O₂ Evolution from the Manganese−Oxo Cubane Core Mn₄O₄⁶⁺:  A Molecular Mimic of the Photosynthetic Water Oxidation Enzyme?

Abstract

Photosynthesis produces molecular oxygen from water catalyzed by an enzyme whose active site contains a tetramanganese−oxo core of incompletely established structure. The first functional mimic of this core has been synthesized containing a cubical [Mn4O4] n + core, surrounded by six facially bridging bidentate chelates to the manganese ions ((dpp)6Mn4O4 (1); dpp- = diphenylphosphinate anion). Bond enthalpy data predict that the Mn4O4 6+ core is thermodynamically capable of releasing molecular O2, but is kinetically prevented from doing so by an activation barrier. UV light absorption into a Mn−O charge-transfer excited state (but not excitation of a Mn ligand-field excited state) efficiently releases an O2 molecule if performed in the gas phase and concomitantly releases a bridging dpp- anion and the cationic species (dpp)5Mn4O2 + (presumed Mn4O2-butterfly core type). All species were identified by high resolution mass spectrometry. This reaction proceeds with high quantum efficiency (>50%) and is the only observable reaction channel. The O2 product derived exclusively from the corner oxo's of the cube based on photochemistry of the 18O-isotopomer, ((dpp)6Mn4(18O)4. Neither O2 release nor dpp- dissociation are observed individually to occur in the excited state, indicating that O−O bond formation and O2 release require dissociation of one of the six dpp- chelates (“Jack-in-the-Box” mechanism for O2 formation). By contrast, neither O2 production nor chelate photodissociation are observed in condensed phases, presumably due to either quenching of the photoexcited state or rapid recombination of dpp- and (dpp)5Mn4O4 + in the solvent cage. Previous results show that chemical reduction of (1) in solution using hydrogen atom donors produces the deoxygenated (dpp)6Mn4O2 core and releases two water molecules as the only products. Thus the [Mn4O4] n + cubane core is an intrinsically reactive core topology that facilitates both the selective chemical reduction of two of the four oxygen atom bridges to water molecules and their photorearrangement to an O2 molecule under the control of chelation of the manganese ions by dpp-. These results may offer insight into the possible nature of the photosynthetic O2-evolving mechanism.

Functional models for the oxygen-evolving complex of photosystem II

“…In the double pivot mechanism, O 2 is evolved by O-O bond formation across a face of the cube and subsequent loss of O 2 freeing two of the manganese atoms to pivot outward and open the cube (Figure 3, top). This hypothesis is supported by gas phase experiments illustrating the formation of O 2 from Mn 4 O 4 cuboidal complexes [40], as well as reduction of similar Mn 4 O 4 complexes to form Mn 4 O 2 and two water molecules [41,42]. The reduction reactions imply that the reverse oxidation reaction is possible.…”

“…Bottom: Schematic representation of the structure of the cubane-like complex synthesized by Dismukes et al as well as its proposed mechanism of oxygen evolution (Figure was reproduced from ref. [40], with permission of the copyright holders). Top: bis-porphyrin functional model for oxygen evolution (figure was reproduced from ref.…”

“…Butterfly/double pivot Mechanism-The Dismukes and Christou groups have proposed a mechanism known as the butterfly or double pivot mechanism [39,40]. This involves an OEC structure with a cubane-like geometry composed of alternating metal and oxo units.…”

“…However, ligand lability of Mn complexes can lead to instability of the catalyst under catalytic conditions, although Nature has overcome this problem of ligand lability by encapsulating the Mn ions in the OEC within the proteins of PSII. While instability is an issue for manganese model complexes, a number of successes have been reported [40,[79][80][81][82][83]. In this section, the manganese-based synthetic water-oxidation catalysts will be examined and their proposed mechanisms compared to the mechanisms proposed for the OEC.…”

“…This difference is minor if you consider that the bis-oxo species isolated in the Naruta et al system [80] can be viewed as an intermediate species formed during the final oxidation step in the Hoganson and Babcock mechanism [44]. [40,85,86]. This cubane-like complex has been shown to release one equivalent of O 2 from each tetramanganese cluster under the gas phase conditions of a laser desorption ionization mass spectrometry (LDI-MS) system when pulsed with 355 nm light.…”