Reduction potentials of heterometallic manganese–oxido cubane complexes modulated by redox-inactive metals

Edited by Harry B. Gray, California Institute of Technology, Pasadena, CA, and approved May 3, 2013 (received for review February 11, 2013)
June 6, 2013
110 (25) 10084-10088


Understanding the effect of redox-inactive metals on the properties of biological and heterogeneous water oxidation catalysts is important both fundamentally and for improvement of future catalyst designs. In this work, heterometallic manganese–oxido cubane clusters [MMn3O4] (M = Sr2+, Zn2+, Sc3+, Y3+) structurally relevant to the oxygen-evolving complex (OEC) of photosystem II were prepared and characterized. The reduction potentials of these clusters and other related mixed metal manganese–tetraoxido complexes are correlated with the Lewis acidity of the apical redox-inactive metal in a manner similar to a related series of heterometallic manganese–dioxido clusters. The redox potentials of the [SrMn3O4] and [CaMn3O4] clusters are close, which is consistent with the observation that the OEC is functional only with one of these two metals. Considering our previous studies of [MMn3O2] moieties, the present results with more structurally accurate models of the OEC ([MMn3O4]) suggest a general relationship between the reduction potentials of heterometallic oxido clusters and the Lewis acidities of incorporated cations that applies to diverse structural motifs. These findings support proposals that one function of calcium in the OEC is to modulate the reduction potential of the cluster to allow electron transfer.
Calcium is an obligatory cofactor for water oxidation in the oxygen-evolving complex (OEC) of photosystem II, which has been structurally and spectroscopically determined to contain a CaMn4Ox cluster (Fig. 1, Left) (1). The exact role of the Ca2+ ion in catalysis is not yet understood, but the observation that only Sr2+ can functionally substitute for Ca2+ has been attributed to the similar Lewis acidities of the two cations (24). The calcium center has been proposed to coordinate water or hydroxide ligands that participate in O–O bond formation (57). Other proposed functions include affecting proton-coupled electron transfer and the redox properties of the cluster, possibly via interactions with neighboring tyrosine residues (811).
Fig. 1.
Proposed structure of the CaMn4O5 cluster in the OEC (Left) (26, 27), structure of previously studied heterometallic dioxido complexes (Center) (23), and structure of tetraoxido complexes studied here (Right).
Many other biological and synthetic electron transfer reactions are affected by the addition of Lewis acidic metal ions (12, 13). For example, synthetic FeIV–oxo complexes have shown enhanced electron transfer rates and more positive reduction potentials upon binding or addition of redox-inactive Lewis acids such as Sc3+ or Ca2+ (14, 15). Group 2 metal ions also enhanced the rates of dioxygen activation by monometallic MnII and FeII complexes (16, 17). Alkali and alkali earth metals have also been proposed as components in heterogeneous water oxidation by cobalt and manganese oxides (1822). Our group recently reported a series of heterometallic trimanganese dioxido clusters [MMn34–O)(µ2–O)] (Fig. 1, Center; M = Na+, Ca2+, Sr2+, Zn2+, and Y3+) and demonstrated that the reduction potentials of the clusters are linearly correlated with the Lewis acidity of the redox-inactive metal (23).
We have previously described a [CaMnIV3O4] cubane complex (1-Ca) (24, 25) supported by a multinucleating ligand framework (H3L, Fig. 2) that is structurally related to the CaMn3 OEC subsite proposed by crystallographic studies (Fig. 1, Right) (2630). In this work, we report the synthesis of a structurally analogous [SrMnIV3O4] complex important for understanding the functional substitution of Sr2+ for Ca2+ in the OEC. We also describe the synthesis of other [MMnIV3O4] (M = Zn2+, Y3+) and [ScMnIIIMnIV2O4] complexes that are structurally more similar to the cubane subsite of the OEC than the previously investigated dioxido clusters (MMn3O2, Fig. 1). Electrochemical studies of the isostructural series of [MMnIV3O4] compounds (M = Ca2+, Sr2+, Zn2+, Y3+, Sc3+, and Mn3+) allowed the systematic investigation of the effect of redox-inactive metal ions upon the redox properties of biologically relevant manganese clusters.
Fig. 2.
Synthesis of Complexes 1-M (M = Sr, Zn, Y).

