Role of oxido incorporation and ligand lability in expanding redox accessibility of structurally related Mn 4 clusters† Jacob S. Kanady, a Rosalie Tran, b Jamie A. Stull, c Luo Lu, c Troy A. Stich, c Michael W. Day, a Junko Yano, * b R. David Britt * c and Theodor Agapie * a Photosystem II supports four manganese centers through nine oxidation states from manganese(II) during assembly through to the most oxidized state before O 2 formation and release. The protein-based carboxylate and imidazole ligands allow for significant changes of the coordination environment during the incorporation of hydroxido and oxido ligands upon oxidation of the metal centers. We report the synthesis and characterization of a series of tetramanganese complexes in four of the six oxidation states from Mn II 3 Mn III to Mn III 2 Mn IV 2 with the same ligand framework (L) by incorporating four oxido ligands. A 1,3,5-triarylbenzene framework appended with six pyridyl and three alkoxy groups was utilized along with three acetate anions to access tetramanganese complexes, Mn 4 O x , with x ¼ 1, 2, 3, and 4. Alongside two previously reported complexes, four new clusters in various states were isolated and characterized by crystallography, and four were observed electrochemically, thus accessing the eight oxidation states from Mn II 4 to Mn III Mn IV 3 . This structurally related series of compounds was characterized by EXAFS, XANES, EPR, magnetism, and cyclic voltammetry. Similar to the ligands in the active site of the protein, the ancillary ligand (L) is preserved throughout the series and changes its binding mode between the low and high oxido-content clusters. Implications for the rational assembly and properties of high oxidation state metal–oxido clusters are presented. 1 Introduction In biological systems, the oxidation of water to dioxygen is performed by the oxygen-evolving center (OEC) of photosystem II (PSII). 1 In the catalytic cycle, or Kok cycle, 2,3 four photo- generated oxidizing equivalents sequentially oxidize the OEC, which releases O 2 upon the fourth oxidation. Although the oxidation states are still debated, 4 a common assignment of the intermediates, denoted S n states (n ¼ 0–4), range in oxidation state from S 0 , Mn III 3 Mn IV , to S 4 , Mn IV 4 –ligand radical or Mn IV 3 Mn V . 1,5–7 While highly efficient, the OEC must be reas- sembled frequently under full solar ux due to photooxidative damage to the inorganic cluster and D1 peptide. 8 The process by which the OEC is assembled, called photoactivation, 9 uses Mn 2+ , Ca 2+ , Cl , water, and oxidizing equivalents generated by light absorption. 10–12 Although bicarbonate is not coordinated to the fully assembled OEC, 13,14 spectroscopic evidence supports a role for bicarbonate in photoactivation of the cluster. 15–17 Kinetically distinct species in photoactivation have been dened, 17–22 and reduction of the intermediates in the Kok cycle have led to species in oxidation states lower than S 0 (S n with n ¼1, 2, 3) with S 3 corresponding to a putative Mn II Mn III 3 oxidation state. 23–26 A remarkable characteristic of PSII is its ability to support four manganese centers over a considerable span of oxidation states from four Mn II at the beginning of photoactivation through to four Mn IV before O–O bond formation utilizing the same, protein-dened set of carboxylate and imidazole ligands. To do so, water is concurrently incorporated and deprotonated to form hydroxido and oxido donors that stabilize the higher oxidation states of the Mn 4 CaO x cluster. Moreover, during catalytic turnover, lower oxidation state and lower oxygen-atom content moieties must be generated upon loss of O 2 . Thus, the protein-derived ligand set available must stabilize the constant reorganization, reoxidation, and reoxygenation of the Mn 4 CaO x cluster. A large effort to synthetically model the OEC has produced a variety of di-, tri-, and tetramanganese–oxido clusters. 27–29 These a Department of Chemistry and Chemical Engineering, California Institute of Technology, 1200 E. California Blvd MC 127-72, Pasadena, CA 91125, USA. E-mail: [email protected]b Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA c Department of Chemistry, University of California – Davis, One Shields Ave., Davis, CA 95616, USA † Electronic supplementary information (ESI) available: Synthetic procedures, NMR spectroscopy, cyclic voltammetry, spectroscopic methods and crystallographic details. CCDC 858642, 858643, 842512 and 938750. For ESI and crystallographic data in CIF or other electronic format see DOI: 10.1039/c3sc51406d Cite this: Chem. Sci., 2013, 4, 3986 Received 20th May 2013 Accepted 18th July 2013 DOI: 10.1039/c3sc51406d www.rsc.org/chemicalscience 3986 | Chem. Sci., 2013, 4, 3986–3996 This journal is ª The Royal Society of Chemistry 2013 Chemical Science EDGE ARTICLE Published on 19 July 2013. Downloaded by Michigan State University on 28/08/2013 15:48:01. View Article Online View Journal | View Issue
94720, USAcDepartment of Chemistry, University of Calif
95616, USA
† Electronic supplementary informationNMR spectroscopy, cyclic voltammcrystallographic details. CCDC 858642, 85crystallographic data in CIF or o10.1039/c3sc51406d
Cite this: Chem. Sci., 2013, 4, 3986
Received 20th May 2013Accepted 18th July 2013
DOI: 10.1039/c3sc51406d
www.rsc.org/chemicalscience
3986 | Chem. Sci., 2013, 4, 3986–399
Role of oxido incorporation and ligand lability inexpanding redox accessibility of structurally relatedMn4 clusters†
Jacob S. Kanady,a Rosalie Tran,b Jamie A. Stull,c Luo Lu,c Troy A. Stich,c
Michael W. Day,a Junko Yano,*b R. David Britt*c and Theodor Agapie*a
Photosystem II supports four manganese centers through nine oxidation states from manganese(II) during
assembly through to the most oxidized state before O2 formation and release. The protein-based
carboxylate and imidazole ligands allow for significant changes of the coordination environment during
the incorporation of hydroxido and oxido ligands upon oxidation of the metal centers. We report the
synthesis and characterization of a series of tetramanganese complexes in four of the six oxidation
states from MnII3MnIII to MnIII
2MnIV2 with the same ligand framework (L) by incorporating four oxido
ligands. A 1,3,5-triarylbenzene framework appended with six pyridyl and three alkoxy groups was
utilized along with three acetate anions to access tetramanganese complexes, Mn4Ox, with x ¼ 1, 2, 3,
and 4. Alongside two previously reported complexes, four new clusters in various states were isolated
and characterized by crystallography, and four were observed electrochemically, thus accessing the eight
oxidation states from MnII4 to MnIIIMnIV
3. This structurally related series of compounds was
characterized by EXAFS, XANES, EPR, magnetism, and cyclic voltammetry. Similar to the ligands in the
active site of the protein, the ancillary ligand (L) is preserved throughout the series and changes its
binding mode between the low and high oxido-content clusters. Implications for the rational assembly
and properties of high oxidation state metal–oxido clusters are presented.
