Photosynthetic O ₂ Formation Tracked by Time-Resolved X-ray Experiments

Abstract

Plants and cyanobacteria produce atmospheric dioxygen from water, powered by sunlight and catalyzed by a manganese complex in photosystem II. A classic S-cycle model for oxygen evolution involves five states, but only four have been identified. The missing S4 state is particularly important because it is directly involved in dioxygen formation. Now progress comes from an x-ray technique that can monitor redox and structural changes in metal centers in real time with 10-microsecond resolution. We show that in the O2-formation step, an intermediate is formed--the enigmatic S4 state. Its creation is identified with a deprotonation process rather than the expected electron-transfer mechanism. Subsequent electron transfer would give an additional S4' state, thus extending the fundamental S-state cycle of dioxygen formation.

Mechanistic Parameters of Electrocatalytic Water Oxidation on LiMn2O4 in Comparison to Natural Photosynthesis

“…[f] Reaction order of the scaled ring with respect to OH − on the NHE scale; the reaction order with respect to H + is the negative value of the reaction order with respect to OH − . [g] Determined by XAS 88, 89. [h] Determined by photothermal beam deflection (PBD) 90, 91…”

Functional models for the oxygen-evolving complex of photosystem II

“…Another area of contention in this mechanism centers on the nature of the high-valent manganese-oxo active species. Recently, it has been proposed that rather than an Mn(V)-oxo, which has not been spectroscopicaly observed [5,50], the active species in the protein is actually a Mn(IV)-oxyl [35], a spin isomer of the Mn (V)-oxo having O radical character. With the oxyl form, Siegbahn [35] finds a 12.5 kcal/mol barrier for a terminal oxyl/bridging oxo coupling in the coordination sphere of Ca.…”

“…Oxides of metals such as iridium, ruthenium, and manganese, in addition to platinum black, are known to evolve small amounts of oxygen in the presence of strong oxidants such as Ce(IV) or oxone [16,102,103] 5 ] 6+ , also known as ruthenium red, have also been shown to have very high activity for oxygen evolution, especially when stabilized as a heterogeneous system [105][106][107]. As shown in Table 1, complexes such as Ru red have oxygen-evolution characteristics comparable to the more well-defined model systems in solution and these characteristics have been found to be considerably improved upon isolation of the catalyst in polymers such as Nafion [55].…”

“…Decades of biophysical study have provided a solid groundwork for this project. Crystal structures of photosystem II [1,2] (PSII) have revealed the location of many important components such as chlorophylls and the oxygen-evolving center (OEC) while spectroscopy such as EXAFS [3][4][5][6][7], EPR [8][9][10][11][12], and IR [13,14] have allowed the study of reactive intermediates, the composition of the OEC and the protein ligation of the metal centers. Unfortunately, while we now have a much better structural and mechanistic basis for PSII, we still are some way from the goal of a molecular mechanistic understanding of water oxidation.…”

No Evidence from FTIR Difference Spectroscopy That Glutamate-189 of the D1 Polypeptide Ligates a Mn Ion That Undergoes Oxidation during the S0 to S1, S1 to S2, or S2 to S3 Transitions in Photosystem II

“…Most interpretations of Mn-XANES data have concluded that the S 1 state consists of two Mn(III) and two Mn(IV) ions and that the S 2 state consists of one Mn(III) and three Mn(IV) ions (for review, see refs 5 and 6). Whether the additional oxidizing equivalent of the S 3 state is localized on a Mn ion (7,8) or on a Mn ligand (9,10) The amino acid residues that ligate the Mn 4 cluster are provided mainly by the D1 polypeptide, one of the core subunits of PSII. This ligation environment was predicted on the basis of spectroscopic analyses of site-directed mutants (for review, see ref 11) and has been largely confirmed by recent X-ray crystallographic studies (12,13).…”