Tetranuclear Manganese Models of the OEC Displaying Hydrogen Bonding Interactions: Application to Electrocatalytic Water Oxidation to Hydrogen Peroxide

Article abstract of DOI:10.1021/jacs.7b03044

Toward the development of structural and functional models of the oxygen evolving complex (OEC) of photosystem II, we report the synthesis of site-differentiated tetranuclear manganese complexes featuring three six-coordinate and one five-coordinate Mn centers. To incorporate biologically relevant second coordination sphere interactions, substituents capable of hydrogen bonding are included as pyrazolates with arylamine substituents. Complexes with terminal anionic ligands, OH^- or Cl^-, bound to the lower coordinate metal center are supported through the hydrogen-bonding network in a fashion reminiscent of the enzymatic active site. The hydroxide complex was found to be a competent electrocatalyst for O-O bond formation, a key transformation pertinent to the OEC. In an acetonitrile-water mixture, at neutral pH, electrochemical water oxidation to hydrogen peroxide was observed, albeit with low (15%) Faradaic yield, likely due to competing reactions with organics. In agreement, 9,10-dihydroanthracene is electrochemically oxidized in the presence of this cluster both via H-atom abstraction and oxygenation with ～50% combined Faradaic yield.

Full text of DOI:10.1021/jacs.7b03044

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Communication
Tetranuclear Manganese Models of the OEC Displaying
Hydrogen Bonding Interactions: Application to
Electrocatalytic Water Oxidation to Hydrogen Peroxide
Zhiji Han, Kyle T. Horak, Heui Beom Lee, and Theodor Agapie
J. Am. Chem. Soc., Just Accepted Manuscript • Publication Date (Web): 06 Jun 2017
Downloaded from http://pubs.acs.org on June 7, 2017
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Tetranuclear Manganese Models of the OEC Displaying Hy-
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Zhiji Han, Kyle T. Horak, Heui Beom Lee and Theodor Agapie*
Division of Chemistry and Chemical Engineering, California Institute of Technology, Pasadena, California 91125, United States
Supporting Information Placeholder
ABSTRACT: Toward the development of structural and function-
al models of the oxygen evolving complex (OEC) of photosystem II
(
PSII), we report the synthesis of site-differentiated tetranuclear
manganese complexes featuring three six-coordinate and one five-
coordinate Mn centers. To incorporate biologically relevant second
coordination sphere interactions, substituents capable of hydrogen
bonding are included as pyrazolates with phenylamino groups. Com-
−
−
plexes with terminal anionic ligands, OH or Cl , bound to the lower
coordinate metal center are supported through the hydrogen-bonding
network in a fashion reminiscent to the enzymatic active site. The
hydroxide complex was found to to be a competent electrocatalyst for
O-O bond formation, a key transformation pertinent to the OEC. In
an acetonitrile-water mixture, at neutral pH, electrochemical water
oxidation to hydrogen peroxide was observed, albeit with low (15%)
Faradaic yield, likely due to competing reactions with organics. In
agreement, 9,10-dihydroanthracene is electrochemically oxidized in
the presence of this cluster both via H-atom abstraction and oxygena-
tion at ~50% combined Faradaic yield.
Figure 1. A) Drawing of the OEC (PDB 4UB8) highlighting a tetra-
nuclear cluster including the dangling Mn (orange) and H-bonding
network (blue)3 ; B) Target synthetic model.
b,d
protons in the chemistry of transition metals with oxygen, a variety of
elegant strategies have been reported for supporting transition metal
oxo and hydroxo chemistry with hydrogen bonding networks in mon-
10
onuclear complexes. Such strategies are significantly limited in the
context of multinuclear complexes. Moreover, terminal oxo or hydroxo
1
1
ligands are rare in multinuclear models of the OEC. Herein, we report
a synthetic strategy to access a Mn cluster model of the OEC that has a
4
dangling Mn motif, a terminal OH ligand, and second coordination
sphere H-bonding to stabilize it (Figure 1B). This species demon-
strates O-O bond formation under electrochemical conditions.