1 Introduction
In biological systems, the oxidation of water to dioxygen isperformed by the oxygen-evolving center (OEC) of photosystemII (PSII).1 In the catalytic cycle, or Kok cycle,2,3 four photo-generated oxidizing equivalents sequentially oxidize the OEC,which releases O2 upon the fourth oxidation. Although theoxidation states are still debated,4 a common assignment of theintermediates, denoted Sn states (n ¼ 0–4), range in oxidationstate from S0, MnIII
3MnIV, to S4, MnIV4–ligand radical or
MnIV3MnV.1,5–7 While highly efficient, the OEC must be reas-
sembled frequently under full solar ux due to photooxidativedamage to the inorganic cluster and D1 peptide.8 The process by
l Engineering, California Institute of
7-72, Pasadena, CA 91125, USA. E-mail:
rkeley National Laboratory, Berkeley, CA
ornia – Davis, One Shields Ave., Davis, CA
(ESI) available: Synthetic procedures,etry, spectroscopic methods and8643, 842512 and 938750. For ESI andther electronic format see DOI:
6
which the OEC is assembled, called photoactivation,9 usesMn2+, Ca2+, Cl�, water, and oxidizing equivalents generated bylight absorption.10–12 Although bicarbonate is not coordinated tothe fully assembled OEC,13,14 spectroscopic evidence supports arole for bicarbonate in photoactivation of the cluster.15–17
Kinetically distinct species in photoactivation have beendened,17–22 and reduction of the intermediates in the Kokcycle have led to species in oxidation states lower thanS0 (Sn with n¼�1,�2,�3) with S�3 corresponding to a putativeMnIIMnIII
3 oxidation state.23–26
A remarkable characteristic of PSII is its ability to supportfour manganese centers over a considerable span of oxidationstates from four MnII at the beginning of photoactivationthrough to four MnIV before O–O bond formation utilizing thesame, protein-dened set of carboxylate and imidazole ligands.To do so, water is concurrently incorporated and deprotonatedto form hydroxido and oxido donors that stabilize the higheroxidation states of the Mn4CaOx cluster. Moreover, duringcatalytic turnover, lower oxidation state and lower oxygen-atomcontent moieties must be generated upon loss of O2. Thus, theprotein-derived ligand set available must stabilize the constantreorganization, reoxidation, and reoxygenation of the Mn4CaOx
cluster.A large effort to synthetically model the OEC has produced a
variety of di-, tri-, and tetramanganese–oxido clusters.27–29 These
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models have provided invaluable spectroscopic benchmarks inthe characterization of the OEC and have helped elucidate thechemistry of multinuclear clusters in general. No single systemhas been shown to stabilize manganese oxidation states aswidely as PSII. We report herein a synthetic framework with awell-dened ligand set that supports tetranuclear, manganese–oxido clusters over the eight oxidation states from MnII
4 toMnIIIMnIV
3.Stepwise oxido incorporation stabilizes the increasing
oxidation state, which vary from MnII4 to MnIIIMnIV
3 with one,two, three, and four oxido donors. Structural (XRD) and spec-troscopic (XAS, EPR) characterization, interconversion of theseclusters, the role of the ancillary ligands, and the relation to theOEC are discussed.
2 Results and discussion2.1 Synthesis of tetramanganese clusters
We have reported a ligand framework – 1,3,5-tris(2-di(20-pyridyl)hydroxymethylphenyl)benzene (H3L) (Scheme 1) – that supportsmultimetallic complexes of a variety of rst-row transitionmetals.30–32 Starting from H3L, trimanganese(II) complex 1 wassynthesized upon in situ deprotonation and reaction with threeequivalents of MnII(OAc)2 (Scheme 1).31 Trinuclear species 1 hasbeen used as a precursor for the synthesis of complexes dis-playing Mn4O4 (6) and Mn3CaO4 cubane moieties as structural
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models of the OEC.32 In order to access tetramanganese clustersin a range of oxidation states and oxido content, 1 was treatedwith oxygenating reagents and MnII precursors under a varietyof reaction conditions.