Results and Discussion

To study whether the correlation between Lewis acidity and redox potentials of the trimanganese dioxido complexes could be extended to the tetraoxido cubane clusters that are structurally more similar to the OEC, we targeted analogs of 1-Ca with other metal ions substituted for calcium. The strontium compound [LSrMn3O4(OAc)3(DMF)]2 ([1-Sr]2, Fig. 2, DMF, N,N-dimethylformamide) was prepared analogously to 1-Ca from a low-oxidation-state trimanganese precursor supported by a triarylbenzene architecture appended with pyridine and alkoxide donors (31, 32). Treatment of a tetrahydrofuran (THF) suspension of LMnII3(OAc)3 and Sr(OTf)2 (OTf, trifluoromethanesulfonate) with KO2, followed by crystallization from DMF, afforded the strontium cubane complex ([1-Sr]2). A single crystal X-ray diffraction (XRD) study of crystals of [1-Sr]2 showed that [1-Sr]2 contains the desired [SrMn3O4] cubane cluster in a dimeric structure, with two 9-coordinate strontium centers of different monomers bridged through acetate and coordinated DMF molecules (Fig. 3A, Table S1, and Dataset S1). The Mn–oxido bond distances [1.821(3)–1.913(3) Å] as well as bond valence sum (BVS) analysis (Table S2) of the manganese–ligand distances are consistent with all MnIV centers per [SrMn3O4] cluster (33). Additionally, a pseudooctahedral high-spin d4 MnIII center is expected to be axially elongated or compressed to accommodate the single unpaired electron in the σ-antibonding orbitals; no such axial distortion is observed. Compound [1-Sr]2 allows direct comparison with 1-Ca due to their structural similarities, and is also a rare example of a molecular mixed metal Sr/Mn complex (23, 34, 35).
Fig. 3.
Truncated solid-state structures of (A) [1-Sr]2, (B) 1-Zn, and (C) [1-Y][OTf], with thermal ellipsoids at the 50% probability level. Portions of the ligand (L), hydrogen atoms, and outer-sphere anions not shown for clarity. (D) Complete solid-state structure of 2. Mn1 is the MnIII center; Mn2 and Mn3 are MnIV. Selected bond lengths (Å): Sc–O1 2.166(1), Sc–O2 2.200(1), Sc–O3 2.164(1), Mn1–O1 1.931(1), Mn1–O2 1.885(1), Mn1–O4 2.142(1), Mn2–O2 1.861(1), Mn2–O3 1.888(1), Mn2–O4 1.903(1), Mn3–O1 1.881(1), Mn3–O3 1.873(1), and Mn3–O4 1.855(1). Bolded lines emphasize the [MMn3O4] moiety.
Under the same reaction conditions, analogs of 1-Ca and [1-Sr]2 containing other metal ions were not isolated, possibly due to solubility differences. However, we previously showed that treatment of a DMF solution of 1-Ca with Sc(OTf)3 cleanly formed the scandium analog LScMn3O4(OAc)3(OTf) ([1-Sc][OTf]) (25). When 1-Ca was treated with Zn(OTf)2 in DMF (Fig. 2), electrospray ionization mass spectrometry (ESI–MS) of the reaction mixture showed a single species at 1,266 m/z, corresponding to [LZnMn3O4(OAc)2]+, with no signals corresponding to residual 1-Ca. The clean conversion of 1-Ca to LZnMn3O4(OAc)3 (1-Zn) is also demonstrated by a change in solubility; while 1-Ca is insoluble in methylene chloride and benzene, the product after treatment with Zn(OTf)2 is soluble in both. An XRD study of crystals of 1-Zn grown from benzene/diethyl ether shows that 1-Zn contains the desired [MMn3O4] moiety, structurally related to 1-Ca and [1-Sr]2, although the smaller zinc center is six-coordinate and does not bind solvent ligands (Fig. 3B). Refinement of this structure with populations of Mn in the apical site shows that the metal center is unambiguously Zn. BVS analysis [Mn–oxido distances 1.822(1)–1.947(1) Å, Table S3] supports the assignment of the compound as in the [MMnIV3O4] oxidation state.