Water oxidation as source of reducing equivalents for artificial pho-
tosynthesis is an appealing approach to solar energy conversion and
Tetranuclear Mn
starting from trinuclear precursor LMn
tion of Ca(OTf)
4
complexes were prepared in a one pot procedure
1
storage. The oxygen evolving complex (OEC) of photosystem II
3
(OAc)
3
1 (Scheme 1). Addi-
2
(
PSII) is the biological catalyst for water oxidation to O
features a multinuclear active site, CaMn
CaMn moiety connected to a “dangling” Mn center; this cluster
2
. The OEC
12
2
(1.6 equiv) and [RNHPz]Na (3.5 equiv) to 1,
4
O , consisting of a cubane
5
followed by iodosobenzene (PhIO) (1.0 equiv) and Mn(II) salt (1-2
equiv) results in the desired tetramanganese complexes. Ca(OTf)
3
O
4
2
coordinates water ligands that are engaged in hydrogen bonding net-
facilitates the substitution of acetate ligands with pyrazolates. PhIO
acts as the O-atom source for the incorporation of the interstitial oxide
moiety. The additional equivalent of Mn(II) is the source of apical
2a, 3
works (Figure 1A).
Significant efforts have been focused on eluci-
2a, 4
dating the mechanism of water oxidation by the OEC in PSII. Given
the complexity of PSII and the challenge to perform structure-function
studies with the biological system, discrete cluster models have been
13
metal in the final cluster. Using [PhNHPz]Na as the bidentate ligand
and
LMn
MnCl
(PhNHPz)
2
as
Mn(II)
precursor
gave
5
targeted to provide insight into the function of the OEC. Synthetic
[
3
3
OMnCl][OTf] (2) in ~55% isolated yield. ESI-MS
cluster models that display both Ca and Mn centers and a cubane moi-
and single crystal X-ray diffraction (XRD, vide infra) characterization is
consistent with this assignment. A similar synthetic strategy was ap-
plied to target a lower coordinate or triflate complex by using
6
ety have been prepared, though they do not display catalytic activity.
2
b,
Multinuclear Mn complexes capable of O-O bond formation are rare.
2
d, 7
More generally, several discrete clusters of first row transition met-
als with structures reminiscent of the OEC have been reported to sup-
port O evolution, although in situ formed heterogeneous metal oxides
can be responsible for catalysis.
Mn(OTf) as the fourth equivalent source. ESI-MS characterization of
2
this product suggests the formation of a hydroxide complex. X-ray
diffraction quality crystals of this compound have not been obtained to
date using the [PhNHPz]Na as the bridging ligand. However, using [4-
2
2
b, 7g-i, 8
In some cases, the substrate oxy-
2a,2b
gen has been proposed to be a terminal metal-oxo species.
Depro-
tBuC
sponding
tBuC NHPz)
XRD studies.
6
H
4
NHPz]Na resulted in a complex with ESI-MS data corre-
to hydroxide species ([LMn (4-
OMn(OH)][OTf], 3) that gave crystals suitable for
tonations are an integral part of the conversion of water to such moiety.
Furthermore, challenging redox steps can be facilitated by coupling of
a
3
6
H
4
3
9
electron and proton transfers. Toward gaining insight into the roles of
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Scheme 1. Synthesis of tetranuclear manganese complexes and crystal structures of 2 and 3. Thermal ellipsoids are shown at the 50% probabil-
ity level. Parts of the ligands, hydrogen atoms, triflate, and co-crystallized solvent molecules are not shown for clarity.
Solid-state structures of 2 and 3 were determined by XRD (Scheme
). In both structures, the three basal Mn centers are in a distorted
differs, the structural parameters are similar between the OEC and 3;
the three non-hydrogen atoms closest to one of the OEC terminal
oxygenic ligand are in the range of 2.67-3.04 Å (Figure 1), which
1
3
d
octahedral coordination environment with two bridging alkoxides, one
pyrazolate, two pyridine, and a µ -oxo ligands each. The apical Mn
displays a trigonal bipyramidal geometry and is connected to the three
basal Mn centers through the interstitial µ -oxo ion. The Cl(1)-N(1)
distance (3.056(7) Å) in 2 is slightly shorter than the range (3.238-
.326 Å) observed in a previously reported five coordinate mononu-
4
includes the range observed in 3 for the O(2)-N distances.