Addition of a solution of Mn(OTf)2$CH3CN (OTf ¼ tri-uoromethanesulfonate) in tetrahydrofuran (THF) to asuspension of 1 in THF followed by one equivalent of iodoso-benzene (PhIO) led to a color change from yellow to brown/purple over two hours (Scheme 1). Electrospray ionization massspectrometry (ESI-MS) analysis of puried purple productsuggests oxygen and manganese incorporation, with peaks at1417.0 and 1268.3 m/z – [LMn4O1(OAc)3(OTf)]
+ and[LMn4O1(OAc)3]
+. A single crystal X-ray diffraction (XRD) studyis consistent with the ESI-MS ndings and supports the struc-ture of 3 as a tetramanganese monooxido species (vide infra).
The addition of KO2 to an equimolar mixture of 1 andMn(OAc)2 or Mn(OTf)2$CH3CN allowed the isolation of differentcomplexes as a function of reaction solvent. A brown solid 2precipitated from the heterogeneous mixture of 1, Mn(OAc)2,and KO2 in THF upon stirring for four days. ESI-MS of 2 shows asingle peak at 1268.4 m/z, corresponding to [LMn4O1(OAc)3]
+,and an XRD study conrms the structure of 2 as a tetra-manganese monooxido species similar to complex 3.
The reaction of 1 with KO2 and Mn(OAc)2 in acetonitrilegenerated tan precipitate 4 aer 3.5 days of stirring. As observedin THF, 2 was the major species in solution at early reaction
ed arrows represent conceptual conversions involving water, proton and electronthanesulfonate. Fc+ = ferrocenium.
times (<10 h, 1H NMR spectroscopy), yet as the reaction pro-gressed, 4 became dominant. The ESI-MS spectrum displaysmajor peaks at 1225.2, 1268.2, and 1285.0 m/z, assigned to[LMn4O2(OAc)2]
+, [LMn4O1(OAc)3]+, and [LMn4O2(OAc)3H]+,
respectively. Vapor diffusion of Et2O into a DMF solution of 4gave crystals amenable to XRD (vide infra).
Complexes 2–6 are 1H NMR active with paramagneticallybroadened and shied peaks. While the resonances could notbe assigned to specic protons, NMR was still useful inobserving the reaction mixtures and purity of the samples.The synthesis and structure of complexes 5 and 6 have beenreported elsewhere.32,33 The cubane moiety of 6 could be furtherfunctionalized by selective removal of an acetate ligand withone equivalent of trimethylsilyl triate followed by addition ofnitrogenous donors such as dimethylpyrazole (eqn (1)). Thisreaction sequence allowed isolation of a cationic MnIII
2MnIV2O4
cubane complex (7).
(1)
Although a large variety of manganese cluster models of theOEC have been reported,27,28 the family of compounds reportedhere is unique in displaying signicant variation in oxidationstate and the number of oxido ligands for four manganesecenters supported by the same set of ancillary ligands. Previ-ously reported tetramanganese–oxido complexes vary inshape, containing buttery,34 planar,35 linear,36 cubic,37,38 ada-mantane,39 and dimer-of-dimer40,41 geometries. The isolation ofoxido-content homologs is rare.42,43
2.2 Solid-state structures
The crystal structure of 3 shows three basal metal centersbridged by three alkoxides forming a six-membered ring, andthe pyridines of each dipyridyloxymethyl moiety coordinate toadjacent metal centers. This motif is conserved from the tri-nuclear 1.31 A centrally located m4-oxido and three k2-acetatesbridge these three basal manganese centers to a fourthmanganese that is capped by a triuoromethanesulfonate(Fig. 1). An outer sphere triuoromethanesulfonate is present inthe solid-state, consistent with a MnII
2MnIII2 oxidation state
assignment. Comparison to structurally related Mn4–m4-Omotifs that have been previously characterized44–51 supports thepresence of MnII and/or MnIII in 3. Elemental analysis resultsindicate the presence of two triate anions in the isolatedcrystalline powder, supporting the oxidation state assignmentas MnII
2MnIII2. In agreement, the cyclic voltammogram of 3
shows two reduction events (Fig. S7†), accessing MnII3MnIII and
MnII4 oxidation states.
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In contrast to 3, 2 has the apical metal center capped by anacetate rather than triuoromethanesulfonate and no outersphere anion, indicating a one-electron reduced state, assignedas MnII
3MnIII (Fig. 1). The acetate bridging Mn3–Mn4 adoptstwo bridging modes, one mode is the usual k2 mode as in theother acetates and the other with a single oxygen atom formingthe bridge, as shown in Figure 1. Mn1 has a shorter bond to O4(the central m4-oxido) than the other three Mn centers: 1.919(4)versus 2.041(4), 2.049(4), and 2.157(3). This short distance ismost consistent with the literature MnIII–oxido distances inMn4–m4-O motifs,44–51 while the other three distances matchMnII–oxido distances. Furthermore, the successful conversionof 3 to 2 with one equivalent of a one-electron reductant indi-cates that 3 and 2 differ by a single electron in oxidation state,consistent with oxidation state assignments of 2 and 3 as stated(vide infra).
For 4, the trimanganese–tris-m2-alkoxide core as found in 1–3is present, and similar to 2, a m4-oxide and two k2-acetatesconnect the fourth manganese center to the basal trinuclearcore. Unlike 2 and 3, however, a second oxido ligand is present,bridging the apical manganese to a basal manganese (O11 of 4in Fig. 1). Analysis of the structural parameters supports anoxidation state assignment as MnII
2MnIII2. Within the diamond
core, the Mn–O bond distances are Mn4–O11, 1.8576(17) A;Mn4–O10, 1.8295(17) A; Mn1–O11, 1.8638(19) A; Mn1–O10,1.9639(16) A; and the Mn1–Mn4 distance is 2.7921(6) A. Theseparameters are consistent with MnIII. The other manganesecenters in the base have similar Mn–alkoxide and Mn–pyridinedistances to 1, and are thus assigned as MnII ions. TheMn4(m4-O)(m2-O) structural motif has not been previouslydescribed, although Mn4O2 complexes of buttery,34 planar,35
fused-cubane,52 and ladder-like53 shapes have been reported, forexample.
