Application of the Marcus theory for analysis of the temperature dependence of the reactions leading to photosynthetic water oxidation: results and implications

Ренгер, Г.; Christen, G.; Karge, M.; Eckert, Hann-Jörg; Irrgang, Klaus−Dieter

doi:10.1007/s007750050245

Cited by 53 publications

(72 citation statements)

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“…The activation energy was very low, about 10 kJ mol -1 (37,38). Taking the gross kinetical ruler of Moser et al (82) at face value and using the observed rate of electron transfer between Y Z and P 680 + , about 5 × 10 7 s -1 in oxygen-evolving PSII (8,37,(83)(84)(85)(86), we calculated a reorganization energy of about 0.5 eV (123,124). An even higher reorganization energy, 0.7 eV, has been obtained, for instance, for the electron transfer (in ∼200 ps) from bacteriopheophytin to Q A in the bacterial reaction center (see ref 82 and references therein).…”

Section: Discussionmentioning

confidence: 99%

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: 99%

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

1998

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“…This relatively long distance eliminates direct H transfer and requires either the existence of an obligatory base for transferring the proton (i.e., pcet) or a large-scale conformational change to reduce the distance to within the deBroglie wavelength of the H atom. A large structural change appears to occur within the PSII-WOC but only on the S 2 3 S 3 3 S 4 transitions, although it is not yet structurally characterized (38).…”

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confidence: 99%

“…Rate measurements for each of the four S-state transitions involving the reduction of a photo-generated tyrosyl radical by the WOC-substrate complex leading up to O 2 production on S 4 indicate successively decreasing first-order rate constants in the range of 2 ϫ 10 4 to 1 ϫ 10 3 s Ϫ1 , activation energies of 1.2, 2.5, 9, and 5 kcal͞mol (38), and KIEs in the range of k H ͞k D Ϸ 1.3-1.4 to 1.3-2.9 (39) and 1.5-2.3 (40). Mechanisms have been proposed in which these rate constants, KIEs, and activation energies have been offered as evidence for concerted H transfer in the rate-limiting process for each S-state transition (8,9,(41)(42)(43).…”

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Kinetics of proton-coupled electron-transfer reactions to the manganese-oxo “cubane” complexes containing the Mn ₄ O\documentclass[12pt]{minimal}\usepackage{amsmath}\usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy}\usepackage{mathrsfs}\setlength{\oddsidemargin}{-69pt}\begin{document}\begin{equation}{\mathrm{_{4}^{6+}}}\end{equation}\end{document} and Mn ₄ O\documentclass[12pt]{minimal}\usepackage{amsma

Maneiro

Ruettinger

Bourlès

et al. 2003

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

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The kinetics of proton-coupled electron-transfer (pcet) reactions are reported for Mn 4O4(O2PPh2)6, 1, and [Mn4O4(O2PPh2)6] ؉ , 1 ؉ , with phenothiazine (pzH). Both pcet reactions form 1H, by H transfer to 1 and by hydride transfer to 1 ؉ . Surprisingly, the rate constants differ by only 25% despite large differences in the formal charges and driving force. The driving force is proportional to the difference in the bond-dissociation energies (BDE >94 kcal͞mol for homolytic, 1H 3 H ؉ 1, vs. Ϸ127 kcal͞ mol for heterolytic, 1H 3 H ؊ ؉ 1 ؉ , dissociation of the OOH bond in 1H). The enthalpy and entropy of activation for the homolytic reaction (⌬H ‡ ‫؍‬ ؊1.2 kcal͞mol and ⌬S ‡ ‫؍‬ ؊32 cal͞mol⅐K; 25-6.7°C) reveal a low activation barrier and an appreciable entropic penalty in the transition state. The rate-limiting step exhibits no H͞D kinetic isotope effect (k H͞kD ‫؍‬ 0.96) for the first H atom-transfer step and a small kinetic isotope effect (1.4) for the second step (1H ؉ pzH 3 1H 2 ؉ pz • ). These lines of evidence indicate that formation of a reactive precursor complex before atom transfer is rate-limiting (conformational gating), and that little or no NOH bond cleavage occurs in the transition state. H-atom transfer from pzH to alkyl, alkoxyl, and peroxyl radicals reveals that BDEs are not a good predictor of the rates of this reaction. Hydride transfer to 1 ؉ provides a concrete example of two-electron pcet that is hypothesized for the OOH bond cleavage step during catalysis of photosynthetic water oxidation.bond-dissociation energy ͉ manganese ͉ hydrogen atom transfer ͉ proton transfer ͉ kinetic isotope effect A tom-and ion-transfer reactions comprise a major class of chemical reactions found in biological systems, notably metabolic pathways (1-5). Reactions involving the net transfer of a hydrogen atom may be viewed in terms of two coupling limits with intermediate cases implicit (6): movement of a H atom between a donor͞acceptor pair vs. independent proton͞electron-transfer steps involving different electron and proton sites. As a class these are referred to as protoncoupled electron-transfer (pcet) processes (7).An example arises in the case of the water-oxidizing͞O 2 -evolving complex of photosynthesis [photosystem-II wateroxidizing complex (PSII-WOC)], which catalyzes the extraction of four electrons and four protons from two water molecules mediated by an inorganic core, Mn 4 O x Ca 1 Cl y , and a tyrosyl radical (8,9). Only a limited number of model Mn complexes having mononuclear (10, 11) or binuclear manganese-oxo cores have contributed to understanding the kinetic steps in pcet chemistry (3, 12). These and related studies led to different results with some systems following a pathway of initial H abstraction (3,13,14) [with large kinetic isotope effect (KIE) in the range of 30-40 (15)], in contrast to other cases that exhibited an electrochemical step followed by a proton-transfer step with minimal H͞D isotope effect (1, 16). Herein we report kinetics parameters for the initial pcet reaction between ...

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“…The driving force of the chemical reaction is the Gibbs free energy, which is composed of enthalpic and entropic components. The theory of electron transfer in chemical and biological system was developed by Marcus (Marcus & Sutin, 1985) and played a key role in advancing the understanding electron transfer mechanisms, including photosynthetic systems (Turro et al, 1996;Renger et al, 1998;Mayer et al, 2006;LeBard et al, 2008). However, one weakness of the theory is the omission of entropic contribution in the electron transfer steps.…”

Section: Resultsmentioning

confidence: 99%

Enthalpy, Entropy, and Volume Changes of Electron Transfer Reactions in Photosynthetic Proteins

Hou¹

2011

Application of Thermodynamics to Biological and Materials Science

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Application of the Marcus theory for analysis of the temperature dependence of the reactions leading to photosynthetic water oxidation: results and implications

Cited by 53 publications

References 1 publication

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

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

Enthalpy, Entropy, and Volume Changes of Electron Transfer Reactions in Photosynthetic Proteins

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