Under the same reaction conditions using Y(OTf)3 instead of Zn(OTf)2, ESI–MS of the reaction mixture displayed a single signal at 1,350 m/z, corresponding to [LYMn3O4(OAc)3]+ (Fig. 2). An XRD study of single crystals of the product, formulated as [LYMn3O4(OAc)3(DMF)2][OTf] ([1-Y]+) shows that the compound contains a [YMn3O4] core (Fig. 3C). The yttrium center is eight-coordinate, with two O-bound DMF molecules, and the triflate counterion is outer sphere. Structural parameters support the MnIV3 oxidation state assignment [Mn–oxido distances 1.839(2)–1.912(2) Å, Table S4]. A CD2Cl2 solution of [1-Y]+ displays a paramagnetically broadened 1H NMR spectrum with signals between –21 and 16 ppm, similar to that of [1-Sc][OTf] (Fig. S1) (25).
With these complexes in hand, in addition to the previously reported compounds 1-Ca, [1-Sc][OTf], and LMn4O4(OAc)3 (24, 25), the effect of changing the redox-inactive metals in the clusters was studied electrochemically. Cyclic voltammograms (CVs) of [1-Sc]+, [1-Y]+, 1-Zn, and [1-Sr]2 (0.1 M NBu4PF6) in N,N-dimethylacetamide (DMA) showed quasireversible redox couples assigned as the [MMnIV3O4]/[MMnIV2MnIIIO4] couple at potentials of –250, –430, –630, and –940 mV, respectively, vs. the ferrocene/ferrocenium couple (Fc/Fc+) (Fig. 4). This assignment was confirmed by the chemical reduction of [1-Sc]+ using one equivalent of decamethylferrocene (Cp*2Fe) in THF (EO ∼ –0.48 vs. Fc/Fc+ in CH2Cl2) to cleanly form the one-electron reduced compound LScMnIV2MnIIIO4(OAc)3(DMF) (2·DMF) after crystallization from DMF (Fig. 5). The reduced product was confirmed by an XRD study (Fig. 3D) and further characterized by NMR spectroscopy (Fig. S2). BVS analysis of the Mn-ligand bond lengths indicate that the oxidation states of the MnIV2MnIII cluster are isolated (Table S5). The MnIII center (Mn1, Fig. 3D) shows an elongation of the O(acetate)–Mn1–O4 axis [Mn1–O(acetate) 2.134(2) Å; Mn1–O4 2.142(1) Å], while the equatorial Mn–O bond lengths are shorter [1.854(1)–1.931(1) Å]. The two MnIV centers (Mn2 and Mn3, Fig. 3D) are not axially distorted [Mn–oxido distances 1.855(1)–1.903(1) Å].
Fig. 4.
CVs corresponding to the [MMnIV3O4]/[MMnIV2MnIIIO4] redox couple (M = Mn3+, Sc3+, Y3+, Zn2+, Ca2+, and Sr2+) in 0.1 M NBu4PF6 in DMA. Scan rate of 100 mV/s. Potentials are referenced to Fc/Fc+. Values for M = Mn3+, Sc3+, and Ca2+ were previously reported (24, 25).
Fig. 5.
Reduction of [1-Sc][OTf].
The reduction potentials of 1-Ca and [1-Sr]2 are similar (E1/2 = –940 mV vs. Fc/Fc+) (24), but the reduction potential of 1-Zn is more positive by greater than 300 mV (E1/2 = –630 mV), even though Zn2+ is also a dicationic redox-inactive metal and all three complexes are neutral in charge. Similarly, although both [1-Sc]+ and [1-Y]+ contain tricationic redox-inactive metals, their reduction potentials differ by ca. 200 mV. This variation in redox potential is inconsistent with a purely electrostatic explanation of the differences in redox potentials (36). The similarity of the redox potentials of the calcium and strontium variants in comparison with those of the other analogs is consistent with the similar electronic structure of the Sr-substituted OEC, as well as the water oxidation activity observed (although lower than that of native photosystem II) (2, 37).