The solid state structure of 7 parallels the structures ofcomplexes 5 and 6 that have been reported previously.32,33
Different from 1–4, the three alkoxides bind terminally to threeMn centers, three pyridines are unbound, and the Mn4 unitmoves away from the triarylbenzene framework. In 7, one of thebridging acetates is replaced with two 3,5-dimethylpyrazolesthat p-stack with a pyridine of the ligand framework (Fig. 1).The N–H groups of the pyrazoles H-bond to a triate coun-terion. As in 6, two manganese centers show axial distortionas expected for pseudo-octahedral MnIII, and two have shorterMn–O distances consistent with MnIV (Table 1).
The four manganese centers in 2, 3, 5, 6, and 7 form atetrahedron with the pseudo-C3 axis of the ligand architecturecoincident with one of the C3 axes of the tetrahedron. Complex 4is more asymmetric, with the top manganese leaning off-axis toaccommodate the MnIII
2O2 diamond core. It is remarkable thatthe four manganese centers hold the same relative geometry infour different oxidation states (eight including electrochemi-cally observed species; see below and ESI†) and the incorpora-tion of four oxides. This tetrahedron contracts as the oxidocontent increases: this translates into shorter average metal–oxido and metal–metal distances (Table 1). For example, theaverage Mn–Mn distances decreases from 3.32 � 0.21 A in 3 to2.92 � 0.10 A in 6.
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Fig. 1 Solid-state structures of complexes 2–5 and 7. Top: depictions of full molecules 2 and 7; bottom: truncated Mn4Ox cores. Thermal ellipsoids are drawn at 50%probability. Hydrogen atoms, outersphere anions, and solvent molecules are not shown for clarity. Bolded bonds highlight the Mn4Ox cores. See ESI† for detailedcrystallographic information. The structure of complex 5 has been reported previously.33
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2.3 XAS
Mn XANES. Mn K-edge X-ray absorption near-edge spectroscopy(XANES) was used to further characterize the metal oxidationstates for complexes 3–6. In addition to the oxidation state,XANES is also sensitive to the coordination environmentsurrounding the metal site.54 Fig. 2 compares the Mn XANESspectra of these four complexes with the spectrum of the OEC inthe S1-state. Although the spectral features may be inuenced bythe variation in geometry and the number of oxido ligands, theabsorption energy shis and edge shapes are consistent withthe Mn oxidation state assignments summarized in Table 1.There is a clear trend of the rising edge position shiing tohigher energy with increasing Mn oxidation.
To determine the absorption edge positions for complexes3–6, inection-point energies (IPE) from second-derivative zerocrossings were obtained. The following values are the calculatedIPEs for the four complexes: 6547.7 � 0.1 eV (3), 6548.0 � 0.1 eV(4), 6549.7 � 0.1 eV (5), and 6551.2 � 0.1 eV (6). Previous studies
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on sets of model Mn complexes with similar ligands have shownthat the IPE increases by 1–2 eV to higher energy upon Mnoxidation.55,56Changing from complexes 4 to 5 and 5 to 6 gives anobserved IPE shi of �1.5–1.7 eV to higher energy, providingsupport forMn oxidation state increase. In contrast, the IPE shiis only �0.3 eV between complexes 3 and 4, suggesting that noMn-based oxidation occurs in this conversion. The small IPEshi observed here is likely due to the additional oxido ligand.
The absorption edge energy position of complex 6 is closestto that for the S1-state of PSII, where the formal Mn oxidationstate is assigned as MnIII
2MnIV2.57–59 Taken together with the
structural analysis and chemical reactivity of these fourcomplexes, the Mn XANES results support the formal oxidationstate assignments of 3–6 as MnII
2MnIII2 (3), MnII
2MnIII2 (4),
MnIII4 (5), and MnIII
2MnIV2 (6).
Mn EXAFS. Complexes 3–6 have also been characterized byMn K-edge extended X-ray absorption ne structure (EXAFS),and the detailed curve-tting parameters are summarized inTable S1.† In general, the EXAFS results for these four
a The bond distance with the corresponding XRD esd in parentheses aregiven for Mn centers with one Mn–O bond. The average Mn–O distancewith a standard deviation are given for Mn centers with multiple Mn–Obonds. Complexes 5 and 6 have been reported previously.32,33 Thesemetrics are included here for comparison. The Mn labels for 6 areequivalent to those given in ref. 32, Fig. 2c.
Fig. 2 Normalized Mn K-edge XANES spectra from complexes 3–6 comparedwith the spectrum from spinach PSII in the S1-state.
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complexes agree well with the solid-state structure distancesreported in Table 1 (see also Table S1; see ESI† for discussion ofthe Mn EXAFS results).
2.4 Magnetism
Magnetic susceptibility measurements were performed onpowdered crystalline samples of 3–6 in the temperature range4–300 K. At room temperature, the cMT values approach 10.3,10.5, 5.0, and 6.0 cm3 Kmol�1, respectively (Fig. 3). All are belowthe spin-only values at 300 K and decrease as temperaturedecreases, indicative of dominant antiferromagnetic coupling.Antiferromagnetically coupled manganese clusters in the liter-ature have also shown signicant deviation at 300 K from theexpected spin-only value.60–64
For 3, the cMT value decreases to 6.8 cm3 mol�1 K at 45 K andthen increases to amaximum value of 7.2 at 10 K before droppingagain, likely due to low temperature effects suchas intermolecularexchange interactions. Upon cooling, the cMT value of 4 decreasesgradually and then drops sharply below 30 K and does notapproachanobvious limiting valueat 4K.ThecMT valueof5and6decrease gradually to 0.4 and 0.8 cm3mol�1 K at 4 K, respectively.
