The mechanism of photosynthetic water splitting

Abstract

Oxygenic photosynthesis, which provides the biosphere with most of its chemical energy, uses water as its source of electrons. Water is photochemically oxidized by the protein complex photosystem II (PSII), which is found, along with other proteins of the photosynthetic light reactions, in the thylakoid membranes of cyanobacteria and of green plant chloroplasts. Water splitting is catalyzed by the oxygen-evolving complex (OEC) of PSII, producing dioxygen gas, protons and electrons. O(2) is released into the atmosphere, sustaining all aerobic life on earth; product protons are released into the thylakoid lumen, augmenting a proton concentration gradient across the membrane; and photo-energized electrons pass to the rest of the electron-transfer pathway. The OEC contains four manganese ions, one calcium ion and (almost certainly) a chloride ion, but its precise structure and catalytic mechanism remain unclear. In this paper, we develop a chemically complete structure of the OEC and its environment by using molecular mechanics calculations to extend and slightly adjust the recently-obtained X-ray crystallographic model with reference to this structure and to some important recent experimental results.

Functional models for the oxygen-evolving complex of photosystem II

“…One area of contention in the nucleophilic water mechanism for the OEC that is modeled by both 1 and 7 is the location of the nucleophilic water. In the Messinger mechanism [34], the nucleophilic oxygen is a μ-oxo group, while in the mechanism proposed by McEvoy et al [31] the nucleophilic water is bound to the Ca 2+ ion. Due to similarities in oxidation state and structure to OEC in the S 2 state, complex 7 can be used as a model for μ-oxo exchange.…”

“…The result is a mechanism where a high-valent manganese-oxo is formed on the lone dangler manganese. This isolated manganese-oxo group is then proposed to react with a coordinated water or hydroxide [31,34]. The involvement of either a nucleophilic water or hydroxo is one area of contention in this mechanism.…”

“…The most recent are based on the X-ray and QM/MM structures of the OEC [31,[34][35][36]. Since the introduction of the S state cycle by Kok et al, it has been known that water is oxidized to oxygen through four distinct oxidation steps.…”

“…In an effort to determine a more detailed structure of the OEC, quantum mechanical (QM) and molecular mechanics (MM) calculations were carried out that use the parameters of the 3.5 Å crystal structure and spectroscopic data [31][32][33]. Using a model including all residues within 15 Å of any of the OEC cluster atoms, a proposed structure for the OEC was calculated using (QM/MM) methods ( Figure 1D).…”

Glutamate-354 of the CP43 polypeptide interacts with the oxygen-evolving Mn4Ca cluster of photosystem II: a preliminary characterization of the Glu354Gln mutant

“…In both structural models (Ferreira et al 2004;Loll et al 2005), this one Mn ion is ligated by Glu354 of the CP43 polypeptide. A second interpretation is that the carboxylate ligands of the Mn 4 Ca cluster are mostly insensitive to changes in the formal oxidation states of the individual Mn ions (McEvoy et al 2005;Sproviero et al 2006). This situation might arise if the S-state transitions cause little increase in the electrostatic charge of the individual Mn ions, a prediction that was obtained from a QM/MM analysis of the approximately 3.5 Å X-ray crystallographic structural model (Sproviero et al 2006 To distinguish between these two explanations, we have begun a characterization of the mutants CP43-Glu354Gln and CP43-Glu354Asp.…”