Formation of CoIV=O intermediate at the Boundary of the “Oxo-wall” Induces Water Oxidation

Development of economically viable articial photosynthesis requires use of 3d metal-based catalysts. Water oxidation by [Co 4 O 4 ] n+ cubane mimics water splitting by CaMn 4 O 5 cluster in Nature but the exact mechanism of O-O bond formation is presently unknown. We demonstrate rst in situ detection Co IV =O (~ 1.67 Å) moiety formed upon activation of [Co 4 O 4 Py 4 Ac 4 ] 0 (Py = pyridine and Ac = CH 3 COO − ) towards O-O bond formation. Combined spectroscopic and DFT analyses show that the intermediate active in O-O bond formation has two Co IV centers and at least one Co IV =O unit of strong radicaloid character that participates in O-O bond formation via water nucleophilic attack. The multimetallic structure of the cubane provides unique stabilization for Co IV =O + H 2 O = Co-OOH + H + transition with the carboxyl accepting the proton and the bridging oxygen stabilizing the peroxide via hydrogen bonding. Results are important for development of oxygen evolution catalysts based on Earth-abundant 3d elements.


Introduction
Water splitting reaction is a keystone in application of solar energy for electrochemical water splitting to obtain hydrogen gas, a sustainable carbon-neutral energy source on an economic-wide scale. 1 The ultimate goal in water oxidation catalysts design is to develop a material comparable with natural photosynthetic cluster CaMn 4 O 5 in water-splitting e ciency. Currently, the most productive electrocatalysts for this process utilize noble metals due to their high stability, small overpotential, and low Tafel value. 2,3 However, the application of precious metal-based catalysts on an industrial scale is cost prohibitive. To make this process more economically viable, oxygen evolution and reduction catalysts have been developed using cobalt and other Earth-abundant metals. 4,5,6,7,8,9 Water oxidation reaction (WOR) electrocatalysts based on transition metal oxides were extensively studied. 10,11,12 Cocubanes bearing [Co 4 O 4 ] n+ oxo-metalate cluster draw considerable attention, as they carry the minimal Co 4 O 4 unit potentially present in the solid oxides but are tangible to the detailed mechanistic studies as the molecular systems. 13,14,15,16,17,18,19 This motif is also similar to the CaMn 4 O 5 oxygen evolving complex (OEC) of Photosystem II (PS II), responsible for water oxidation in natural photosynthesis 7,13,16,20 . Elucidating the mechanism of the O-O bond formation in such catalysts is crucial to the development of economically viable arti cial photosynthesis.
Several mechanisms of WOR have been proposed for Co-based complexes, including [Co 4 O 4 Py 4 Ac 4 ] 0 (1) (Fig. 1a). 13,14,15,16,17,21,22,23 (1) + or "cubium", is water-soluble in basic conditions and can oxidize water at pH=10 and above with O 2 and H + release. It was found that the crucial process necessary for (1) + -promoted WOR catalytic cycle at basic pH is coordination of hydroxyl ion (OH -) to a Co center. 14 Catalytic mechanisms of (1) have been studied using UV-Vis, EPR, mass-spectrometry, X-ray spectroscopy, DFT calculations, and O 2 evolution measurements at different pH and with the use of isotopically-labelled reagents. 14, 22, 24 Different conformations of the mixed Co IV /Co III cubane intermediates and the O-O forming units have been discussed previously (Fig. 1b, c) but there remains no consensus on the mechanism. 14, 21, 23 Possible formation of a side-on peroxo-unit on Co III metal center (geminal 1,1-intermediate) was concluded following lack of activity of its bpy (2.2'-bipyridine) analogue, where such a conformation is impossible (Fig. 1b). The mechanism suggests that after OH --promoted hydrolysis of Co-OAc site, formation of the Co(OH) 2 intermediates occurs. Then, these 1,1-(hem)-dihydro species undergo oxidation by (1) + , followed by O 2 release. Several assumptions about the architecture of [Co 4 O 4 ] n+ cluster bearing highly-oxidized Co=O species during WOR have been made (Fig. 1c) but such species so far escaped detection due to their high reactivity. 