To determine the magnitude of exchange between neigh-boring metal centers in 3, 4, and 6, the magnetic behavior of thecompounds was analyzed using the isotropic spin Hamiltonianconsidering the three exchange pathways of an asymmetrictetrahedron (see ESI† for coupling scheme). Ideally, a four Jcoupling scheme would be used to model all of the differentMn–Mn interactions; however, to determine the eigenvaluesusing the Kambe65 method, we modeled the four MnIIMnIII
interactions in each of 3 and 4 with one J (Jnm in Table 2).Similarly, the four MnIIIMnIV interactions in 6 were modeledwith one coupling constant. The J values for all coupling path-ways are relatively small (<25 cm�1, ca. 0.07 kcal mol�1) withantiferromagnetic values greater than ferromagnetic values,consistent with the decreasing cMT values.
The exchange parameters of 5 were analyzed using a twoexchange pathway model based on the pseudo-C3 symmetryof 5 (see ESI†).66 Both types of MnIIIMnIII interactions wereantiferromagnetic, with couplings of �39.3 cm�1 between thethree, basal ve-coordinate Mn and �30.7 cm�1 between the
Fig. 3 cMT vs. T data (circles) and fits (lines) for compounds 3–6. See Table 2 forfit parameters.
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a n and m refer to the oxidation states of the Mn centers whoseinteraction the coupling constant is representing. n ¼ 2 and m ¼ 3 forcomplexes 3 and 4, whereas n ¼ 3 and m ¼ 4 for 6. b JTOP describes tothe three interactions of the six-coordinate MnIII center with the ve-coordinate MnIII centers in 5. JBOT describes the interactions betweenthe three ve-coordinate MnIII centers.
Fig. 4 Temperature-dependent (see legends for temperatures employed) CWX-band EPR spectra of the frozen solutions of (from top to bottom) 3 (dissolved in1 : 1 dichloromethane–acetonitrile), 4 (dissolved in pure dichloromethane), 5–6(dissolved in 1 : 1 dichloromethane–toluene), and 7 (dissolved in pure toluene).Experimental parameters: microwave frequency ¼ 9.33–9.37 GHz; power ¼2.0 mW for all complexes except power ¼ 1.0 mW for complex 3, 0.02 mW forcomplex 4, and 0.5 mW for complex 7; modulation amplitude ¼ 10 G; modula-tion frequency ¼ 100 kHz. Data for complex 6 are staggered for ease ofcomparison. The signal from a small amount of contaminating mononuclear MnII
was subtracted from the data for complex 7.
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top, six-coordinate Mn and the basal, ve-coordinate Mn. Thesevalues are similar to MnIII
2(m3-O)2 systems with similar Mn–O–Mn angles.34
2.5 EPR
X-band continuous-wave (CW) EPR studies were performed onfrozen solution samples of complexes 3–7 (Fig. 4). All speciesexplored exhibit signicant temperature-dependent lineshapechanges. These spectral changes are diagnostic of exchange-coupled spin systems with (at least some) rather small exchangecoupling constants (i.e. on the order of kBT), consistent withmagnetic susceptibility results (Table 2). That the overall inte-grated intensity of the EPR spectrum increases with increasingtemperature also indicates that anti-ferromagnetic couplings,in particular, are dominant. At higher temperatures, states withlarger S-values are populated and the transition between spinlevels of these states have larger transitions probabilities givingrise to increased signal intensity.
Each of the complexes 3–7 is expected to have an evennumber of unpaired electrons and, in the case of maximalantiferromagnetic coupling, we would expect an ST ¼ 0 groundstate. Nonetheless, all of the complexes give rise to EPR signalsowing to thermal population of paramagnetic excited states thatare quite low in energy. In addition, exchange-coupled systemswith three or more spin centers can exhibit “spin-frustration” inwhich all pair-wise couplings that are antiferromagnetic (i.e.negative J-value) are not achievable. This leads to ground statetotal spin quantum numbers that are greater than zero.
In the example of complex 3, neglecting any contribution tothe eigenvalue from zero-eld splitting, using the J-values inTable 2 predicts that the ground state is S¼ 3withanS¼ 4 excitedstate approximately 0.2 cm�1 higher in energy at zero eld. Thesemanifolds are roughly equally populated at 5 K. The next excitedstate—predicted to be an S¼ 4manifold—is 13.3 cm�1 higher inenergyandshouldbeappreciablypopulatedat 15–20K.This statecould give rise to the temperature-dependent signals discussednext. The 5 K CWEPR spectrum of 3 contains weak signals at loweld. As the temperature is increased up to 25 K, a negativefeature becomes more prominent at g ¼ 15.2 that then starts todiminish at 40K. A corresponding feature appears in the parallel-
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mode spectrum (data not shown). These two properties conrmthe formulation of 3 as being an integer spin system with a largevalue for the ground state S.
The 5 K EPR spectrum of 4 is weak and broad with two clearresonances at g ¼ 7.4 and 2.9 that become slightly broader asthe temperature is raised until 50 K when they begin to disap-pear. The g¼ 7.4 feature also has a corresponding negative peakin the parallel-mode spectrum (data not shown). The relativelylarge value for Jmm pairs the spins of the two MnIII ions thus thelowest energy states of 4 consist of the 36 microstates of theexchange-coupled MnII ions.
