Mechanism of light induced water splitting in Photosystem II of oxygen evolving photosynthetic organisms

Abstract

The reactions of light induced oxidative water splitting were analyzed within the framework of the empirical rate constant-distance relationship of non-adiabatic electron transfer in biological systems (C. C. Page, C. C. Moser, X. Chen , P. L. Dutton, Nature 402 (1999) 47-52) on the basis of structure information on Photosystem II (PS II) (A. Guskov, A. Gabdulkhakov, M. Broser, C. Glöckner, J. Hellmich, J. Kern, J. Frank, W. Saenger, A. Zouni, Chem. Phys. Chem. 11 (2010) 1160-1171, Y. Umena, K. Kawakami, J-R Shen, N. Kamiya, Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9Å. Nature 47 (2011) 55-60). Comparison of these results with experimental data leads to the following conclusions: 1) The oxidation of tyrosine Y(z) by the cation radical P680(+·) in systems with an intact water oxidizing complex (WOC) is kinetically limited by the non-adiabatic electron transfer step and the extent of this reaction is thermodynamically determined by relaxation processes in the environment including rearrangements of hydrogen bond network(s). In marked contrast, all Y(z)(ox) induced oxidation steps in the WOC up to redox state S(3) are kinetically limited by trigger reactions which are slower by orders of magnitude than the rates calculated for non-adiabatic electron transfer. 3) The overall rate of the triggered reaction sequence of Y(z)(ox) reduction by the WOC in redox state S(3) eventually leading to formation and release of O(2) is kinetically limited by an uphill electron transfer step. Alternative models are discussed for this reaction. The protein matrix of the WOC and bound water molecules provide an optimized dynamic landscape of hydrogen bonded protons for catalyzing oxidative water splitting energetically driven by light induced formation of the cation radical P680(+·). In this way the PS II core acts as a molecular machine formed during a long evolutionary process. This article is part of a Special Issue entitled: Photosynthesis Research for Sustainability: from Natural to Artificial.

The functional role of protein dynamics in photosynthetic reaction centers investigated by elastic and quasielastic neutron scattering

“…The essential processes of photosynthetic water splitting [1,2] take place in a membrane-bound protein assembly denoted as Photosystem II (PS II). The structure of the PS II core at 3.8Å resolution [3] is shown in Fig.…”

“…1. The PS II core comprises two different types of pigment-protein complexes with distinct functional designation: i) the light-harvesting complexes CP43 and CP47 and ii) the reaction center (RC) represented by the central heterodimer D1/D2, where a light-triggered charge separation initiates the photochemical processes in PS II [1,2].…”

“…2 (see [1][2][3] and references therein). In brief, the primary charge separation leads to the generation of an ion radical pair P680 + Pheo − and subsequently to electron transfer from Pheo to a plastoquinone molecule Q A within about 300 ps [4].…”

Synthesis and characterization of chlorophyllaenol derivatives: Chlorophyllatert-butyldimethylsilyl-enol ether and 131-deoxo-131, 132-didehydro-chlorophylla

“…the water oxidizing complex (WOC) or oxygen evolving complex (OEC), in all oxygenic organisms such as the cyanobacteria, green algae and plants [41][42][43][44][45][46][47][48][49][50][51][52][53][54][55][56][57][58]. The PS II is difficult to isolate and crystallize in its water oxidizing form [43,44].…”

Microcrystallization techniques for serial femtosecond crystallography using photosystem II from Thermosynechococcus elongatus as a model system

“…It catalyses the light-driven, transmembrane electron transfer from water, which serves as the electron source, to the plastoquinone. The reaction of water oxidation involves four charge separation events, where two water molecules are oxidized, leading to the generation of four protons, four electrons and one molecule of oxygen (for a review on PSII see [14]). This reaction is unique in nature, where PSII has produced all the oxygen in the atmosphere and changed our planet from an anoxygenic to an oxygenic atmosphere 2.5 billion years ago.…”