A Manganese(IV)-Hydroperoxo Intermediate Generated by Protonation of the Corresponding Manganese(III)-Superoxo Complex

Article abstract of DOI:10.1021/jacs.0c02756

Earlier work revealed that metal-superoxo species primarily function as radicals and/or electrophiles. Herein, we present ambiphilicity of a MnIII-superoxo complex revealed by its proton- A nd metal-coupled electron-transfer processes. Specifically, a MnIV-hydroperoxo intermediate, [Mn(BDPBrP)(OOH)]+ (1, H2BDPBrP = 2,6-bis((2-(S)-di(4-bromo)phenylhydroxylmethyl-1-pyrrolidinyl)methyl)pyridine) was generated by treatment of a MnIII-superoxo complex, Mn(BDPBrP)(O2a￠) (2) with trifluoroacetic acid at-120 °C. Detailed insights into the electronic structure of 1 are obtained using resonance Raman and multi-frequency electron paramagnetic resonance spectroscopies coupled with density functional theory calculations. Similarly, the reaction of 2 with scandium(III) triflate was shown to give a Mn(IV)/Sc(III) bridging peroxo species, [Mn(BDPBrP)(OO)Sc(OTf)n](3-n)+ (4). Furthermore, it is found that deprotonation of 1 quantitatively regenerates 2, and that one-electron oxidation of the corresponding MnIII-hydroperoxo species, Mn(BDPBrP)(OOH) (3), also yields 1.

Full text of DOI:10.1021/jacs.0c02756

Subscriber access provided by The University of Melbourne Libraries
Communication
A Manganese(IV)-Hydroperoxo Intermediate Generated by
Protonation of the Corresponding Manganese(III)-Superoxo Complex
Yen-Hao Lin, Yury Kutin, Maurice van Gastel, Eckhard
Bill, Alexander Schnegg, Shengfa Ye, and Way-Zen Lee
J. Am. Chem. Soc., Just Accepted Manuscript • DOI: 10.1021/jacs.0c02756 • Publication Date (Web): 15 May 2020
Downloaded from pubs.acs.org on May 16, 2020
Just Accepted
“Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted
online prior to technical editing, formatting for publication and author proofing. The American Chemical
Society provides “Just Accepted” as a service to the research community to expedite the dissemination
of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in
full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully
peer reviewed, but should not be considered the official version of record. They are citable by the
Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore,
the “Just Accepted” Web site may not include all articles that will be published in the journal. After
a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web
site and published as an ASAP article. Note that technical editing may introduce minor changes
to the manuscript text and/or graphics which could affect content, and all legal disclaimers and
ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or
consequences arising from the use of information contained in these “Just Accepted” manuscripts.
is published by the American Chemical Society. 1155 Sixteenth Street N.W.,
Washington, DC 20036
Published by American Chemical Society. Copyright © American Chemical Society.
However, no copyright claim is made to original U.S. Government works, or works
produced by employees of any Commonwealth realm Crown government in the course
of their duties.

Page 1 of 7
Journal of the American Chemical Society
1
2
3
4
5
6
7
8
9
A Manganese(IV)-Hydroperoxo Intermediate Generated by Protona-
tion of the Corresponding Manganese(III)-Superoxo Complex
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
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
†
‡,§
⊥
‡
,‡
Yen-Hao Lin, Yury Kutin, Maurice van Gastel, Eckhard Bill, Alexander Schnegg,* Shengfa
Ye,*, and Way-Zen Lee*
⊥,∞
,†,#
†Department of Chemistry, National Taiwan Normal University, Taipei 11677, Taiwan
‡Max-Planck-Institut fꢀr Chemische Energiekonversion, Mꢀlheim an der Ruhr D-45470, Germany
⊥Max-Planck-Institut fꢀr Kohlenforschung, Mꢀlheim an der Ruhr D-45470, Germany
∞State Key Laboratory of Catalysis, Dalian Institute of Chemical Physics, Chinese Academy of Sciences, Dalian
1
16023, China
#Department of Medicinal and Applied Chemistry, Kaohsiung Medical University, Kaohsiung 807, Taiwan
ABSTRACT: Earlier work revealed that metal-superoxo species primarily function as radicals and/or electrophiles. Herein,
III
we present ambiphilicity of a Mn -superoxo complex revealed by its proton- and metal-coupled electron transfer processes.
