S 3 states provides valuable insights about water oxidation.Due to the ease of generation an...

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Section: Introductionmentioning

confidence: 99%

Substitution of the D1-Asn87 site in photosystem II of cyanobacteria mimics the chloride-binding characteristics of spinach photosystem II

Banerjee

Ghosh

Kim

et al. 2018

Journal of Biological Chemistry

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“…Choride is also an essential ion for PSII activity (24,26,(41)(42)(43)(44)(45)(46)(47)(48)(49)(50)(51)(52)(53). In plant PSII, removal of Cl Ϫ inhibits oxygen evolution and perturbs the Mn 4 cluster to a variable extent depending on the precise Cl Ϫ -depletion method used (24,26,46).…”

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confidence: 99%

“…In plant PSII, removal of Cl Ϫ inhibits oxygen evolution and perturbs the Mn 4 cluster to a variable extent depending on the precise Cl Ϫ -depletion method used (24,26,46). The removal of Cl Ϫ by incubation in Cl Ϫ -free buffer increased the proportion of the Mn 4 cluster in the high-spin state (g ϭ 4 EPR signal), but the enzyme continues to work at a reduced rate (46). When Cl Ϫ is removed by a high pH shock, the high-spin state is formed, and the S-state cycle is blocked after S 2 formation in the majority of centers, whereas treatment with SO 4 2Ϫ inhibits the enzyme but allows radical (Tyr Z ⅐ ) formation in the presence of S 2 , giving rise to the split EPR signal, at least in a fraction of the centers (46,47,53,54).…”

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Biosynthetic Exchange of Bromide for Chloride and Strontium for Calcium in the Photosystem II Oxygen-evolving Enzymes

Ishida

Sugiura

Rappaport

et al. 2008

Journal of Biological Chemistry

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The active site for water oxidation in photosystem II goes through five sequential oxidation states (S 0 to S 4 ) before O 2 is evolved. It consists of a Mn 4 Ca cluster close to a redox-active tyrosine residue (Tyr Z ). Cl ؊ is also required for enzyme activity. To study the role of Ca 2؉ and Cl ؊ in PSII, these ions were biosynthetically substituted by Sr 2؉ and Br ؊ , respectively, in the thermophilic cyanobacterium Thermosynechococcus elongatus. Irrespective of the combination of the non-native ions used (Ca/Br, Sr/Cl, Sr/Br), the enzyme could be isolated in a state that was fully intact but kinetically limited. The electron transfer steps affected by the exchanges were identified and then investigated by using time-resolved UV-visible absorption spectroscopy, time-resolved O 2 polarography, and thermoluminescence spectroscopy. The effect of the Ca 2؉ /Sr 2؉ and Cl ؊ /Br ؊ exchanges was additive, and the magnitude of the effect varied in the following order: Ca/Cl < Ca/Br < Sr/Cl < Sr/Br. In all cases, the rate of O 2 release was similar to that of the S 3 Tyr Z ⅐ to S 0 Tyr Z transition, with the slowest kinetics (i.e. the Sr/Br enzyme) being ≈6 -7 slower than in the native Ca/Cl enzyme. This slowdown in the kinetics was reflected in a decrease in the free energy level of the S 3 state as manifest by thermoluminescence. These observations indicate that Cl ؊ is involved in the water oxidation mechanism. The possibility that Cl ؊ is close to the active site is discussed in terms of recent structural models.Light-driven water oxidation by the photosystem II (PSII) 3 enzyme is responsible for the O 2 on Earth and is at the origin of the production of most of the biomass. Refined three-dimensional x-ray structures at 3.5 and 3.0 Å resolution have been obtained by using PSII isolated from the thermophilic cyanobacterium Thermosynechococcus elongatus (1, 2). PSII is made up of more than 20 membrane protein subunits, 35-36 chlorophyll molecules, more than 10 carotenoid molecules, several lipids, two hemes, and the cofactors involved in the electron transfer reactions (1, 2). Absorption of a photon by chlorophyll is followed by the formation of a radical pair in which the pheophytin molecule, Pheo D1 , is reduced and the accessory chlorophyll molecule, Chl D1 , is oxidized (3-5). The cation is then stabilized on P 680 , a weakly coupled chlorophyll dimer (see e.g. Refs. 6 and 7 for energetic considerations). The pheophytin anion transfers the electron to a quinone, Q A , which in turn reduces a second quinone, Q B . P 680 .ϩ oxidizes a tyrosine residue of the D1 polypeptide, Tyr Z , which in turn oxidizes the Mn 4 Ca cluster.The Mn 4 Ca cluster acts as a device for accumulating oxidizing equivalents and as the active site for water oxidation. During the enzyme cycle, the oxidizing side of PSII goes through five sequential redox states, denoted as S n , where n varies from 0 to 4 upon the absorption of four photons (8). Upon formation of the S 4 state, two molecules of water are rapidly oxidized, the S 0 state is r...

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“…These cofactors serve various functions during water oxidation: The Mn cluster stores at least two of the oxidizing equivalents (namely on transitions S 0 w S 1 and S 1 w S 2 of the catalytic cycle) and may bind the reactive water molecules (5). It is proposed that the cofactor X is both oxidized and deprotonated on S 2 w S 3 (8, 9) and that the two ions adjust the redox potentials of the other compounds (8,13).Tyrosine Y Z probably occupies a position on subunit D1 relative to P 680 which is similar to the one of LArg135 or MHis162 in the reaction center of Rhodopseudomonas Viridis (1,14,15). This has been inferred from the distance estimates of about 12 Å to P 680 (15,(79)(80)(81)) and a projection of about 4 Å on the membrane normal according to the relative electrogenicity of electron transfer between Y Z and P 680 + (16,17).…”

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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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Properties of the Chloride-Depleted Oxygen-Evolving Complex of Photosystem II Studied by Electron Paramagnetic Resonance

Cited by 82 publications

References 60 publications

Substitution of the D1-Asn87 site in photosystem II of cyanobacteria mimics the chloride-binding characteristics of spinach photosystem II

Substitution of the D1-Asn87 site in photosystem II of cyanobacteria mimics the chloride-binding characteristics of spinach photosystem II

Biosynthetic Exchange of Bromide for Chloride and Strontium for Calcium in the Photosystem II Oxygen-evolving Enzymes

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

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