The electrochemical properties of 3 were investigated by cyclic volt-
ammetry (Figure 2). Two reversible one-electron redox events are
observed at -0.72 and -0.21 and a quasireversible redox couple at 0.35
4
+
3
V vs Fc/Fc . In the context of water oxidation by the OEC, the electro-
clear Mn-Cl complex with intramolecular hydrogen bonding networks
indicating that all NH bonds engage in dative hydrogen bonding inter-
actions with the chloride.14
The Mn-µ
4
-oxo distances in 3 are consistent with the presence of
two Mn(II) (Mn(3) and Mn(4)) and two Mn(III) (Mn(1) and
1
3
Mn(2)). These oxidation state assignments, charge balance, and
localization of OH and NH hydrogens in the electron density map
support the assignment of the apical ligand as a hydroxide. Compound
3 displays two short O-N distances between the hydroxide oxygen and
the aniline nitrogens (2.774(5) and 2.805(7) Å, for N(1) and N(2),
respectively). These distances correspond to strong hydrogen bonding
interactions, in the range previously reported (2.721-2.848 Å) for
mononuclear Mn(III)-oxo species.1 The geometry at nitrogen is
consistent with the two anilines acting as hydrogen bond donors to the
hydroxide lone pairs. The third O-N distance is longer (2.939(5) Å, to
N(3)), and the orientation is consistent with the aniline serving as the
hydrogen bond acceptor. The N(3)H bond acts as a hydrogen bond
donor to a triflate ion. The differences in the hydrogen bonding inter-
actions in 2 vs 3 highlight the versatility of the aniline moiety in ac-
commodating both donor and acceptor functions. The Mn(1)-O(2)
distance (1.874(3) Å) is comparable to a mononuclear complex dis-
playing an intramolecular hydrogen bonding network, at 1.872(2) Å,
suggesting that the coordination environment for the Mn(1)-OH moi-
ety is similar to monomanganese species despite being part of a clus-
0a
Figure 2. Cyclic voltammograms of 1.0 mM of [LMn
tBuC NHPz) OMn(OH)][OTf] (3) in MeCN without water
(gray dash) and in the presence of water with increasing concentration
(other colors). Conditions: 0.1 M [n-Bu N][ClO ], GC working elec-
trode, 0.07 cm , Pt wire counter electrode, scan rate: 100 mV/s.
3
(4-
6
H
4
3
1
0a
ter. All structural parameters are consistent with a cluster supporting
a Mn(III)-coordinate terminal hydroxide that is engaged in several
hydrogen bonds. Although the geometry of the donors and acceptors
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chemical behavior of 3 in the presence of water is of interest. Inde-
pendently, compound 3 was found to be soluble and stable in
reaction conditions for the synthesis of 3 in small concentrations could
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be the active catalysts, several preparations were tested leaving some of
the reagents out (Figures S18-19). In all cases tested, smaller catalytic
current was observed compared to 3 at the same concentration. Thus,
the control experiments are consistent with 3 as the active molecular
MeCN/H
2
O mixtures containing up to 10 % volume water as observed
1
by H NMR spectroscopy (Figure S13). The CV of 3 was recorded in
the presence of various concentrations of water (Figure 2). Increased
concentration of water correlates with increased current close to the
second oxidation event, which is assigned to a catalytic process.
catalyst for water oxidation to H
2
2
O .
In summary, we report the synthesis of tetranuclear manganese
complexes displaying hydrogen bonding networks as more accurate
structural models of the biological water oxidation catalyst that include
second coordination sphere interactions. In particular, a cluster dis-
playing a terminal hydroxide ligand is reminiscent of structural motifs
involving the dangler Mn center of the OEC. Hydrogen bond donors
and acceptors stabilize the terminal hydroxide ligand. This species
The catalytic wave observed upon addition of water suggests that
compound 3 acts as water oxidation catalyst. In order to quantify the
reaction products upon electrochemical oxidation, we performed con-
+
trolled potential electrolysis (CPE) experiments at 0.57 V (vs Fc/Fc ).
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Complex 3 was dissolved in a mixture of MeCN/H
2
O (19:1 v/v) with
0
.1 M [n-Bu N][ClO ] as supporting electrolyte. The experiments
4
4
were performed in a two-compartment cell separated by an anion-
exchange membrane. In a typical experiment, with a total amount of
supports electrocatalytic water oxidation to H
2
2
O , albeit in low yield, in
a rare demonstration of function (O-O bond formation) with a struc-
tural model of the OEC. Related to the mechanism of the biological
system, the present results suggest that a terminal Mn-hydroxide moie-
ty can serve as precursor to O-O bond formation chemistry. Important-
ly, control experiments are inconsistent with the generation of a heter-
ogeneous active species, and support complex 3 as a discrete and well-
defined electrocatalyst for water oxidation. Complex 3 is also able to
perform both H-atom abstraction and oxygenation reactions with 9,10-
dihydroanthracene under electrocatalytic conditions. Current studies
are focused on the mechanistic aspects of these transformations.
