Synthetic model of the asymmetric [Mn ₃ CaO ₄ ] cubane core of the oxygen-evolving complex of photosystem II

Abstract

The laboratory synthesis of the oxygen-evolving complex (OEC) of photosystem II has been the objective of synthetic chemists since the early 1970s. However, the absence of structural information on the OEC has hampered these efforts. Crystallographic reports on photosystem II that have been appearing at ever-improving resolution over the past ten years have finally provided invaluable structural information on the OEC and show that it comprises a [Mn 3 CaO 4 ] distorted cubane, to which is attached a fourth, external Mn atom, and the whole unit attached to polypeptides primarily by aspartate and glutamate carboxylate groups. Such a heterometallic Mn/Ca cubane with an additional metal attached to it has been unknown in the literature. This paper reports the laboratory synthesis of such an asymmetric cubane-containing compound with a bound external metal atom, [Mn IV 3 Ca 2 O 4 ðO 2 CBu t Þ 8 ðBu t CO 2 HÞ 4 (1)] . All peripheral ligands are carboxylate or carboxylic acid groups. Variable-temperature magnetic susceptibility data have established 1 to possess an S ¼ 9∕2 ground state. EPR spectroscopy confirms this, and the Davies electron nuclear double resonance data reveal similar hyperfine couplings to those of other Mn IV species, including the OEC S 2 state. Comparison of the X-ray absorption data with those for the OEC reveal 1 to possess structural parameters that make it a close structural model of the asymmetric-cubane OEC unit. This geometric and electronic structural correspondence opens up a new front in the multidisciplinary study of the properties and function of this important biological unit.crystal structure | magnetic properties | spectroscopic properties P hotosystem II (PSII) is a multicomponent assembly of proteins and cofactors that is located in the thylakoid membrane of plants, algae, and cyanobacteria. It carries out the sunlightdriven oxidation of water to O 2 , the generated protons driving ATP synthase and the electrons providing the reducing equivalents that ultimately lead to carbon dioxide fixation. The oxidation of water is an energetically demanding process, but the development approximately 2.7 billion years ago of a catalytic system capable of carrying it out efficiently made available as a raw material the vast quantities of water on the planet. The site of water oxidation to O 2 is the oxygen-evolving complex (OEC), and the determination of its structure has been the focus of much study by various biochemical and spectroscopic techniques. X-ray absorption spectroscopy (XAS), including extended X-ray absorption fine structure (EXAFS) and X-ray absorption near edge spectroscopy (XANES), have been invaluable tools in assessing possible metal topologies and distances between atoms that compose the OEC. These studies, along with those by EPR spectroscopy, have allowed for the description of Mn oxidation states at each of the S states (S n , where n ¼ 0-4) of the Kok cycle. Many groups have employed such spectroscopic data to guide their efforts toward the preparation of inorganic mod...

Artificial photosynthesis: understanding water splitting in nature

“…While the points above pose interesting theoretical questions, from a more practical perspective, the static properties of heterobimetallic cubane appear to be universal and can be reproduced in simpler model compound systems [89][90][91]. Similarly, heterogeneous Mn/Ca materials already show reasonable, if somewhat slow water splitting capacity normalized to Mn content [82,92,93].…”

From natural to artificial photosynthesis

“…Given that ruthenium is not an abundant metal, attention has been focused on the design and synthesis of watersplitting catalysts composed of readily available elements such as Mn, Co, Fe [66,67,86]. Remarkable advances were recently achieved by Agapie and co-worker [87] and Christou and co-worker [88] in the synthesis of Mn 3 CaO 4 -clusters (figure 9a,b) geometrically very closely resembling the Mn 4 Ca-cluster of PSII. These PSII-mimics have yet to be investigated for any catalytic activity and almost certainly will require further modification of their coordination spheres to give stability and facilitate efficient water-splitting properties.…”

“…Selected synthetic electrocatalysts that mimic the [Mn 4 Ca]-cluster and the active sites of hydrogenases. Synthetic [Mn 3 CaO 4 ]-clusters designed by Agapie and co-workers (a) [87] and Christou and co-workers (b) [88]; Co 4 O 16 core stabilized within [PW 9 O 34 ] ligand synthesized by Hill and co-workers (c) [89]; Nocera CoPi solid catalyst and its proposed atomic structure (d) [90]; synthetic [FeFe] and [NiFe] models designed by Pickett and co-workers [91] and Ogo and co-workers [92] (e) and (f ); bioinspired model designed by Dubois and co-workers (g) [93]. Figure 10.…”

Structural Changes of the Oxygen-evolving Complex in Photosystem II during the Catalytic Cycle

“…8. Such an O-5 shuffling possibility has been suggested by Pantazis and co-workers (48,49), but as a reason for the change from the S 2 low spin (S ϭ 1/2) (multiline species) to S 2 high spin state (S ϭ 7/2) (g ϭ 4 species for spinach and g ϭ 6 -10 for T. elongatus), and by Isobe et al (57) Thus far, Mn/Ca heteronuclear complexes have been synthesized by Christou and co-workers and Agapie and co-workers (58,59). The Mn We have considered two possible structural models for the S 3 state, if a Mn 3 CaO 4 closed cubane-like moiety is formed in this state as follows: one with five coordinated Mn1 upon oxygen O-5 shuffling, and the other with six coordinated Mn1 and no oxygen shuffling.…”