17,21,23 These mechanisms also implied participation of the neighboring Co-Co di-m-oxo moieties in high oxidation states (presumably Co IV =O) during formation of peroxo-species and O 2 release (Fig. 1c). Generally, formation of the high-valent metal oxo species is considered a key factor in catalyst activation for oxidation reactions, including WOR but detecting such species remains highly challanging. 15,25,26,27,28 The peroxo-intermediates of Co and other transition metal oxides participating in WOR were detected using mostly different IR spectroscopic techniques. 29 Besides the Co IV /Co IV formation 21 the possibilities of Co III /Co V and cofacial hydroxo-oxospecies Co III (OH)/Co IV have been considered. 21,23 A similar conformational motif of the edge sites was proposed for the electrocatalytic intermediates of the Co oxides and Co-Pi catalytic lms. 30,31,32 Although formation of Co IV =O species as a key intermediate was hypothesized in majority of mechanistic schemes (Fig. 1c) these oxo species have never been observed. Here, we present in situ X-ray absorption spectroscopy (XAS and EXAFS) detection of the Co IV =O fragment, supported by EPR and DFT analysis to uncover structure of the reactive intermediates in WOR catalyzed by (1). Co=O species are extremely elusive, highlighting the concept of the "Oxo wall" -an empirical observation of scarcity of M=O (M is a transition metal) complexes beyond Group 8 of the periodic table. These species formation has been reported only in exceptional cases, mostly in pyrolytic transformations of Co-based complexes, and none during the WOR. 21,25,26,27 Our direct observation con rms the generation of the Co IV  Results And Discussion 1. In situ X-ray absorption spectroscopy. In this study we determined the presence of Co IV =O intermediate state using in situ XANES and EXAFS of electrochemical WOR of (1) at 1.4 V vs. Ag/AgCl potential in a basic water solution (pH = 12) for prolonged time (8 hours) (Fig. 2a, b, Table S1). XAS measurements were performed for initial (1), in situ bulk electrolysis (BE) of (1) at pH=12, and (1) oxidized with cerium (IV) ammonium nitrate (Ce IV ) at pH = 1 (measured at 20K) (Fig. 2a, b). Due to high activity of this catalyst, pH of the electrochemical solution of (1) during the bulk electrolysis shifted towards increasing acidity; pH monitoring and basi cation occurred prior to each X-ray scan, as necessary. Formation of Co species in high oxidation states is re ected in the shift to the higher energy and shape change of the Co K-edge ( Fig. 2a). At pH = 1, XAS of the (1) oxidized with 20 equiv of Ce IV also revealed K-edge shift to the higher energy (Fig. S1).
Compound (1) contains four Co III ions, while (1) + has a single Co IV . According to DFT calculations, further oxidation of (1) + to the [Co III 2 Co IV 2 O 4 ] 2+ is possible (Tables S2, S3) in non-protic solvents. Co K-edge XANES measured during BE of (1) in water at pH = 12 ( Fig. 2a) also re ects a formation of the [Co III 2 Co IV 2 ] intermediate as reported earlier for electrolysis in CH 3 CN ( ~1 eV K-edge shift compared to solution before the BE). 21 In addition, the top of the edge shape becomes pointier (Fig. 2a). This change indicates a potential geometric change in the cluster and change in the form of the cluster frontier's orbitals. EPR analysis of the samples quickly frozen from the in situ cell during prolonged BE under applied potential indicates mostly EPR silent species, agreeing with [Co III 2 Co IV 2 ] oxidation state assignment (Fig. 3a, b).
EXAFS analysis indicates considerable changes in the structure of (1) at pH=12 and the applied potential ( Fig. 2b). EXAFS ts of the initial (1) and (1) + formed by Ce IV oxidation agree with known structures of these species (Table S4, Fig. S2). In situ experiment at pH=12 was conducted at two different beamtimes, ensuring EXAFS reproducibility (Table S1). First coordination sphere of Co is comprised of oxygens as m 3 -oxo bridges, expected Co-O a ~1.85 Å, and single nitrogen ligand from pyridine with Co-N at ~1.90 Å. However, to achieve satisfactory EXAFS ts of the in situ data, addition of short ~1.65-1.70 Å Co-O vector is required (Table S1) ) mono ] 0 model also predicts two groups of Co-Co distances: one shorter (~2.73 Å) and one longer (~2.86-2.91 Å). EXAFS ts improve if Co-Co vector is split into two shells (Table  S1).