IV
Br
+
Br
Specifically, an unprecedented Mn -hydroperoxo intermediate, [Mn(BDP P)(OOH)] (1, H
2
BDP P = 2,6-bis((2-(S)-di(4-
III
bromo)phenylhydroxylmethyl-1-pyrrolidinyl)methyl)pyridine) was generated by treatment of a Mn -superoxo complex,
Mn(BDP P)(O ) (2) with trifluoroacetic acid at −120 °C. Detailed insights in the electronic structure of 1 are obtained by
Br
•
2
characterizations using resonance Raman and multi-frequency electron paramagnetic resonance spectroscopies coupled
with density functional theory calculations. Similarly, the reaction of 2 with scandium(III) triflate was shown to give a
Br
(3-n)+
Mn(IV)/Sc(III) bridging peroxo species, [Mn(BDP P)(OO)Sc(OTf)
n
]
(4). Furthermore, it is found that deprotonation
III
of 1 quantitatively regenerates 2, and that one-electron oxidation of the corresponding Mn -hydroperoxo species,
Br
Mn(BDP P)(OOH) (3), also yields 1.
7
Metal-superoxo species are key intermediates for O
2
acti-
ford the ketone final product (Scheme 1B). Moreover, ki-
1
II
•
−
vation and transport and have been found to carry out var-
ious transformations. Not surprisingly, they function as
netic investigations on the reactions of [LCu (O )] with a
series of acidic para-substituted phenols suggested for-
mation of a transient intermediate that was hypothesized
to be a Cu -hydroperoxo species (Scheme 1C). However,
spectroscopic evidence for its existence remains lacking. In
fact, a similar proton-coupled electron transfer process,
which effects a superoxo-to-hydrperoxo conversion with
the distal Fe center being the electron donor, has been put
forward to rationalize reversible O binding in hemerythrin
(Scheme 1D). To be precise, in the aforementioned four
reactions, the superoxo moiety was proposed to act not
only as a nucleophile but also as an electrophile. How-
ever, such an ambiphilic character of the metal bound su-
peroxo moiety has yet to be experimentally confirmed.
2
•
radicals as indicated by their reactions with NO and radi-
2
III
8
cal substrates to form metal-peroxynitrite and -al-
3
kylperoxo complexes. Furthermore, they perform hydro-
gen atom abstraction (HAA) and oxygen atom transfer to
4
5
produce metal-hydroperoxo and -oxo complexes, reflect-
ing their electrophilicity. In contrast, reactions of metal-
superoxo species with electrophiles are complex, and their
role in such reactions has not been clearly established. For
II
2
1
c,9
O
2
activation mediated by -ketoglutarate (KG) depend-
III
10
ent dioxygenases, a Fe -superoxo intermediate was pro-
posed to initiate nucleophilic attack on the carbonyl group
(
C =O) of KG, which is concurrent with two-electron
β
transfer from the C
superoxo moiety. Eventually, the reaction yields an Fe -al-
kylperoxo intermediate and releases CO

-C
β
-bond to the Fe center and the
II
6
2
(Scheme 1A). An
analogous mechanism may be operative for the reaction of
II
•
−
[
LCu (O )] (L = N,N’-bis(2,6-diisopropylphenyl)-2,6-pyri-
2
dinedicarboxamide) with 2-phenylpro-pionaldehyde (2-
III
PPA). The reaction first generates a Cu -alkylperoxo inter-
mediate, which then undergoes C−C bond cleavage to af-
ACS Paragon Plus Environment

Journal of the American Chemical Society
Page 2 of 7
Scheme 1. Reactivities of Reported Metal-Superoxo
Species
solution of 2 at −80 °C, a transient intermediate 1 was de-
tected within 2 min before its rapid decomposition (Figure
S3). In order to increase the lifetime of 1, we carried out the
reaction in MeTHF at −120 °C and found no detectable de-
cay. Upon treating 2 with TFA, an immediate color change
from yellow to dark-purple was observed, and at the same
time three isosbestic points at 430, 470 and 660 nm
emerged, suggesting complete conversion without inter-
vening intermediates. Complex 1 exhibits two characteris-
tic UV-vis absorption bands at 370 and 530 nm (Figures S4
and 1). Further titration experiments (the inset of Figure 1)
confirmed that the highest yield of 1 was achieved by add-
ing 1 equiv of TFA with an equilibrium constant Keq of ~ 102
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
A
His
Asp
His
His
Asp FeIII O
His
His
Asp FeII
His
His
Asp FeIV
O
His
FeII
O
O2
O
O
O
O
O
O
O
O
O
O
CO2
O
O
O
O
O
O
O
O
O
B
O
O
O
H
H3C
H
H3C
H
H3C
O
H
O
3
H C
O
H
H
+
O
+
O
O
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
O
O
LCuIII
LCuIII
HO
LCuII
H
X
C
D
HO
X
O
X
(
Figure S5). Conversely, treating 1 equiv of 1,8-diazabicy-
+
clo[5.4.0]undec-7-ene (DBU) or NEt to a MeTHF solution
3
O
X = NO2, CF3, Cl
OH
O
O
O
of 1 at −120 °C quantitatively regenerated 2 (Figures S6 and
S7).