5
.8 C passed charge over the course of 1.5 h (Figure S9), H
2
O was
2
detected with a Faradaic efficiency of ~15% using a chemilumines-
cence method with 10-acetyl-3,7-dihydroxyphenoxazine in combina-
tion of horseradish peroxidase (Figure S1). Addition of catalase to the
reaction mixture after electrolysis produced O as detected by gas
chromatography, which is also consistent with the generation of H
1
5
2
2
O
2
by 3 (Figure S2). The exact overpotential of the system remains unde-
termined due to the use of a mixture of solvents. The potential for
water oxidation to O
for example.
2
drifts ~ 200 mV more positive in acetonitrile,16
ASSOCIATED CONTENT
Supporting Information
The low observed Faradaic yield for H
2
2
O formation could be due to
side reactions between the highly reactive species generated upon oxi-
dation, such as Mn-oxo or Mn-(hydro)peroxo species, with organic
moieties. To test this hypothesis, CPE was conducted in the presence
of 9,10-dihydroanthracene (0.1 M) as a source of weak C-H bond to
This material is available free of charge via the Internet at
http://pubs.acs.org. Crystallographic data (CIF). General considera-
tions, physical methods, and synthetic procedure. Figures S1-S18,
Table S1 (PDF)
react with the intermediates. H
2
2
O was not detected in this experiment
and the combined Faradaic efficiency corresponding to 9,10-
dihydroanthracene oxidation to anthracene and anthraquinone was
AUTHOR INFORMATION
Corresponding Author
5
1% (Figure S10). CV control experiments show that there is no oxi-
dative wave for 9,10-dihydroanthracene in the absence of 3 at the ap-
plied potential of CPE experiments (Figure S11). Stirring 9,10-
dihydroanthracene in the presence of 3 without applied potential also
results in no oxidized products. These observations are consistent with
the generation of reactive intermediates that perform H-atom abstrac-
tion and oxygenation reactions of C-H bonds competitive with water
*
agapie@caltech.edu
Notes
The authors declare no competing financial interests.
oxidation. The lack of H
2
2
O formation and the significant increase of
ACKNOWLEDGMENT
the Faradaic yield in the presence of 9,10-dihydroanthracene indicate a
faster reaction between the intermediates and the weak C-H bonds of
This research was supported by the NIH (R01-GM102687A). We
thank L. M. Henling for assistance with crystallography, J.C. Tran for
this substrate than both H
organic solvent.
2
2
O formation and side reactions with the
assistance with the characterization of the 4-tBuC
6
4
H NHPzH, and B.
M. Hunter for helpful discussion on H
2
2
O detection.
To evaluate the stability of 3 during catalysis in more detail, electro-
chemical experiments reveal that the voltammogram traces remain
unchanged for 200 continuous cycles over the course of 3 h (Figure
S12). After these scans, rinsing the electrode gently without polishing
gave no catalytic wave and no redox features in a fresh electrolyte solu-
tion (Figure S12). Similar rinsing experiments were performed after
CPE and showed no consumption of charge (Figure S9). These obser-
vations suggest that there is no deposition of catalytically active metal
species on the electrode. Furthermore, to test the possibility of for-
REFERENCES
1. (a) Lewis, N. S.; Nocera, D. G., Proc. Natl. Acad. Sci. U.S.A. 2006,
103, 15729-15735; (b) Gray, H. B., Nat. Chem. 2009, 1, 7-7.
2. (a) Yano, J.; Yachandra, V., Chem. Rev. 2014, 114, 4175-4205; (b)
Blakemore, J. D.; Crabtree, R. H.; Brudvig, G. W., Chem. Rev. 2015,
115, 12974-13005; (c) Vinyard, D. J.; Ananyev, G. M.; Dismukes, G.
C., Annu. Rev. Biochem. 2013, 82, 577-606; (d) Kärkäs, M. D.;
Åkermark, B., Dalton Trans. 2016, 45, 14421-14461.
