High-spin Mn–oxo complexes and their relevance to the oxygen-evolving complex within photosystem II

Abstract

The structural and electronic properties of a series of manganese complexes with terminal oxido ligands are described. The complexes span three different oxidation states at the manganese center (III-V), have similar molecular structures, and contain intramolecular hydrogen-bonding networks surrounding the Mn-oxo unit. Structural studies using X-ray absorption methods indicated that each complex is mononuclear and that oxidation occurs at the manganese centers, which is also supported by electron paramagnetic resonance (EPR) studies. This gives a high-spin Mn V -oxo complex and not a Mn IV -oxy radical as the most oxidized species. In addition, the EPR findings demonstrated that the Fermi contact term could experimentally substantiate the oxidation states at the manganese centers and the covalency in the metal-ligand bonding. Oxygen-17-labeled samples were used to determine spin density within the Mn-oxo unit, with the greatest delocalization occurring within the Mn V -oxo species (0.45 spins on the oxido ligand). The experimental results coupled with density functional theory studies show a large amount of covalency within the Mn-oxo bonds. Finally, these results are examined within the context of possible mechanisms associated with photosynthetic water oxidation; specifically, the possible identity of the proposed high valent Mn-oxo species that is postulated to form during turnover is discussed.metal-oxo complexes | water oxidation | inorganic chemistry | photosynthesis | oxygen-evolving complex P hotosynthetic water oxidation is an essential chemical reaction that is responsible for producing Earth's aerobic environment. Dioxygen production occurs at the active site of the enzyme photosystem II, referred to as the oxygen-evolving complex (OEC), which contains a unique Mn 4 CaO cluster (1, 2). Several features of the OEC are known, including an approximate arrangement of the metal ions within the cluster (Fig. 1A) (3, 4), its structural flexibility during turnover (5, 6), and its ability to store oxidizing equivalents via five photo-induced redox states (S i , i = 0-4 and known as the Kok cycle) (7). Substrate water molecules bind to the cluster and, upon oxidation, are coupled to produce dioxygen and 4 eq of protons. There is agreement that formation of the O-O bond occurs in the highest oxidized state of the Mn 4 CaO 5 cluster (S 4 ), after which the cluster reverts to the most reduced state, S 0 (1-6, 8-10). The transient S 4 state has eluded detection, making it difficult to experimentally probe the structural and physical requirements necessary to promote dioxygen production. Magnetic resonance and density functional theory (DFT) studies of the S 2 and S 3 states have been used to infer that the beginning and ending oxidation states of the Kok cycle are Mn 3 III Mn IV (S 0 ) and Mn 3 IV Mn V or Mn 3 IV Mn IV O • (S 4 ) (11-14). The location of the Mn V center within the cluster is not certain, yet one possibility is the dangling Mn A4 site, which is coordinated to anionic donors and is surrounded by a ne...

An Mn(V)–oxo role in splitting water?

“…It is also worth being reminded that, although the ground state of the Mn-O units in the OEC may be diamagnetic, thermal population of high-spin states is possible at ambient temperatures (20), and thus covalency-driven radical character on the oxo group, like that illustrated here by Gupta et al (10), may be possible even in tetragonal ligand fields.…”

“…Distinguishing between these two possibilities is crucial for understanding the mechanism of O-O bond formation, which may proceed by a radical coupling mechanism or a nucleophilic attack of a water or hydroxide on an electrophilic Mn-oxo (9). In PNAS, Gupta et al (10) reveal a middle ground in this debate by providing spectroscopic evidence for O radical character in a complex containing a formal Mn(V) ion.…”

“…In this manner, the authors demonstrate experimentally that significant spin density at the oxo ligand may be achieved in certain orbital configurations without having to invoke an O-centered radical. These works (10,14) provide a beautiful example of synthesis and spectroscopic and computational characterization of a series of trigonally symmetric Mn-oxo complexes, but what does this tell us about the nature of the OEC during O-O bond formation? The two Mn centers most often invoked as participating in the O-O bond-forming reaction in the OEC are Mn4A, the dangler manganese, and Mn1D, ligated by His332, the only histidine ligand in the first coordination sphere.…”

Proton-Coupled Electron Transfer in Organic Synthesis: Fundamentals, Applications, and Opportunities

“…Manganese-oxo complexes have also been designed for PCET and HAT reactions, and have been studied extensively in the context of the special role of manganese oxo clusters in the oxygen evolving complex of photosystem II [60][61][62][63]. Borovik has disclosed a compound with the backbone structure 4, which features an unusual non-bridging terminal hydroxo ligand, and has measured its pK a and redox properties ( Figure 7) [64][65][66].…”

Leaf optical properties and dynamics of photosynthetic activity

“…the cytosolic environment within the thylakoids), which become acidified during the process. The oxidised P 680 eventually receives a new electron from an H 2 O molecule that is split into molecular oxygen (O 2 ), electrons and protons by the PSII oxygen-evolving complex (OEC) (Antal et al 2013;Gupta et al 2015).…”