LCuII
LCuIII
LCuII
(
L = N,N’-bis(2,6-diisopropylphenyl)-2,6-pyridinedicarboxamide)
H
O
H
O
H
O
O
Complex 1 can also be generated from one-electron oxi-
His
His
His
His
O
His
His
O
His
His
His
FeIII
O
His
FeIII
Br
O2
dation of Mn(BDP P)(OOH) (3). Adding equimolar of
FeII
O
FeII
FeII
O
FeIII
O
His
O
O
His
O
O
His
O
O
tris(4-bromophenyl)ammoniumyl hexachloroantimonate,
often referred to as magic blue, to a n-PrCN solution of 3 at
−110 °C resulted in a dark-purple solution, whose absorp-
tion spectrum displayed the same signature features as
those found for 1 (Figure S8). Conversely, addition of
equimolar of decamethylferrocene (Fc*) to a MeTHF solu-
tion of in situ prepared 1 at −120 °C lead to a pale-purple
solution, which showed identical features as those ob-
served for 3 (Figure S9, black trace). On the basis of these
His
His
O
O
O
Scheme 2. Reaction of 2 with 2-PPA, Reversible Inter-
conversion of 1, 2 and 3, and Formation of 4
O
O
H
CH3
H
III
H3C
findings, we surmised that complex 1 is either a Mn -hy-
Br
Br
+
Br
Br
IV
droperoxyl or a Mn -hydroperoxo species.
N
N
H+
Base
O
N
O
N
N
MnIII
N
MnIV
O
O
_
O
O
O
Br
Br
Br
Br
HO
2
1
Sc(OTf)3
TEMPOH
Ox. Red.
Br
(3-n)+
Br
Br
Br
N
N
O
N
O
N
N
MnIV
N
MnIII
O
O
O
O
Br
Br
Br
OTf)nScIII
O
Br
HO
(
4
3
II
II
Recently, some of us reported that adding O
2
to Fe , Co
II
and Mn , precursors lead to formation of the correspond-
ing trivalent metal-superoxo species, which can activate a
weak O-H bond to convert into the metal-hydroperoxo
Figure 1. UV-vis spectral changes of the reaction of 2 (1.0
mM, orange trace) with 1 equiv of TFA in MeTHF at −120
11
complexes via HAA (Scheme 2). In light of the transfor-
°
C. Inset: titration curve of 2 with TFA. X-axis: the equiva-
mations discussed above, herein we examined reactions of
III
Br
•
Br
lent of TFA, Y-axis: the conversion ratio of the absorption
peak at 530 nm.
Mn -superoxo complex Mn(BDP P)(O
2
) (2, H BDP P =
2
2
,6-bis((2-(S)-di(4-bromo)phenylhydroxylmethyl-1-pyr-
rolidinyl)methyl)pyridine) with 2-PPA and trifluoroacetic
acid (TFA). Reaction of 2 with 100 equiv of 2-PPA in THF
at −80 °C exhibited a gradual decay in a period of 7.5 hr.
GC-MS analyses revealed that the resulting mixture con-
tained 92% of acetophenone product relative to 2 (Figure
S1). However, during the reaction no intermediate has been
accumulated as monitored by using UV-vis spectroscopy
To identify the nature of 1, resonance Raman (rR) and
multi-frequency EPR spectroscopies were employed. Its rR
(
λ
ex at 594 nm, in CH
2
Cl ) spectrum exhibited signals at 860
2
−1
−1
and 584 cm , which shifted to 813 and 561 cm , respec-
tively, upon O substitution (Figure 2). The two features
18
can be assigned to the O–O (the former) and Mn–O (the
latter) stretching vibrations, based on the observed isotope
(
Figure S2), a similar situation encountered in earlier stud-
–1
shifts of 47 and 23 cm matching the values estimated by
7
ies. In contrast, when 1 equiv of TFA was added to a THF
ACS Paragon Plus Environment

Page 3 of 7
Journal of the American Chemical Society
–
1
Hooke’s Law. More importantly, the O–O stretching fre-
quency measured for 1 indicates its O moiety is at the
 1.2 cm . An upper boundary can be determined from ’.
1
2
3
4
5
6
7
8
9
–1
2
From this transition D = 1.25 cm was determined. Further-
more, the |A
(hf) tensor (inset in Figure 3A) can be determined from the
55
peroxo level (Table S1). As seen in Table S1, the O–O
z
| and |A | components of the Mn hyperfine
y
IV
stretching frequencies reported for a series of Mn -peroxo
complexes are all considerably higher than that deter-
mined for 1. Furthermore, the rR spectrum of the one-elec-
tron oxidized form of 3 is nearly identical to that of 1. Both
observations suggest that 1 probably contains a hydroper-
oxo ligand (Figure S10).
partly overlapping  and . For  and  no resolved hf-split-
ting is observed. Thus, the A component could not be de-
x
termined. Spin Hamiltonian parameters of 1 are summa-
rized in Table 1. The obtained axial zfs lies in the range,
which was previously found for a series of well-character-
IV
ized high-spin Mn complexes featuring similar coordina-
*
* *
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
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
tion environments. This allows us to safely assign a 4+ ox-
idation state to the Mn center in 1 (see Table S2 for a com-
IV
parison of recently published Mn zfs- and hf-values).