3. (a) Ferreira, K. N.; Iverson, T. M.; Maghlaoui, K.; Barber, J.; Iwata,
S., Science 2004, 303, 1831-1838; (b) Umena, Y.; Kawakami, K.;
Shen, J. R.; Kamiya, N., Nature 2011, 473, 55-65; (c) Suga, M.; Akita,
F.; Hirata, K.; Ueno, G.; Murakami, H.; Nakajima, Y.; Shimizu, T.;
Yamashita, K.; Yamamoto, M.; Ago, H.; Shen, J. R., Nature 2015, 517,
99-103; (d) Young, I. D.; Ibrahim, M.; Chatterjee, R.; Gul, S.; Fuller, F.
mation of heterogeneous MnO catalysts via free Mn ions, chelating
x
ligands were added to solutions of 3 during CV measurements. No
decrease of catalytic current was observed (Figures S14-16).17 Addi-
tionally, dynamic light scattering measurements do not detect any
nanoparticles (Figure S20). These observations are consistent with the
absence of MnO
x
formation from 3 in our electrochemical experi-
ments. To evaluate whether other clusters that may form under the
3
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Journal of the American Chemical Society
Page 4 of 5
D.; Koroidov, S.; Brewster, A. S.; Tran, R.; Alonso-Mori, R.; Kroll, T.;
al., e., Nature 2016, 540, 453-457.
4. Cox, N.; Retegan, M.; Neese, F.; Pantazis, D. A.; Boussac, A.; Lubitz,
W., Science 2014, 345, 804-808.
9. Weinberg, D. R.; Gagliardi, C. J.; Hull, J. F.; Murphy, C. F.; Kent, C.
A.; Westlake, B. C.; Paul, A.; Ess, D. H.; McCafferty, D. G.; Meyer, T.
J., Chem. Rev. 2012, 112, 4016-4093.
1
2
3
4
5
6
7
8
9
1
1
1
1
1
1
1
1
1
1
2
2
2
2
2
2
2
2
2
2
3
3
3
3
3
3
3
3
3
3
4
4
4
4
4
4
4
4
4
4
5
5
5
5
5
5
5
5
5
5
6
10. (a) Shirin, Z.; Hammes, B. S.; Young, V. G.; Borovik, A. S., J. Am.
Chem. Soc. 2000, 122, 1836-1837; (b) MacBeth, C. E.; Gupta, R.;
Mitchell-Koch, K. R.; Young, V. G.; Lushington, G. H.; Thompson, W.
H.; Hendrich, M. P.; Borovik, A. S., J. Am. Chem. Soc. 2004, 126,
2556-2567; (c) Shook, R. L.; Peterson, S. M.; Greaves, J.; Moore, C.;
Rheingold, A. L.; Borovik, A. S., J. Am. Chem. Soc. 2011, 133, 5810-
5817; (d) Borovik, A. S., Acc. Chem. Res. 2005, 38, 54-61; (e) Ford,
C. L.; Park, Y. J.; Matson, E. M.; Gordon, Z.; Fout, A. R., Science
2016, 354, 741-743; (f) Zong, R.; Thummel, R. P., J. Am. Chem. Soc.
2005, 127, 12802-12803; (g) Dogutan, D. K.; McGuire, R.; Nocera,
D. G., J. Am. Chem. Soc. 2011, 133, 9178-9180; (h) Chang, C. J.;
Chng, L. L.; Nocera, D. G., J. Am. Chem. Soc. 2003, 125, 1866-1876;
(i) Carver, C. T.; Matson, B. D.; Mayer, J. M., J. Am. Chem. Soc.
2012, 134, 5444-5447; (j) Rigsby, M. L.; Wasylenko, D. J.; Pegis, M.
L.; Mayer, J. M., J. Am. Chem. Soc. 2015, 137, 4296-4299.
11. A CSD search of small Mn clusters displaying terminal hydroxide
ligands resulted in few examples characterized by crystallography: (a)
Wieghardt, K.; Bossek, U.; Nuber, B.; Weiss, J.; Bonvoisin, J.; Corbella,
M.; Vitols, S. E.; Girerd, J. J., J. Am. Chem. Soc. 1988, 110, 7398-
7411; (b) Pal, S.; Armstrong, W. H., Inorg. Chem. 1992, 31, 5417-
5423; (c) Pal, S.; Chan, M. K.; Armstrong, W. H., J. Am. Chem. Soc.
