Pentanuclear clusters resembling the cubane-dangler connectivity in the native oxygen-evolving center of photosystem II

Abstract

A series of pentametallic “cubane-plus-dangler” complexes have been target synthesized. Among them, the [Fe₃Ni₂] aggregate strongly resembled the native oxygen-evolving center by mimicking the “cubane-plus-dangler” skeleton, the aqua binding site, and the connectivity between the pendent ion and the parent cubane. Our synthetic strategy that uses tri-substituted methanol as the “cubane-generator” and carboxylate as the pendant ligand provides a feasible approach for accessing model compounds of biological catalyst systems.

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The oxidation of water into dioxygen by plants, algae, and cyanobacteria is performed at the oxygen-evolving center (OEC) of photosystem II (PSII).¹ X-Ray diffraction (XRD) studies revealed that the core of the OEC consists of a low-symmetry Mn₃CaO₄ cubane motif and a “dangler” Mn ion (Scheme 1a).² To better understand the mechanism behind the formation of dioxygen and the proposed intermediates during the water oxidation process, synthetic coordination clusters as OEC mimics are highly desired. Early efforts mainly focused on reproducing the cubane structure of the native OEC by using tetra-manganese aggregations.³ Cubane analogs containing various metal ions and/or bridging atoms have also exhibited certain catalytic activity under homogeneous oxidation conditions, demonstrating the vital role of the cubane structural motif in multielectron redox processes.⁴ Following the biochemical studies on the essential role of calcium ions in the water oxidation activity of the OEC,⁵ more accurate OEC models with Mn/Ca heterometallic compounds have also been targeted.⁶ In the native OEC, the [Mn₃CaO₄] cubane core is appended with a dangling Mn ion. The latter is commonly believed to play an important role in O–O bond formation by storing multiple electron–hole pairs and binding substrate water molecules. A similar phenomenon was also observed in carbon monoxide dehydrogenases (CODHs) from Carboxydothermus hydrogenoformans, which contain [Fe₃NiS₄] cubane cores with a dangling Fe²⁺ ion on the active site.⁷ Thus, the targeted synthesis of model compounds mimicking the “cubane-plus-dangler” motif is of great importance to understand the vital role of the dangling ion in biological multielectron redox reactions. However, such complexes are extremely rare with only four known examples (Scheme 1b–e).^8–11 It should be noted that none of the reported compounds showed water binding ability neither at the cubane metal site nor at the dangling site. The absence of water binding sites and μ₂-O bridges between the dangler and the parent cubane, both of which are vital in the native OEC water oxidation process, diminished the potential of these compounds as more accurate structural mimics. Here, we report a new “cubane-plus-dangler” compound with a Zn²⁺ ion appending the [Fe₃Zn] motif. More importantly, substitution of Zn²⁺ with Ni²⁺ resulted in a new [Fe₂Ni₂]Fe complex, in which the coordination environment of the dangling ion as well as its connectivity with the parent cubane precisely resembles those of the native OEC.

Scheme 1 “Cubane-plus-dangler” structures of the native OEC (a) and the artificial mimics (b–e), highlighting the coordination environment of the dangling ions and their connectivity with the parent cubane core.