The E1/2 values of the [MMnIV3O4]/[MMnIV2MnIIIO4] couples measured above in DMA and those of previously prepared complexes (24, 25) were plotted against the pKa of the metal aqua ions measured in water (38), used here as a measure of the Lewis acidity of cation M (Table S6). As with the related series of trimanganese dioxido complexes (23), a linear correlation is observed (Fig. 6). Hence, the chemical property that the reduction potentials of the clusters depend on is the Lewis acidity of the incorporated redox inactive metal. The positive shift in reduction potential with increasing Lewis acidity is likely due to the increased electron-withdrawing effect upon the µ3-oxido ligands, which stabilizes the more reduced manganese oxidation state. Remarkably, both lines have similar slopes, with each pKa unit shifting the potential by ca. 100 mV, despite the differences in cluster structure, ancillary ligands, number of oxido ligands, and manganese oxidation states. The intercepts of the two series are different by ca. 900 mV, with the [MMnIV3O4] complexes having more negative reduction potentials than the corresponding [MMnIVMnIII2O2] complexes containing the same metal ions, despite the higher overall manganese oxidation state of the tetraoxido clusters. This negative shift in potential with additional oxido ligands highlights a different path for tuning the reduction potential. An increased number of oxido ligands per redox active metal shifts the potentials negatively as the cluster becomes more electron-rich and the higher Mn oxidation states are stabilized. The synthetic calcium cubane discussed here, 1-Ca, has a very negative potential compared with the thermodynamic potential of water oxidation. However, the structurally related OEC has a lower oxide–Mn ratio, likely driving the potential positively.
Fig. 6.
Reduction potentials of MMn3O4 complexes (red squares) and MMn3O2 complexes (23) (blue diamonds) vs. pKa of the corresponding M(aqua)n+ ion as a measure of Lewis acidity. Potentials were referenced to ferrocene/ferrocenium.
The similar linear dependences upon Lewis acidity of the dioxido and tetraoxido complexes suggest that a more general correlation exists between the redox potentials of mixed metal oxides and the Lewis acidity of incorporated redox-inactive metals. Such a relationship may provide a quantitative method for tuning the potentials of both homogeneous and heterogeneous metal oxide electrocatalysts, either by changing the redox-inactive metal in isostructural compounds or by increasing or decreasing the oxide content. The wide range of reduction potentials found within the [MMn3O4] clusters demonstrates that a large change in the thermodynamics of a catalyst can be effected by simple substitution, (e.g., ca. 16 kcal/mol when substituting Sc3+ for Ca2+).
In summary, [MMn3O4] cubane clusters structurally related to the CaMn3 subsite of the OEC substituted with divalent and trivalent redox-inactive metals were prepared. This series of compounds allowed for the systematic study of the electrochemical effect of the Lewis acidic metal ions on the manganese reduction potentials. Varying the Lewis acidity of the capping metal from Mn3+ to Sr2+ shifted the redox potentials of these clusters by over 1 V. These results support proposals that in addition to its other possible functions in the OEC, Ca2+ plays a role in modulating the redox potential of the manganese centers via the µ-oxido ligands. Current studies are focused on studying these effects in other metal–oxido compounds of varying structure, metal character, and oxidation state to better understand the fundamental basis for water oxidation in complex metal clusters.