2. In situ EPR. Oxidation of (1) by one electron results in well-known paramagnetic (S=1/2) cubium signal (1) + . 14 This signal can be produced by oxidation with Ce IV at acidic pH or by bulk electrolysis at neutral pH~7 where the catalyst is inactive (Fig. S6). EPR samples from bulk electrolysis in pH=12 solution at 1.4 V vs. Ag/AgCl electrode were quickly frozen and analyzed by X-band EPR at 20K (Fig. 3a, b). Such samples are largely EPR silent, except for the background due to frozen oxygen evolved under these BE conditions. Loss of EPR signal is consistent with further sample oxidation to (1) 2+ state, which can have [Co III 2 O 4 Co IV =O/Co IV (CH 3 CO 2 ) mono ] 0 form, as discussed below based on XAS analysis and DFT. Traces of cubium (1) + signal are detected upon sample melting (data not shown). New, short-lived S=1/2 signal is detected when spectra are closely analyzed (Fig. 3, b). The signal peaks at g ~2.08 and has g zz component centered around g~1.80. Hyper ne splitting ~50-60 G is noticeable around g zz component and to the left of the g ~2.08 peak. It is assigned to the 59 Co I=7/2 hfs. The g-tensor values near g~2 indicate a signi cant electron localization on the ligand. Low g-tensor values were previously reported for Co III -O 2 superoxo com-  (Figure 1b, c). 13,14,15,16,17,21,22,24 4 Ac 2 ] 2+ is not an active catalyst called for a speci c mechanism with side-on peroxide formation from Co(OH) 2 corner (Figure 1b). 14 The redox potential for (1) to form Co III 2 Co IV 2 in acetonitrile solvent 21 is in Table S2. Cyclic voltammogram data for (1) in acetonitrile has con rmed the earlier result 21 ( Figure S3), while in the same electrochemical window the bpy analog reversibly oxidizes at ~+0.71 V. 6,36 However, no second redox couple was observed. Hence, oxidation of the bpy derivative requires greater energy input, likely due to its positive charge. DFT calculations con rm this effect (Table S3). Note that protic solvents are known to form hydrogen bonds to the cubane μ 3 -oxos, reducing donation to cobalt and raising the potentials in aqueous solution. 17 This effect causes (1) and the bpy analog to reach the Co III 3 Co IV level at identical potential in water. Nonetheless, the Co III 2 Co IV 2 level was observed for (1) and remain undetected for the bpy analog, potentially explaining lack of its catalytic activity.
The [Co III 2 Co IV 2 ] 2+ cubane can be in a triplet (S=1) or a singlet state (S=0). Both these states are energetically equal. 21 Figure  1d). For this structure, the triplet state is ~0.7 eV lower than the singlet (Table S5) (Table S1). Co-Co distances that are separated into two groups, the shorter (~2.73 Å) and the longer (~2.85 Å), also match the DFT model (Table S1).
Recent time-resolved rapid-scan IR observation of photo-oxidized cubane at pH=12.3 indicates no free acetate at reaction conditions, suggesting that all acetates remain at least as the terminal ligands to the cubane. 29 However, this observation contradicts the paper's following interpretations: assigning ~833 cm -1 band to Co-OO-Co peroxo species. Thus, we explored [Co III 2 O 4 Co IV =O/Co IV (CH 3 CO 2 ) mono ] 0 reaction with water via WNA mechanism which has negative (-0.27 eV) DG in the calculations done with 15% of Hartree Fock exchange (Table 1, Fig. 1d). Multiple Table 2. DFT computed key spectroscopic characteristics of the reactive intermediates in BE of (1) in water solution at pH = 12 at 1.4V vs Ag/AgCl applied potential.  (Table 1). Energetically, this pathway is similar in energy to WNA but was not further investigated pending an experimental evidence.