The trisubstituted methanol ligand scaffold has a strong tendency to form cubane-like metal clusters.¹² We thus decided to explore their potential to stabilize the more complex “cubane-plus-dangler” structures. The reaction of Fe(ClO₄)₃·xH₂O, Zn(OAc)₂·2H₂O, and 2-(hydroxy(bipyridin-2-yl)methyl)phenol (H₂L) in anhydrous methanol gave a dark brown solution, from which dark brown crystals with the formula [Fe₃Zn₂L₃O(OAc)₃(CH₃OH)](ClO₄)₂·(CH₃OH)_1.5 were subsequently isolated (Scheme 2). Single-crystal X-ray diffraction (XRD) studies revealed a [ZnFe₃O₄] cubane linked to a pentacoordinate “dangler” Zn²⁺via one μ₄-O and three bridging acetate ligands (Fig. 1a). The three hexacoordinated Fe³⁺ ions on the cubane are symmetrically identical and each of them is coordinated with one pyridine, one phenoxide, and two μ₃-alkoxide from L²⁻ other than the bridging μ₄-O and acetate ligand. The cubane Zn²⁺ is hexacoordinated with three pyridine and three μ₃-alkoxide from three different L²⁻. Moreover, the dangling Zn²⁺ exhibits a trigonal bipyramidal coordination configuration with three acetates, one μ₄-O, and one terminal CH₃OH molecule. It should be noted that, regardless of the metal constitution and stoichiometrical deviation, the connecting mode of the dangling ion with the parent cubane through μ₄-O and three acetate ligands is consistent with that of Zhang's Mn₄Ca¹¹ and Tilley's Co₄Mn¹⁰ and is very similar to that of Christou's Mn₃Ca₂,⁸ in which one more bridging acetate is present. However, on the native OEC, other than μ₄-O and two carboxylate groups, the dangling ion is also coordinated with the μ₂-O and terminal water molecules, both of which were proposed to play vital roles during the water oxidation process.¹³ With the goal of producing a more accurate model compound, various metal ions other than zinc were introduced and their impact on the self-assembled products was systematically investigated.

Scheme 2 Synthesis of compounds 1 and 4.

Fig. 1 Crystal structure of compound 1 (a), compound 4 (b) and the native OEC (c) (Fe: red brown; Zn: light gray; Ni: green; Ca: light blue; Mn: purple; C: dim gray; O: red; and N: blue; H atoms are omitted for clarity).

Substitution of Zn²⁺ ions by Co²⁺ and Mn²⁺ resulted in the isolation of compounds 2 and 3, respectively. XRD characterization revealed that compound 3 is isostructural with compound 1. The quality of the XRD data for compound 2 was low, but did allow determination of the unit cell and symmetry, both of which are consistent with those of compounds 1 and 3. Electrospray ionization mass spectrometry (ESI-MS) (vide infra) and ICP-OES (Fig. S2 and S3, ESI†) results also suggested that compounds 1, 2 and 3 are isostructural. Introduction of Ca²⁺ into the system failed and only resulted in a mixed-valent homometallic manganese cubane,^12b likely due to the large ionic radius of calcium, which cannot fit the cubane vertices. When Ni²⁺ was introduced into the reaction, deep red block crystals of compound 4 with the formula [Fe₃Ni₂L₃O(OAc)₂(OCH₃)(H₂O)(CH₃OH)](ClO₄)₂ were obtained (Scheme 2). XRD studies revealed an asymmetric [Fe₂Ni₂] cubane core linked to a hexacoordinate “dangler” Fe³⁺ (Fig. 1b). The Fe/Ni metal site assignment was based on the shorter average Fe–O/Fe–N bond distance and the longer Ni–O/Ni–N one.¹⁴ The ICP-OES results confirmed the Fe/Ni stoichiometry ratio of 3 : 2. The most striking structural feature of 4 is the connectivity between the dangling Fe³⁺ and the cubane core, which is through one μ₄-O, one lateral μ₂-OR and two carboxylate groups. Furthermore, the implementation of an aqua ligand at the dangling site in 4 is unprecedented, and it is an important step towards O–O bond formation via water attack and exchange processes for a truly operational OEC mimic. Consequently, this compound strongly resembles the native OEC by mimicking the “cubane-plus-dangler” skeleton, the aqua binding site on the dangling metal ion, and the connectivity between the dangling ion and the parent cubane core. We tried to investigate the catalytic reactivity of 4 for oxygen evolution reaction (OER). Unfortunately, ESI-MS studies revealed no ion peaks corresponding to the [Fe₃Ni₂] motif, suggesting that 4 is unstable in solution (Fig. S4, ESI†) and diminishing its potential as a homogenous catalyst.