1992, 114, 6398-6406; (d) Chen, H. Y.; Collomb, M. N.; Duboc, C.;
Blondin, G.; Riviere, E.; Faller, J. W.; Crabtree, R. H.; Brudvig, G. W.,
Inorg. Chem. 2005, 44, 9567-9573; (e) Corbella, M.; Costa, R.; Ribas,
J.; Fries, P. H.; Latour, J. M.; Ohrstrom, L.; Solans, X.; Rodriguez, V.,
Inorg. Chem. 1996, 35, 1857-1865; (f) Ng, G. K. Y.; Ziller, J. W.;
Borovik, A. S., Chem. Commun. 2012, 48, 2546-2548.
5
1
6
. Tsui, E. Y.; Kanady, J. S.; Agapie, T., Inorg. Chem. 2013, 52, 13833-
3848.
. (a) Zhang, C. X.; Chen, C. H.; Dong, H. X.; Shen, J. R.; Dau, H.;
Zhao, J. Q., Science 2015, 348, 690-693; (b) Kanady, J. S.; Lin, P. H.;
Carsch, K. M.; Nielsen, R. J.; Takase, M. K.; Goddard, W. A.; Agapie,
T., J. Am. Chem. Soc. 2014, 136, 14373-14376; (c) Mukherjee, S.;
Stull, J. A.; Yano, J.; Stamatatos, T. C.; Pringouri, K.; Stich, T. A.;
Abboud, K. A.; Britt, R. D.; Yachandra, V. K.; Christou, G., Proc. Natl.
Acad. Sci. U.S.A. 2012, 109, 2257-2262; (d) Kanady, J. S.; Tsui, E. Y.;
Day, M. W.; Agapie, T., Science 2011, 333, 733-736.
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
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5
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2
3
4
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0
7. (a) Limburg, J.; Vrettos, J. S.; Liable-Sands, L. M.; Rheingold, A. L.;
Crabtree, R. H.; Brudvig, G. W., Science 1999, 283, 1524-1527; (b)
Naruta, Y.; Sasayama, M.; Sasaki, T., Angew. Chem. Int. Ed. 1994, 33,
1
839-1841; (c) Karlsson, E. A.; Lee, B. L.; Åkermark, T.; Johnston, E.
V.; Kärkäs, M. D.; Sun, J. L.; Hansson, O.; Bäckvall, J.; Åkermark, B.,
Angew. Chem. Int. Ed. 2011, 50, 11715-11718; (d) Najafpour, M. M.;
Renger, G.; Holynska, M.; Moghaddam, A. N.; Aro, E. M.; Carpentier,
R.; Nishihara, H.; Eaton-Rye, J. J.; Shen, J. R.; Allakhverdiev, S. I.,
Chem. Rev. 2016, 116, 2886-2936; (e) Poulsen, A. K.; Rompel, A.;
McKenzie, C. J., Angew. Chem. Int. Ed. 2005, 44, 6916-6920; (f)
Beckmann, K.; Uchtenhagen, H.; Berggren, G.; Anderlund, M. F.;
Thapper, A.; Messinger, J.; Styring, S.; Kurz, P., Energ. Environ. Sci.
2
008, 1, 668-676; (g) Ruettinger, W.; Yagi, M.; Wolf, K.; Bernasek, S.;
Dismukes, G. C., J. Am. Chem. Soc. 2000, 122, 10353-10357; (h)
Brimblecombe, R.; Kolling, D. R. J.; Bond, A. M.; Dismukes, G. C.;
Swiegers, G. F.; Spiccia, L., Inorg. Chem. 2009, 48, 7269-7279; (i)
Dismukes, G. C.; Brimblecombe, R.; Felton, G. A. N.; Pryadun, R. S.;
Sheats, J. E.; Spiccia, L.; Swiegers, G. F., Acc. Chem. Res. 2009, 42,
12. Tsui, E. Y.; Kanady, J. S.; Day, M. W.; Agapie, T., Chem. Commun.
2011, 47, 4189-4191.
1
8
935-1943.
13. (a) de Ruiter, G.; Thompson, N. B.; Lionetti, D.; Agapie, T., J. Am.
Chem. Soc. 2015, 137, 14094-14106; (b) de Ruiter, G.; Thompson,
N. B.; Takase, M. K.; Agapie, T., J. Am. Chem. Soc. 2016, 138, 1486-
1489; (c) de Ruiter, G.; Carsch, K. M.; Gul, S.; Chatterjee, R.;
Thompson, N. B.; Takase, M. K.; Yano, J.; Agapie, T., Angew. Chem.