DFT-computed spectroscopic properties of proposed intermediates are summarized in Table 2 Fig. 1d). Similar radicaloid character of the Ru V =O fragment oxygen was established via direct spin density mapping by EPR for water oxidation intermediate in the "blue dimer" catalyst. 48 In the PS II, the O-O bond was proposed to form via radical coupling between the oxygens in Mn IV =O and bridging Mn-O-Mn. 37,49 Mechanism observed for the [Co III 2 O 4 Co IV =O/Co IV (CH 3 CO 2 ) mono ] 0 with involvement of the carboxylate and bridging oxygen as proton acceptors in the O-O bond formation (Fig. 1d), prompted analysis of similar con gurations for the OEC (Fig. 4). The S 3 state model allows WNA of the Ca 2+ -bound H 2 O on the Mn IV =O. The closest carboxylate ligand able to accept a proton is E189, while two oxo bridges, the left (~+0.2 eV) and the right one (~+1.5 eV), of the Mn IV =O fragment may form hydrogen bonds with the peroxides formed (Fig. 4b). Such peroxides are energetically plausible for formation, even at S 3 state.
Note that formation of a peroxide via radical coupling will better agree with the TR-XRD data of the S 3 state, as this does not require additional oxygen atoms except already detected in TR-XRD. 45,46,47 To account for peroxides formed via WNA on the Mn IV =O, additional oxygen density should be present in the S 3 state (Fig. 4a). Thus, such a peroxide can only be possible as a minor con guration. One electron oxidation of the OEC forming the S 4 state results in similar energetics with (~+1.8 eV) for the left and (~+0.2 eV) for the right (Fig. 4b, Table S9). Future detection of electron densities in the S 4 state (formed 200-1000 msec in the S 3 to S 0 transition) will help to discriminate between radical coupling and WNA mechanisms.

Methods
Complex (1) was prepared as previously described. 14 UV-vis spectra were recorded on Varian Cary 300-Bio spectrophotometer. Aqueous solutions were prepared using ultrapure (Type 1) water (resistivity 18.2 MΩ·cm at 25 0 C) from Q-POD unit of Milli-Q integral water puri cation system (Millipore, Billerica, MA, USA). XAS measurements were made for bulk electrolysis of (1) in water in situ in a basic media at beamline 9 of Argonne National Laboratory using a potentiostat (CHI 627C; CH Instruments Inc., Austin, TX, USA) and a custom made single-compartment 3-electrode cell with exible grafoil tape as a working electrode and 4µm polypropylene tape window for XAS. The electrolysis of (1) was performed in 0.1 M sodium sulfate water solution basi ed with appropriate amount of sodium hydroxide to pH = 12. The cell was equipped with grafoil as the working electrode, Pt wire as the counter electrode in an auxiliary chamber and Ag/AgCl as the reference electrode at 1.4 V vs. Ag/AgCl applied potential and 0.4 µM mylar tape window on the X-ray path. A basicity of the solutions in the cell and auxiliary chamber were measured after each scan and adjusted to pH = 12 if necessary. Electrochemical measurements which did not take place at the beamline were performed on a Biologic VSP potentiostat with a typical three electrode cell: Glassy carbon working electrode, Pt wire counter electrode, and Ag/AgCl reference. The medium was 0.1 M tetrabutylammonium hexa uorophosphate in acetonitrile, and measurements were performed under an N 2 atmosphere. The data are referenced to the experimentally determined ferrocene redox couple.
X-band EPR measurements were conducted at 20 K temperature with Bruker EMX X-band spectrometer and CW microwave radiation using ColdEdge-closed cycle cryostat. The EPR samples were prepared by mixing 200 ul of 1 mM of (1) in 0.1 M HNO 3 with appropriate amount of Ce IV in an EPR tube, followed by freezing in liquid N 2 in less than 30 seconds.
All reported measurements were repeated several times to ensure the reproducibility of results.

Conclusions
Observation of Co IV =O intermediate and its comparison with CaMn 4 O 5 cluster of PSII during WOR strengthens understanding of the water oxidation mechanisms for both systems. The "oxo-wall" effect may be mitigated in the multi-metal clusters like [Co 4 O 4 Ac 4 Py 4 ] 0 . X-ray spectroscopy data and DFT calculations indicate an importance of water nucleophilic attack in electrochemical water oxidation promoted by Co 4 O 4 -cubane. This pathway is similar to WOR catalyzed by group 8 transition metals, forming intermediates in high oxidation states. 28,50 Formation of Co V has not been supported experimentally or with DFT. Thus, O-O bond formation likely proceeds through the