*
*
IV
Br
+
Figure 2. rR spectra of [Mn BDP P(OOH)] (1) in frozen
1
6
CH
2
Cl (10 mM, ex 594 nm, 20 mW, 77 K; red line: 1- O,
blue line: 1- O, black line: difference spectrum 1- O − 1-
O). Asterisks denote solvent peaks.
2
1
8
16
1
8
Figure 3 depicts X-band (A, fmw ≈ 9.4 GHz) and Q-band
B, fmw ≈ 34 GHz) EPR spectra of 1 alongside spin-energy
(
levels for different orientations of the magnetic field (B
0
)
to the zfs-tensor. X-band EPR simulations assume S = 3/2,
1
2
positive axial zfs (D) and non-zero rhombicity E/D. From
simulations it was concluded that the energy gap between
the ground and excited state doublets is significantly larger
–
1
than 0.3 cm . Consequently, X-band mw quanta can only
excite transitions within the doublets (pink arrows in Fig-
ure 3; C, D and E). In the X-band spectrum the leftmost
lines are assigned to transition , corresponding to an ex-
cited state transition with parallel orientation of the z-axis
Figure 3. (A) X-band and (B) Q-band EPR spectra of 1
(
exp.: black solid and sim.: red dotted lines). The inset in
A) depicts the low-field part of the X-band spectrum,
where transitions  (purple) and  (brown) are simulated
separately. (C), (D) and (E) contain calculated spin-energy
to B
inate from ground state transitions with B
) and B || z (). The broad feature between 550 and 750
mT arises from the excited state transition  with B || x.
The X-band EPR line shape is largely determined by E/D =
0
(B
0
|| z). The intense resonances at higher fields orig-
levels for B
0
|| y, B
0
|| x and B || z, respectively. Pink and
0
0
|| y (), B || x
0
blue arrows indicate X- and Q-band transitions, respec-
tively. Individual transitions are labeled with small Greek
letters. Measurement conditions: Continuous wave (cw) X-
band: T = 10 K, fmw = 9.6 GHz; pseudo-modulated pulse Q-
band: T = 9 K, fmw = 34.2 GHz.
(
0
0
1
2
0
.163(6). As depicted in Figure S11B, the relative intensity
of  increases with temperature. From the temperature de-
–
1
pendence of , D ~ 1 cm was approximated (Figure S11C).
A precise assignment of D was obtained by simulating ’
and ’ in the Q-band spectrum.
Table 1. Spin Hamiltonian parameters of 1.
g-tensor
= 1.989
g = 1.982
Axial zfs
E/D
55Mn hf-tensor,
|A | = 180 MHz
|A | = 193 MHz
-
1
Q-band microwave energies (1.14 cm ) can excite inter-
doublet transition  (see Figure 4E). ’ overlaps with , di-
rectly reflecting the size of D. For larger D,  shifts rapidly
to higher magnetic fields (see Figure S15). The fact that
these features are not observed sets a lower boundary of D
D = 1.25 cm–1
0.163
g
⊥
y
||
z
ACS Paragon Plus Environment

Journal of the American Chemical Society
To gain more insight into the nature of 1, especially the
Page 4 of 7
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
protonation state of the peroxo ligand, we have computa-
tionally investigated a series of models for 1 (Figure 4). Spe-
cifically, the O moiety features different binding modes in
2
D – G, whereas A – C contain hydroperoxo ligands. On the
basis of the computed O–O stretching frequencies, D – G
were ruled out, because the calculated values are at least
–
1
100 cm higher than experiment. Moreover, D and E are
more than 17 kcal/mol higher in energy than A and B.
These findings indicate that the O moiety in 1 is not a
2
peroxo, but a hydroperoxo. Formation of an intramolecular
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
H-bond (1.735 Å) in A between the hydroperoxo ligand and
Br 2−
one of the two O donors in BDP P ligand further lowers
its energy by 3.8 kcal/mol relative to B. C possesses an H-
−
bond of the hydroperoxo ligand with CF
3
COO and hence
can be viewed as the initial stage of B. Theoretical results
−
revealed that dissociation of CF
3
COO in C to finally con-
vert into A is exergonic. Of all models, A is the only one
that successfully reproduces the sign of D (Table S3), and
the estimated magnitudes of D for A – C are all within the
1
3
uncertainty range of the calculations. Therefore, A should
be the most viable model for 1. The MO analysis further
Figure 4. Computed Models for 1.