Materials and Methods

Unless indicated otherwise, reactions performed under inert atmosphere were carried out in oven-dried glassware in a glovebox under a nitrogen atmosphere. Anhydrous THF was purchased from Aldrich in 18 L Pure-Pac containers. Anhydrous acetonitrile, benzene, dichloromethane, diethyl ether, and THF were purified by sparging with nitrogen for 15 min and then passing under nitrogen pressure through a column of activated A2 alumina (Zapp’s). CD2Cl2 was purchased from Cambridge Isotope Laboratories, dried over calcium hydride, then degassed by three freeze-pump-thaw cycles and vacuum transferred before use. 1H NMR spectra were recorded on a Varian 300 MHz instrument, with shifts reported relative to the residual solvent peak. 19F NMR spectra were recorded on a Varian 300 MHz instrument, with shifts reported relative to the internal lock signal. Elemental analyses were performed by Midwest Microlab and Robertson Microlit. High-resolution mass spectrometry (HRMS) was performed at the California Institute of Technology Mass Spectrometry Facility. LMn3(OAc)3, LCaMn3O4(OAc)3(THF) (1-Ca), and LScMn3O4(OAc)3(OTf) ([1-Sc][OTf]) were prepared according to previously published procedures (24, 25, 32).

Synthesis of [LSrMn3O4(OAc)3(DMF)]2 ([1-Sr]2).

In a glovebox, LMn(OAc)3 (0.310 g, 0.259 mmol) and Sr(OTf)2 (0.115 g, 0.298 mmol, 1.2 eq) were combined in a scintillation vial equipped with a stir bar. We added 10:1 THF–DME (20 mL), and the heterogeneous yellow mixture was stirred for 5 min. KO2 (0.055 g, 0.774 mmol, 3.0 eq) was added in small portions over a minute, and the mixture was stirred at room temperature for 12 h, darkening to a red–brown mixture. The reaction mixture was filtered through Celite, and the filtrate was dried in vacuo. The red–brown solid was then washed with acetonitrile, then extracted with DMF, and dried again to yield the clean product (0.030 g, 7%). HRMS–ESI (m/z): [M+H]+ calculated for C63H48N6O13Mn3Sr (no solvent coordinated to Sr), 1,350.0555; found, 1,350.0597. Single crystals of a dimer of the complex coordinated by DMF molecules were grown by vapor diffusion of diethyl ether into a DMF solution of the product at room temperature.

Synthesis of LZnMn3O4(OAc)3 (1-Zn).

In a glovebox, 1-Ca (0.044 g, 0.032 mmol) and Zn(OTf)2 (0.016 g, 0.035 mmol, 1.1 eq) were combined in a scintillation vial equipped with a stir bar and dissolved in DMF (3 mL). The brown mixture was stirred at room temperature for 15 min, then dried in vacuo. Benzene (4 mL) was added to the resulting brown solid, and the mixture was filtered through Celite to remove calcium triflate salts. The filtrate was dried in vacuo to yield the product as a red–brown solid (0.029 g, 68%). X-ray quality single crystals were grown by vapor diffusion of diethyl ether into a benzene solution of 1-Zn at room temperature. Analysis calculated for C63H48Mn3N6O13Zn: C, 57.01; H, 3.65; N, 6.33. Found: C, 56.01; H, 3.79; N, 6.11. HRMS–ESI (m/z): M+ calculated for C63H48N6O13Mn3Zn, 1,325.0712; found, 1,325.0754.

Synthesis of [LYMn3O4(OAc)3(DMF)2][OTf] ([1-Y][OTf]).

In a glovebox, 1-Ca (0.046 g, 0.0335 mmol) and Y(OTf)3 (0.020 g, 0.0368 mmol, 1.1 eq) were combined in a scintillation vial equipped with a stir bar and dissolved in DMF (3 mL). The brown mixture was stirred at room temperature for 15 min. Diethyl ether (40 mL) was added to precipitate the product as a red–brown solid. The precipitate was collected over Celite, washed with diethyl ether, then extracted with dichloromethane. The extract was dried in vacuo to yield the product as a red–brown solid (0.039 g, 71%). Single crystals for XRD were grown by vapor diffusion of diethyl ether into a DMF solution of [1-Y][OTf] at room temperature. 1H NMR (300 MHz, CD2Cl2): δ 16.1, 11.9, 11.3, 9.2, 6.1, 4.6, 1.5, –21.1 ppm. 19F NMR (CD2Cl2): δ –78.2 ppm. Anal. Calcd. for C70H62F3Mn3N8O18SY: C, 51.08; H, 3.80; N, 6.81. Found: C, 50.79; H, 3.77; N, 6.36. HRMS–ESI (m/z): M+ calculated for C63H48N6O13Mn3Y (no solvent coordinated to Y), 1,350.0479; found, 1,350.0524.

Synthesis of LScMn3O4(OAc)3(L′) (2·L′, L′ = THF or DMF).