A multiline feature containing 11 peaks centered at g ¼ 1.98and split by 9.5–12.9 mT is faintly visible at all temperaturesexplored. This signal is reminiscent of spectra for weaklycoupled MnIIIMnIV dimers in which the exchange coupling issmall compared to the zero-eld splitting of the MnIII ion. Theamount to which this signal contributed to the spectrum variedwith different preparations of 4 leading to the conclusion thatthe corresponding species is likely a degradation product.
The spectrum of 5 collected at 5 K reveals two peaks at g ¼7.57 and 4.95. The feature at g ¼ 4.95 disappears quickly whenthe temperature is raised from 5 K whereas the feature at g ¼7.57 exhibits Curie-type behavior (i.e. is proportional to 1/T). Anadditional feature appears at g ¼ 2.5 at temperatures above 25K. Overall, the spectrum of 5 is very reminiscent of that for amononuclear MnIV center (cf. for example, the spectrum of MnIV
3,5-di-tert-butylquinone67). However, we interpret the markedincrease in integrated spectral intensity with increasingtemperature as being diagnostic of these resonances arisingfrom an exchange-coupled system, not a mononuclear one.
Complex 6 yields a spectrum at 5 K that is somewhat remi-niscent of the multiline signal corresponding to the S ¼ 1/2form of the S2 state of the [Mn4CaO5] cluster in PSII. Namely,there is a broad feature (spanning 250 mT) centered at g ¼ 1.98;however the 55Mn hyperne contributions are unresolved in thecase of complex 6. As the temperature is increased from 5 K to20 K the g ¼ 1.98 feature grows slightly in intensity until 20 Kand it begins to decrease in intensity and split into two peaks.That this feature is similar to the multiline signal for photo-system II could suggest that some of 6 became oxidized by oneelectron to give a MnIIIMnIV
3 complex, the oxidation statescheme employed to rationalize the S2 EPR and X-ray absorp-tion results. Alternatively, the spectrum can be rationalized ascoming from a S¼ 1 or S¼ 2 state (these are the two lowest spinstates for 6 based on the exchange couplings in Table 2, seeESI†) with a relatively small zero-eld splitting (ZFS) parameter(D � 1000 and 600 MHz, respectively) and convolved by broad,unresolved 55Mn hyperne features. Such small ZFS is generallyunexpected for a MnIII-containing compound; however struc-tural considerations provide a rationale. XRD data for 6 show ahighly symmetric cube especially compared to complex 3, 4 or 5,and the pseudo-Jahn–Teller (JT) axes of the two MnIII ions areperpendicular to each other. This orthogonality effectivelycancels the contributions of the two MnIII site-specic ZFStensors to the molecular ZFS tensor.68
The lowest-temperature EPR spectrum of complex 7 is fairlysimilar to that for 6, though a bit broader indicating a slightlylarger ZFS for this lowest energy state. This behavior is notsurprising given themodest difference in ligand set between thetwo species. However, there is a much more dramatic
3992 | Chem. Sci., 2013, 4, 3986–3996
temperature dependence in which features at g ¼ 2.16 and g ¼1.81 grow in as the temperature is raised.
2.6 Cluster reactivity and interconversion
Thepresent series of clusters of varying oxidation state and oxidocontent provides a unique opportunity to investigate clusterreactivity conceptually related to the PSII photoactivation. PSIIbinds fourMncenters, photooxidizing theMnand incorporatingoxido/hydroxido ligands to stabilize the increasingMn oxidationstates up through MnIV
4. As shown in Scheme 1 by dashedarrows, oxidative water incorporation formally interconvertsmany of the complexes 2–6, and thus cluster interconversionwasexplored here to conceptually model these key steps of photo-activation and turnover. Complex 2 formally differs from 3byoneelectron and a ligand exchange from triuoromethanesulfonateto acetate. Complex 4 corresponds formally to water incorpora-tion and double deprotonation from 3. Complex 5 is the productof a formal oxygen-atom addition to 4 – a process comprised ofwater incorporation, a two-electron oxidation, and doubledeprotonation. Complex 6 represents a similar oxygen-atomaddition to 5.
The conversion of 3 to 2 involves a one-electron reduction,without change in the oxygen content of the cluster. Cyclicvoltammetry studies of 3 in CH2Cl2 with 0.1 M [nBu4N][PF6]showed two irreversible reductions at �0.2 V and �1.0 V versusthe Fc/Fc+ couple, suggesting the formation of MnII
3MnIII andMnII
4 species (Fc ¼ ferrocene) (Fig. S7†). Indeed, if one equiv-alent of bis(pentamethylcyclopentadienyl)iron(II) was added to3, a new species was formed that upon isolation, dissolution inCH3CN, and addition of excess [nBu4N][OAc] cleanly precipi-tated complex 2 (1H NMR; Fig. S2†).
Water incorporation/deprotonation was investigated for theconversion of 3 to 4. However, reaction of 3 with water in thepresence of amines or hydroxide as bases generated complicatedmixtures that did not contain4by 1HNMRspectroscopy. Cationic3 is soluble in water, generating a green solution rather thanpurple-brown as observed in organic solvents. Removal of waterin vacuo aer thirty minutes and dissolution in CH3CN regen-erated 3 (1H NMR) as a purple-brown solution. Water coordina-tion likely occurs at the ve-coordinate apical metal center ratherthan the six-coordinate, basal metal centers. The weakly coordi-nating OTf� anion might be displaced by the incoming Lewisbase; if water binds at this axial position, isomerization to theequatorial position and displacement of a k2-acetate must occurbefore bridging to the basal metal centers as in 4. The stericallyopen apical manganese could be prone to oligomerization byhydroxide or acetate bridges, precluding conversion to 4.