IV
confirms that A is a high-spin Mn -hydroperoxo species
During the reaction of 2 with TFA, the doubly occupied
O–O π* orbital of 2 donates the electron density to the in-
coming proton leading to a nascent O–H bond in 1. Mean-
while, the singly populated O–O π* orbital accepts an elec-
tron from the Mn center. As such, the ambiphilicity of the
superoxo moiety in 2 should be traced back to a common
electronic-structure feature of metal-superoxo species, i.e.
all have a doubly and a singly occupied O–O π* orbital in
the upper valence region, which therefore imparts am-
biphilicity to them.
(
Figure S17).
IV
Complex 1 represents the first example of Mn -hydrop-
eroxo complexes reported thus far, which prompted us to
examine the reaction of 2 with Lewis acids. Treatment of 2
with Sc(OTf) in THF at −80 °C generated a product, which
3
showed nearly identical absorption and EPR spectra to
those found for 1 (Figures S18 and S19). Furthermore, its rR
−
1
−1
spectrum displayed νO-O at 858 cm and νMn-O at 581 cm ,
−
1
18
which shifted to 813 and 561 cm , respectively, upon
O
substitution (Figure S20). All observations thus suggest
III
In summary, protonation of Mn -superoxo 2 affords
IV
III
formation of an unprecedented Mn -peroxo-Sc species,
IV
Mn -hydroperoxo 1 and treatment of 2 with Sc(OTf)
3
Br
(3-n)+
[Mn(BDP P)(OO)Sc(OTf)
n
]
(4). The present findings
IV
III
yields Mn -peroxo-Sc 4. Both reactions provide strong
experimental supported for the proposed ambiphilic prop-
erty for the metal-superoxo complexes. Interestingly,
are distinct from a previous study, which revealed that re-
II
•
+
2
action of [L’Cu (O
2
)] (L’ = 1,1,1-tris(2-(N -1,1,3,3-tetra-
methylguanidino)ethyl)amine) with TFA afforded a 1:1 hy-
III
Mn -superoxo 2 can be quantitatively regenerated from
II
•
+ 14
drogen bond adduct, [L’Cu (O )(TFA)] .
2
deprotonation of 1, and 1 can also be prepared from one-
III
electron oxidation of Mn -hydroperoxo 3. Our present
findings represent an important step towards better under-
standing of O activation and evolution processes occur-
2
ring in metalloenzymes and artificial catalysts.
ASSOCIATED CONTENT
Supporting Information
The Supporting Information is available free of charge on the
ACS Publications website.
Experimental procedures, UV–vis, EPR, rR spectra and com-
putational results (PDF)
AUTHOR INFORMATION
Corresponding Author
*
*
*
wzlee@ntnu.edu.tw;
shengfa.ye@kofo.mpg.de;
alexander.schnegg@cec.mpg.de
ACS Paragon Plus Environment

Page 5 of 7
Journal of the American Chemical Society
Present Addresses
§Y.K. Department of Chemistry and Chemical Biology, TU
Dortmund University, D-44227 Dortmund, Germany
Rev. 2018, 358, 178-180; (c) Gardner, P. R.; Gardner, A. M.;
1
2
3
4
5
6
7
8
9
Martin, L. A.; Salzman, A. L. Nitric Oxide Dioxygenase: An
Enzymic Function for Flavohemoglobin. Proc. Natl. Acad. Sci.
U. S. A. 1998, 95, 10378-10383; (d) Das, A. K.; Meuwly, M.
Kinetic Analysis and Structural Interpretation of Competitive
Ligand Binding for NO Dioxygenation in Truncated
Hemoglobin N. Angew. Chem. Int. Ed. 2018, 57, 3509-3513; (e)
Sharma, S. K.; Schaefer, A. W.; Lim, H.; Matsumura, H.;
Moënne-Loccoz, P.; Hedman, B.; Hodgson, K. O.; Solomon, E.
I.; Karlin, K. D. A Six-Coordinate Peroxynitrite Low-Spin
Iron(III) Porphyrinate Complex—The Product of the Reaction
of Nitrogen Monoxide (·NO(g)) with a Ferric-Superoxide
Species. J. Am. Chem. Soc. 2017, 139, 17421-17430; (f) Cao, R.;
Elrod, L. T.; Lehane, R. L.; Kim, E.; Karlin, K. D. A Peroxynitrite
ACKNOWLEDGMENT
We thank Mr. Dennis Skerra at the Max-Planck Institute for
Chemical Energy Conversion for rRaman measurements and
Mr. Tzu-Hsien Tseng at Department of Chemistry, National
Chung Hsing University for variable temperature CW X-band
EPR measurements. The authors are grateful for the financial
supports from the Ministry of Science and Technology of Tai-
wan (MOST 108-2113-M-003-009-MY3 to W.-Z.L.) and the
Max-Planck Society. W.-Z.L. and S.Y. also acknowledge the
MOST-DAAD Project-Based Personnel Exchange Program
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
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
Dicopper Complex: Formation via Cu-NO and Cu-O
2
(
MOST 107-2911-I-003-502 and DAAD 57320810).