Int. Ed. 2017, 56, 4772-4776. (d) Kanady, J. S.; Tran, R.; Stull, J. A.;
Lu, L.; Stich, T. A.; Day, M. W.; Yano, J.; Britt, R. D.; Agapie, T., Chem.
Sci. 2013, 4, 3986-3996.
14. Sickerman, N. S.; Park, Y. J.; Ng, G. K. Y.; Bates, J. E.; Hilkert, M.;
Ziller, J. W.; Furche, F.; Borovik, A. S., Dalton Trans. 2012, 41, 4358-
4364.
15. Zhou, M. J.; Diwu, Z. J.; PanchukVoloshina, N.; Haugland, R. P.,
Anal. Biochem. 1997, 253, 162-168.
. (a) Evangelisti, F.; More, R.; Hodel, F.; Luber, S.; Patzke, G. R., J.
Am. Chem. Soc. 2015, 137, 11076-11084; (b) Yin, Q. S.; Tan, J. M.;
Besson, C.; Geletii, Y. V.; Musaev, D. G.; Kuznetsov, A. E.; Luo, Z.;
Hardcastle, K. I.; Hill, C. L., Science 2010, 328, 342-345; (c) Stracke,
J. J.; Finke, R. G., J. Am. Chem. Soc. 2011, 133, 14872-14875; (d)
Brimblecombe, R.; Swiegers, G. F.; Dismukes, G. C.; Spiccia, L.,
Angew. Chem. Int. Ed. 2008, 47, 7335-7338; (e) Hocking, R. K.;
Brimblecombe, R.; Chang, L. Y.; Singh, A.; Cheah, M. H.; Glover, C.;
Casey, W. H.; Spiccia, L., Nat. Chem. 2011, 3, 461-466; (f) McCool,
N. S.; Robinson, D. M.; Sheats, J. E.; Dismukes, G. C., J. Am. Chem.
Soc. 2011, 133, 11446-11449; (g) Berardi, S.; La Ganga, G.; Natali,
M.; Bazzan, I.; Puntoriero, F.; Sartorel, A.; Scandola, F.; Campagna, S.;
Bonchio, M., J. Am. Chem. Soc. 2012, 134, 11104-11107; (h) Smith,
P. F.; Kaplan, C.; Sheats, J. E.; Robinson, D. M.; McCool, N. S.; Mezle,
N.; Dismukes, G. C., Inorg. Chem. 2014, 53, 2113-2121; (i) Ullman,
A. M.; Liu, Y.; Huynh, M.; Bediako, D. K.; Wang, H. S.; Anderson, B.
L.; Powers, D. C.; Breen, J. J.; Abruna, H. D.; Nocera, D. G., J. Am.
Chem. Soc. 2014, 136, 17681-17688; (j) Nguyen, A. I.; Ziegler, M. S.;
Ona-Burgos, P.; Sturzbecher-Hohne, M.; Kim, W.; Bellone, D. E.;
Tilley, T. D., J. Am. Chem. Soc. 2015, 137, 12865-12872; (k) Smith,
P. F.; Hunt, L.; Laursen, A. B.; Sagar, V.; Kaushik, S.; Calvinho, K. U.
D.; Marotta, G.; Mosconi, E.; De Angelis, F.; Dismukes, G. C., J. Am.
Chem. Soc. 2015, 137, 15460-15468; (l) Okamura, M.; Kondo, M.;
Kuga, R.; Kurashige, Y.; Yanai, T.; Hayami, S.; Praneeth, V. K. K.;
Yoshida, M.; Yoneda, K.; Kawata, S.; Masaoka, S., Nature 2016, 530,
16. Pegis, M. L.; Roberts, J. A. S.; Wasylenko, D. J.; Mader, E. A.; Appel,
A. M.; Mayer, J. M., Inorg. Chem. 2015, 54, 11883-11888.
17. A MnO
x
catalyst has been shown to produce H
2
2
O only at basic
pH: Izgorodin, A.; Izgorodina, E.; MacFarlane, D. R., Energ. Environ.
Sci. 2012, 5, 9496-9501.
4
65-468; (m) Cady, C. W.; Crabtree, R. H.; Brudvig, G. W., Coord.
Chem. Rev. 2008, 252, 444-455.
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Waterꢀoxidation:
Ser169
R
R
N
NH
OTf [H O]
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R
H
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H
O
O
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Ca
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Asp61
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OH2
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OO
Mn
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Mn
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Biological
Oxygen Evolving Complex
Synthetic Model
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