Oxygen-atom transfer in the context of cluster reorganizationwas studied for the conversion of 4 to 5. Complex 5 wassuccessfully generated from the reaction of 4with PhIO, albeit asa minor species in a mixture of products. Reaction of 4 withexcess PhIO leads to the generation of complex 6 in low yield.The conversion of 4 to 5 is remarkable given the extent of reor-ganization that the cluster has to undergo due to the change inthe bindingmode of the ligand L. The generation of amixture ofproducts is consistent with an incomplete reorganization
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leading to unidentied species. The observed conversion of 4 to6 corresponds to the addition of two oxygen atoms, analogous toincorporation and full reduction of one equivalent of dioxygen.Correspondingly, reaction of a dilute solution of 4 in DMF withone atmosphere of O2 leads to the generation of complex 6 overthirteen days (Fig. S5†). This one-step conversion is notablebecause it involves the reduction of O2 to two O2� moieties by atetramanganese site, which represents the microscopic reverseof the O–O bond forming reaction performed by the OEC. Thelow oxidation states of manganese in precursor 4 allow for thereaction to proceed in the O2-reduction direction.
Oxido–ligand incorporation into partial cubane 5 to form 6was reported previously,33 with detailed mechanistic studiesperformed. For both oxidative water incorporation and reduc-tive oxygen-atom transfer, m3-oxido migration within the Mn4
cluster was found to be a key mechanistic step, with implica-tions for the structure and turnover of the OEC.
2.7 Electrochemistry and potential leveling
The redox properties of 5, 6, and 7 were studied by cyclic vol-tammetry (Fig. 5). Although voltammograms of 5 and 6 havebeen reported,33 no comparative discussion was presented inthe context of potential leveling and are thus included herealongside complex 7. Complex 5 irreversibly reduces to aproposed MnIIMnIII
3 oxidation state ca. �1.0 V vs. ferrocene/ferrocenium (Fc/Fc+) in THF with a coupled return oxidationand oxidizes quasireversibly at +100 mV vs. Fc/Fc+ to theMnIII
3MnIV oxidation state. In contrast, 6 reduces to theMnIII
3MnIV state at �870 mV in THF. This oxidation state is ca.1 V more negative in 6 because of the presence of the fourthoxide versus the three oxides of 5. An oxidation of 6 was alsoobserved at +250 mV in THF, proposed to correspond to theMnIII
2MnIV2/MnIIIMnIV
3 couple. Complex 7, a cationic ratherthan neutral MnIII
2MnIV2 complex, quasireversibly oxidizes at
+340 mV in THF and irreversibly reduces at �510 mV. Theoxidation event varies little (ca. 90 mV) in potential from 6
Fig. 5 Redox properties of 5–7. Cyclic voltammograms of 5 (bottom), 6 (middle)and 7 (top) referenced to Fc/Fc+. The scan rate was 50 mV s�1 in the positivedirection. The analyte concentration was 1.0 mM. The electrolyte was 0.1 M[nBu4N][PF6] in THF. Open-circuit potential for 5 ¼ �460 mV, for 6 ¼ �200 mV,and for 7 ¼�50 mV. E1/2 values: 5
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despite the buildup of charge at the now dicationic complex.Although the product of chemical oxidation has not yet beenfully characterized, the electrochemical oxidation of 6 and 7indicates that the MnIIIMnIV
3 species is accessible. Only oneMnIIIMnIV
3O4 cubane has been previously reported.69,70
The reduction and oxidation events of 5 parallel those of 6,with the reductions only differing by ca. 130 mV and theoxidations by 150 mV (Fig. 5, Scheme 2). With only a slightincrease in potential, a MnIIIMnIV
3 oxidation state can beaccessed in 6 where only a MnIII
3MnIV oxidation state is acces-sible in 5. This can be explained by the neutralization of chargebuildup on the cluster by incorporation of an O2� donor(Scheme 2). The water incorporated into 5 to give 6 is deproto-nated twice, allowing access to oxidation states two units moreoxidized at close to the same potential. Neutralization of chargebuildup has been demonstrated for a dimanganese catalasemodel system with a terminal water/hydroxide.71 Notably, thatsystem was able to span four oxidation states – MnII
2 throughMnIIIMnIV – with little change in the chelating ligand frame-work as observed herein.72,73 This redox leveling of the clusterupon formal water incorporation and deprotonation is relevantto the OEC, as the oxidizing equivalents come at the samepotential for all four oxidations during catalysis to generate O2.
2.8 Ligand exibility as design element
The propensity of the present supporting multinucleatingligand to allow for different binding modes is instrumental forsupporting the wide span of metal oxidation states and oxidocontent. The lability of the dipyridylalkoxymethyl moiety is welldocumented in the coordination chemistry of dipyridylketoneand the gem-diol or hemiacetal form thereof, which chelate andbridge metal ions in a wide variety of binding modes.74 Bridgingthree dipyridylalkoxymethyl units through a triarylbenzenescaffold therefore provides rich possibilities for coordinationthat benet the formation of complexes 2 through 7. Clustersrich in labile MnII are coordinated by nine donors from L,binding to twelve coordination sites (counting three m-alkox-ides) while the higher oxidation state species, displaying MnIII
and MnIV, require only six donors (Fig. 6). The switch in coor-dination mode is likely due to the strong Mn–oxido bonds thatlead to the displacement of the pyridine and m2-alkoxide donors.The three acetates from precursor 1 complete the metal coor-dination spheres by bridging the Mn3(m-OR)3 core of 2–4 to thefourth manganese and the three diamond core motifs in 5–7.The versatility of carboxylate ligation in manganese clusterchemistry has also been documented.75 The presentcompounds show conservation of the ancillary ligands (L and
Scheme 2 Effect of oxidation state and oxido ligand content on leveling ofreduction potentials for 5 and 6.