It is well accepted that the presence of redox-inactive metal ions has a great impact on the redox-active constituents in both biological and artificial catalysis systems.¹⁵ For example, Ca²⁺ is essential for the water oxidation activity in the native OEC of PSII.⁵ Substitution of the Ca²⁺ by other redox-inactive metal ions increases the redox potential of the OEC and decreases the activity.¹⁶ Such a heterometallic dependence on the redox potentials has also been extensively studied in iron compounds.¹⁷ Agapie et al. demonstrated that the reduction potentials of clusters are linearly correlated with the Lewis acidity of the redox-inactive metal. Although comparisons of related compounds have only been focused on their one-electron reduction potential, this heterometallic dependence has been evidenced by the systematic electrochemical study of a series of heterometallic Fe₃M and Mn₃M compounds.¹⁸ Therefore, it is of great interest to determine whether the effects could be applied in our system.

To probe the structural integrity of these compounds in the solution/gas phase, ESI-MS measurements were conducted on CH₂Cl₂/DMF (20 : 1) solutions of crystals of 1, 2, and 3. For compound 1, a series of double charged ion peaks appeared, with mean peaks belonging to the same [Fe^III₃Zn^II₂(L)₃O(OAcCH₃)_x]²⁺ motif (Fig. 2). Similar results were observed for compounds 2 and 3 (Fig. S2 and S3, ESI†), clearly demonstrating that the core structures of all compounds remain intact. The structural homogeneity of this series of compounds, together with their structural integrity in solution, allowed us to electrochemically investigate the effect of changing heterometal ions in the clusters on the iron reduction potentials. Cyclic voltammograms (CVs) in CH₂Cl₂/DMF (20 : 1) showed quasireversible redox processes assigned as the [Fe^III₃M^II₂]/[Fe^III₂Fe^IIM^II₂] couple at −636 (M^II = Zn^II), −649 (M^II = Co^II) and −695 mV (M^II = Mn^II) vs. the ferrocenium/ferrocene couple (Fc⁺/Fc) (Fig. S5, ESI†). The decrease in the reduction potential observed here correlates with the trend of increased Lewis acidity of the heterometal ions.¹⁹ Although the potential differences are not significant due to the small variations in their heterometal ion pK_a values, such a Lewis acidity dependence is reproducible under identical conditions. Hence, the reduction potentials of the iron clusters can be tuned by incorporating heterometal ions with different Lewis acidity. Our results also suggested that this effect is not just limited to redox-inactive metals and can be extended to other 3d metals.

Fig. 2 ESI-MS of compound 1 in DCM/DMF (20 : 1). Charge states are indicated as 2+. Experimental (black) and simulated (red) mass spectra of the isotopic envelopes are exhibited. The formulas of each species are given in the table.

In summary, a pentanuclear [Fe₃Zn₂] cluster was synthesized and structurally characterized, the structure of which exhibits high similarity to that of the native OEC. Substitution of Zn²⁺ with Co²⁺ and Mn²⁺ resulted in isostructural compounds. Electrochemical investigation revealed that the reduction potentials of the iron clusters can be tuned by using the Lewis acidity of the incorporated heterometal ions. Replacement of Zn²⁺ by Ni²⁺ produced a new model compound that perfectly mirrors the “cubane-plus-dangler” skeleton, the aqua binding site on the dangling metal ion, and the connectivity between the dangling ion and the parent cubane core of the native OEC. Our synthetic strategy that uses tri-substituted methanol as the “cubane-generator” and carboxylate as the pendant ligands provides a feasible approach for accessing model compounds of biological catalyst systems. Although these heterometallic clusters showed no catalytic activity for OER, they could be employed as single-source precursors for the synthesis of corresponding mixed-metal oxide materials for potential OER catalysts.²⁰ This work is currently underway in our laboratory.

This work was supported by the National Natural Science Foundation of China (21471066 and 21871105). We would like to acknowledge the BL17B beamline of the National Center for Protein Sciences Shanghai (NFPS) at the Shanghai Synchrotron Radiation Facility (SSRF).

Conflicts of interest

There are no conflicts to declare.

Notes and references

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Footnote

† Electronic supplementary information (ESI) available. CCDC 2033749–2033751. For ESI and crystallographic data in CIF or other electronic format see DOI: 10.1039/d0cc07050e

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