Intermediates and Reactivity via O-O Cleavage Chemistry. J.
Am. Chem. Soc. 2016, 138, 16148-16158; (g) Liu, J. J.; Siegler, M.
A.; Karlin, K. D.; Moenne-Loccoz, P. Direct Resonance Raman
REFERENCES
(
1) For selected examples: (a) Kovaleva, E. G.; Lipscomb, J. D.
Characterization of
a
Peroxynitrito Copper Complex
Versatility of Biological Non-Heme Fe(II) Centers in Oxygen
Activation Reactions. Nat. Chem. Biol. 2008, 4, 186-193; (b)
Costas, M.; Mehn, M. P.; Jensen, M. P.; Que, L. Dioxygen
Activation at Mononuclear Nonheme Iron Active Sites:ꢀ
Enzymes, Models, and Intermediates. Chem. Rev. 2004, 104,
939-986; (c) Jasniewski, A. J.; Que, L., Jr. Dioxygen Activation
by Nonheme Diiron Enzymes: Diverse Dioxygen Adducts,
High-Valent Intermediates, and Related Model Complexes.
Chem. Rev. 2018, 118, 2554-2592; (d) Elwell, C. E.; Gagnon, N.
L.; Neisen, B. D.; Dhar, D.; Spaeth, A. D.; Yee, G. M.; Tolman,
W. B. Copper-Oxygen Complexes Revisited: Structures,
Spectroscopy, and Reactivity. Chem. Rev. 2017, 117, 2059-2107;
Generated from O and NO and Mechanistic Insights into
2
Metal-Mediated Peroxynitrite Decomposition. Angew. Chem.
Int. Ed. 2019, 58, 10936-10940.
(
3) For selected examples: (a) Kovaleva, E. G.; Lipscomb, J. D.
2+
Crystal Structures of Fe Dioxygenase Superoxo, Alkylperoxo,
and Bound Product Intermediates. Science 2007, 316, 453; (b)
Kumar, P.; Lindeman, S. V.; Fiedler, A. T. Cobalt Superoxo and
Alkylperoxo Complexes Derived from Reaction of Ring-
Cleaving Dioxygenase Models with O
41, 10984-10987.
4) For selected examples: (a) Blakely, M. N.; Dedushko, M.
A.; Yan Poon, P. C.; Villar-Acevedo, G.; Kovacs, J. A. Formation
of Reactive, Alkyl Thiolate-Ligated Fe(III)-Superoxo
Intermediate Derived from Dioxygen. J. Am. Chem. Soc. 2019,
41, 1867-1870; (b) Kunishita, A.; Kubo, M.; Sugimoto, H.;
2
. J. Am. Chem. Soc. 2019,
1
(
(
e) Dickman, M. H.; Pope, M. T. Peroxo and Superoxo
a
Complexes of Chromium, Molybdenum, and Tungsten. Chem.
Rev. 1994, 94, 569-584; (f) Ray, K.; Pfaff, F. F.; Wang, B.; Nam,
W. Status of Reactive Non-Heme metal-Oxygen Intermediates
in Chemical and Enzymatic Reactions. J. Am. Chem. Soc. 2014,
136, 13942-13958; (g) Sahu, S.; Goldberg, D. P. Activation of
Dioxygen by Iron and Manganese Complexes: A Heme and
Nonheme Perspective. J. Am. Chem. Soc. 2016, 138, 11410-11428;
1
Ogura, T.; Sato, K.; Takui, T.; Itoh, S. Mononuclear
Copper(II)−Superoxo Complexes that Mimic the Structure
and Reactivity of the Active Centers of PHM and DβM. J. Am.
Chem. Soc. 2009, 131, 2788-2789; (c) Peterson, R. L.; Himes, R.
A.; Kotani, H.; Suenobu, T.; Tian, L.; Siegler, M. A.; Solomon,
E. I.; Fukuzumi, S.; Karlin, K. D. Cupric Superoxo-Mediated
Intermolecular C−H Activation Chemistry. J. Am. Chem. Soc.
(
h) Fukuzumi, S.; Lee, Y. M.; Nam, W. Structure and Reactivity
of the First-Row D-Block Metal-Superoxo Complexes. Dalton
Trans 2019, 48, 9469-9489; (i) Noh, H.; Cho, J. Synthesis,
Characterization and Reactivity of Non-Heme 1st Row
Transition Metal-Superoxo Intermediates. Coord. Chem. Rev.