Fig. 6 Ligand flexibility as function of cluster oxido content and oxidation state:binding modes of dipyridylalkoxide arms in clusters 1–7.
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acetates) over a large set of oxidation states and oxide contents,indicating that donor exibility is an important factor in thedesign of ligands for clusters in multielectron chemistryinvolving transfers of oxygenous moieties.
2.9 Relation to the assembly and turnover of the OEC;design implications for oxidized metal–oxide clusters
PSII stabilizes four manganese centers through nine oxidationstates. The present compounds comprise eight oxidation statesfromMnII
4 to MnIIIMnIV3, mimicking states from the beginning
of photoactivation, a hypothetical S�5, through to S2. As in PSII,the higher oxidation states are stabilized by incorporation ofstrong oxido ligands. Alongside three acetates, the semilabileligand framework L is conserved throughout the series with adecrease in the number of coordinating donors from L. The typeof change in coordination observed here might be relevant tothe assembly of the OEC in PSII. The early biochemical inter-mediates in photoactivation are reported to proceed to fullyassembled OEC in low yields relative to light absorption.20,76,77
Additional nitrogen and oxygen donors are present in theprotein close to the active site, such as His337 and Asp61. Thesedo not coordinate to the fully assembled cluster, but have beenproposed to be important in binding the metal centers in thelow oxidation state intermediates of photoactivation (<S0),16
although Asp170 has been shown to coordinate to the rst MnII
center during assembly and remains coordinated to the fullOEC.18,78 A slow kinetic step aer the initial binding andphotooxidation of MnII has been proposed to be a proteinconformational change, which may involve ligandrearrangements.20,77
The charge neutralization demonstrated by 5 and 6conceptually mimics how the OEC can access high oxidationstates. In PSII, the oxidizing equivalents, all with the samepotential, are provided by the photooxidized chlorophyll P680via a tyrosine Yz_.71,79–82 Therefore, as the OEC is oxidized duringturnover, water is incorporated and deprotonated, neutralizingthe positive charge built up from oxidation and facilitatingaccess to high oxidation state Mn. Complexes 5 and 6 show thatcharge neutralization manifests in high oxidation state, tetra-manganese–oxido synthetic models of the OEC.
Beyond the assembly of the OEC, the present series ofcompounds suggests a rational strategy for the synthesis of highoxidation state clusters from reduced precursors. Low oxidationstate clusters support fewer oxido ligands due to negative chargebuildup. Consequently, additional donors from the multi-nucleating ligands are necessary to satisfy the coordination
3994 | Chem. Sci., 2013, 4, 3986–3996
sphere of the metal and avoid oligomerization. Upon oxidation,water incorporation and deprotonation, the clusters includeadditional oxido moieties. These moieties facilitate furtheroxidation. Increased number of oxido moieties require somesupporting ligand dissociation tomaintain similar coordinationnumbers. Labile pendant donors, such as the pyridines in thepresent case, facilitate not only the isolation of the reducedclusters, but also provide coordination exibility to support thehigher oxidation state, higher oxido content clusters.
3 Conclusions
In summary, a series of tetramanganese complexes of variableoxido-content (one through four) and oxidation state (MnII
4
through MnIIIMnIV3) has been obtained. Six clusters in four
oxidation states were crystallographically characterized, andfour further redox events were accessed electrochemically.XANES data support the assigned oxidation states, and EXAFSwere consistent with XRD. Magnetism and EPR studies wereperformed to elucidate the electronic structures. Thesecomplexes conceptually mimic the wide range of tetramanga-nese–oxido species in photoactivation and the Kok cycle of theOEC in PSII. Cluster interconversion was achieved in severalcases. These transformations show that the coordination envi-ronment around the metal centers changes as a function of thenumber of oxido moieties due to their propensity to bridge andform strong bonds. Similar to the OEC active site, several linkeddonors in a multinucleating ancillary ligand support the four-manganese cluster over a broad range of oxidation states andoxido content. Ligand lability was found instrumental foraccommodating the increased number of oxido moieties. Thepresence of labile pendant donor groups is a design feature thatis expected to apply generally to the rational synthesis of metal–oxido clusters from reduced precursors.
Acknowledgements
We are grateful to California Institute of Technology, the SearleScholars Program, an NSF CAREER (CHE-1151918) award (TA),the Rose Hill Foundation, and the NSF GRFP (J.S.K.) for fund-ing. We thank L. M. Henling for assistance with crystallography.The Bruker KAPPA APEXII X-ray diffractometer was purchasedvia an NSF CRIF:MU award to Caltech (CHE-0639094). Weacknowledge the Gordon and Betty Moore Foundation, theBeckman Institute, and the Sano-Aventis BRP for theirsupport of the Molecular Observatory at Caltech. The workcarried out by RDB was funded by the Division of ChemicalSciences, Geosciences, and Biosciences, Office of Basic EnergySciences of the U.S. Department of Energy (DE-FG02-11ER16282). SSRL is operated by Stanford University for theDOE and supported by its Office of Biological and Environ-mental Research, and by the NIH, NIGMS (includingP41GM103393) and the NCRR (P41RR001209). X-ray spectros-copy studies were supported by the NIH (F32GM100595 to R.T.)and by the Director of the Office of Basic Energy Science, Divi-sion of Chemical Sciences, Geosciences, and Biosciences, DOE(DE-AC02-05CH11231 to J.Y.).
This journal is ª The Royal Society of Chemistry 2013
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