In a glovebox, a solution of decamethylferrocene (0.006 g, 0.018 mmol, 1.4 eq) in THF (1 mL) was added to a THF solution of [1-Sc][OTf] (0.019 g, 0.013 mmol, 3 mL) The mixture was stirred for 5 min, then filtered through Celite. The filtrate was dried in vacuo. Benzene was added, and the brown mixture was filtered through Celite to remove the remaining green decamethylferrocenium triflate. The benzene filtrate was dried in vacuo, then washed with diethyl ether to yield the product as a red–brown solid (0.014 g, 78%). 1H NMR (300 MHz, C6D6): δ 22.4, 11.2, 10.3, 9.3, 5.6, 4.8, 3.6, –28.0 ppm. Anal. Calcd. for C66H55Mn3N7O14Sc [LScMn3O4(OAc)3(THF)]: C, 58.36; H, 4.09; N, 6.09. Found: C, 58.23; H, 3.36; N, 6.15. HRMS–ESI (m/z): M+ calculated for C63H48N6O13Mn3Sc (no solvent coordinated to Sc), 1,306.0980; found, 1,306.0996. X-ray quality single crystals of the product with coordinated DMF rather than THF were grown from DMF/diethyl ether.

Electrochemical Measurements.

Electrochemical measurements were recorded with a Pine Instrument Company AFCBP1 bipotentiostat using the AfterMath software package. CVs were recorded on ca. 1 mM solutions of the relevant complexes in the glovebox at 20 °C with an auxiliary Pt-coil electrode, a Ag/Ag+ reference electrode (0.01 M AgNO3, 0.1 M nBu4NPF6 in CH3CN), and a 3.0 mm glassy carbon electrode disk (Bioanalytical Systems, Inc.). The electrolyte solution was 0.1 M nBu4NPF6 in DMA. Reported potentials were referenced internally to ferrocene/ferrocenium, and are an average of at least two separate CV experiments. The measured reduction potentials typically varied by less than 15 mV between experiments.

Crystallographic Information.

CCDC 923216–923219 contain the supporting crystallographic data for this paper. These data can be obtained free of charge from The Cambridge Crystallographic Data Centre via

Data Availability

Data deposition: The atomic coordinates have been deposited in the Cambridge Crystallographic Data Centre database, (accession nos. CCDC 923216–923219).


We thank L. M. Henling for assistance with crystallography. This work was supported by the California Institute of Technology, the Searle Scholars Program, the National Science Foundation (NSF) CAREER CHE-1151918 (to T.A.), and a Sandia Campus Executive Fellowship (to E.Y.T.). The Bruker KAPPA APEXII X-ray difractometer was purchased via an NSF Chemistry Research Instrumentation award to the California Institute of Technology (CHE-0639094).

Supporting Information

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Supporting Information


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Go to Proceedings of the National Academy of Sciences
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Proceedings of the National Academy of Sciences
Vol. 110 | No. 25
June 18, 2013
PubMed: 23744039


Data Availability

Data deposition: The atomic coordinates have been deposited in the Cambridge Crystallographic Data Centre database, (accession nos. CCDC 923216–923219).

Submission history

Published online: June 6, 2013
Published in issue: June 18, 2013


  1. electrochemistry
  2. heterometallic complexes
  3. manganese clusters
  4. model complexes
  5. photosynthesis


We thank L. M. Henling for assistance with crystallography. This work was supported by the California Institute of Technology, the Searle Scholars Program, the National Science Foundation (NSF) CAREER CHE-1151918 (to T.A.), and a Sandia Campus Executive Fellowship (to E.Y.T.). The Bruker KAPPA APEXII X-ray difractometer was purchased via an NSF Chemistry Research Instrumentation award to the California Institute of Technology (CHE-0639094).


This article is a PNAS Direct Submission.



Emily Y. Tsui
Division of Chemistry and Chemical Engineering, California Institute of Technology, Pasadena, CA 91125
Theodor Agapie1 [email protected]
Division of Chemistry and Chemical Engineering, California Institute of Technology, Pasadena, CA 91125


To whom correspondence should be addressed. E-mail: [email protected].
Author contributions: E.Y.T. and T.A. designed research; E.Y.T. performed research; E.Y.T. and T.A. analyzed data; and E.Y.T. and T.A. wrote the paper.

Competing Interests

The authors declare no conflict of interest.

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