2011, 133, 1702-1705; (d) Cho, J.; Woo, J.; Nam, W. An “End-On”
Chromium(III)-Superoxo Complex: Crystallographic and
Spectroscopic Characterization and Reactivity in C−H Bond
Activation of Hydrocarbons. J. Am. Chem. Soc. 2010, 132, 5958-
2
019, 382, 126-144; (j) Cai, X.; Majumdar, S.; Fortman, G. C.;
Cazin, C. S. J.; Slawin, A. M. Z.; Lhermitte, C.; Prabhakar, R.;
Germain, M. E.; Palluccio, T.; Nolan, S. P.; Rybak-Akimova, E.
V.; Temprado, M.; Captain, B.; Hoff, C. D. Oxygen Binding to
5
959; (e) Kelm, H.; Krüger, H.-J. A Superoxovanadium(V)
Complex Linking the Peroxide and Dioxygen Chemistry of
Vanadium. Angew. Chem. Int. Ed. 2001, 40, 2344-2348.
3
[Pd(L)(L′)] (L= NHC, L′ = NHC or PR , NHC = N-Heterocyclic
(
5) For selected examples: (a) Kieber-Emmons, M. T.;
Carbene). Synthesis and Structure of a Paramagnetic trans-
Annaraj, J.; Seo, M. S.; Van Heuvelen, K. M.; Tosha, T.;
Kitagawa, T.; Brunold, T. C.; Nam, W.; Riordan, C. G.
Identification of an “End-on” Nickel−Superoxo Adduct,
1
[Pd(NHC)
2
(η -O
2
)
2
] Complex. J. Am. Chem. Soc. 2011, 133, 1290-
1
293; (k) Huacuja, R.; Graham, D. J.; Fafard, C. M.; Chen, C.-H.;
Foxman, B. M.; Herbert, D. E.; Alliger, G.; Thomas, C. M.;
Ozerov, O. V. Reactivity of a Pd(I)−Pd(I) Dimer with O
+
[
Ni(tmc)(O
Yao, S.; Bill, E.; Milsmann, C.; Wieghardt, K.; Driess, M. A
Side-on” Superoxonickel Complex [LNi(O )] with a Square-
Planar Tetracoordinate Nickel(II) Center and Its Conversion
into [LNi(μ-OH) NiL]. Angew. Chem. Int. Ed. 2008, 47, 7110-
113; (c) Cho, J.; Woo, J.; Nam, W. A Chromium(III)–Superoxo
2
)] . J. Am. Chem. Soc. 2006, 128, 14230-14231; (b)
2
:
Monohapto Pd Superoxide and Dipalladium Peroxide in
Equilibrium. J. Am. Chem. Soc. 2011, 133, 3820-3823; (l) Zhang,
X.; Loppnow, G. R.; McDonald, R.; Takats, J. {HB(3,5-
“
2
2
2
3 2 2
Me2pz) } Sm(η -O ): First Example of a Lanthanide Superoxo
7
Complex. J. Am. Chem. Soc. 1995, 117, 7828-7829.
(2) For selected examples: (a) Herold, S.; Koppenol, W. H.
Peroxynitritometal Complexes. Coord. Chem. Rev. 2005, 249,
Complex in Oxygen Atom Transfer Reactions as a Chemical
Model of Cysteine Dioxygenase. J. Am. Chem. Soc. 2012, 134,
1
1112-11115; (d) Fujita, K.; Schenker, R.; Gu, W.; Brunold, T. C.;
Cramer, S. P.; Riordan, C. G. A Monomeric Nickel−Dioxygen
Adduct Derived from a Nickel(I) Complex and O . Inorg.
4
99-506; (b) Harcourt, R. D. Oxyheme Valence Bond
Structures and the Oxyhemeꢀ+ꢀNO Reaction. Coord. Chem.
2
ACS Paragon Plus Environment

Journal of the American Chemical Society
Page 6 of 7
Chem. 2004, 43, 3324-3326; (e) Tano, T.; Okubo, Y.; Kunishita,
(10) (a) Hong, S.; Sutherlin, K. D.; Park, J.; Kwon, E.; Siegler,
M. A.; Solomon, E. I.; Nam, W. Crystallographic and
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
A.; Kubo, M.; Sugimoto, H.; Fujieda, N.; Ogura, T.; Itoh, S.
Redox Properties of a Mononuclear Copper(II)-Superoxide
Complex. Inorg. Chem. 2013, 52, 10431-10437; (f) Liu, L.-L.; Li,
H.-X.; Wan, L.-M.; Ren, Z.-G.; Wang, H.-F.; Lang, J.-P. A
Mn(iii)–Superoxo Complex of a Zwitterionic Calix[4]arene
Spectroscopic Characterization and Reactivities of
a
Mononuclear Non-Haem Iron(III)-Superoxo Complex. Nat.
Commun. 2014, 5, 5440-5547; (b) Sankaralingam, M.; Lee, Y.-
M.; Nam, W.; Fukuzumi, S. Amphoteric reactivity of metal–
oxygen complexes in oxidation reactions. Coord. Chem. Rev.
2018, 365, 41-59; (c) Corcos, A. R.; Villanueva, O.; Walroth, R.
C.; Sharma, S. K.; Bacsa, J.; Lancaster, K. M.; MacBeth, C. E.;
Berry, J. F. Oxygen Activation by Co(II) and a Redox Non-
Innocent Ligand: Spectroscopic Characterization of a Radical-
Co(II)-Superoxide Complex with Divergent Catalytic
Reactivity. J. Am. Chem. Soc. 2016, 138, 1796-1799.
(11) (a) Chiang, C. W.; Kleespies, S. T.; Stout, H. D.; Meier,
K. K.; Li, P. Y.; Bominaar, E. L.; Que, L., Jr.; Munck, E.; Lee, W.
Z. Characterization of a Paramagnetic Mononuclear Nonheme
Iron-Superoxo Complex. J. Am. Chem. Soc. 2014, 136, 10846-
10849; (b) Wang, C. C.; Chang, H. C.; Lai, Y. C.; Fang, H.; Li, C.
C.; Hsu, H. K.; Li, Z. Y.; Lin, T. S.; Kuo, T. S.; Neese, F.; Ye, S.;
Chiang, Y. W.; Tsai, M. L.; Liaw, W. F.; Lee, W. Z. A
Structurally Characterized Nonheme Cobalt-Hydroperoxo
Complex Derived from Its Superoxo Intermediate via
Hydrogen Atom Abstraction. J. Am. Chem. Soc. 2016, 138,
14186-14189; (c) Lin, Y. H.; Cramer, H. H.; van Gastel, M.; Tsai,
Y. H.; Chu, C. Y.; Kuo, T. S.; Lee, I. R.; Ye, S.; Bill, E.; Lee, W. Z.
Mononuclear Manganese(III) Superoxo Complexes: Synthesis,
Characterization, and Reactivity. Inorg. Chem. 2019, 58, 9756-
9765.
(12) (a) Bennet, B. EPR of Cobalt-Susbstituted Zinc Enzymes.
Hanson, G.; Berliner, L. (eds.), Biological Magnetic Resonance,
29, 345-370; (b) Wang, D. M.; Pilbrow, J. R. Symmetry
relationships for the four energy levels and the angular
property of the EPR spectra for a spin-3/2 system. J. Magn.
Reson. 1988, 77, 411–423.
(13) Neese, F. Calculation of the zero-field splitting tensor
on the basis of hybrid density functional and Hartree-Fock
theory. J. Chem. Phys. 2007, 127, 164112.
(14) Peterson, R. L.; Ginsbach, J. W.; Cowley, R. E.; Qayyum,
M. F.; Himes, R. A.; Siegler, M. A.; Moore, C. D.; Hedman, B.;
Hodgson, K. O.; Fukuzumi, S.; Solomon, E. I.; Karlin, K. D.
Stepwise Protonation and Electron-Transfer Reduction of a
Primary Copper-Dioxygen Adduct. J. Am. Chem. Soc. 2013, 135,
16454-16467.
with an Unprecedented Linear End-On Mn(iii)–O
2
Arrangement and Good Catalytic Performance for Alkene
Epoxidation. Chem. Commun. 2011, 47, 11146-11148.
(
6) (a) Ye, S.; Riplinger, C.; Hansen, A.; Krebs, C.; Bollinger Jr,
J. M.; Neese, F. Electronic Structure Analysis of the Oxygen-
Activation Mechanism by FeII- and α-Ketoglutarate (αKG)-
Dependent Dioxygenases. Chem. Eur. J. 2012, 18, 6555-6567; (b)
Borowski, T.; Bassan, A.; Siegbahn, P. E. M. Mechanism of
dioxygen activation in 2-oxoglutarate-dependent enzymes: a
hybrid DFT study. Chem. Eur. J. 2004, 10, 1031–1041.
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
(
7) (a) Pirovano, P.; Magherusan, A. M.; McGlynn, C.; Ure, A.;
Lynes, A.; McDonald, A. R. Nucleophilic Reactivity of a
Copper(II)–Superoxide Complex. Angew. Chem. Int. Ed. 2014,
1
26, 6056-6060; (b) Bailey, W. D.; Gagnon, N. L.; Elwell, C. E.;
Cramblitt, A. C.; Bouchey, C. J.; Tolman, W. B. Revisiting the
Synthesis and Nucleophilic Reactivity of an Anionic Copper
Superoxide Complex. Inorg. Chem. 2019, 58, 4706-4711.
(
8) Bailey, W. D.; Dhar, D.; Cramblitt, A. C.; Tolman, W. B.
Mechanistic Dichotomy in Proton-Coupled Electron-Transfer
Reactions of Phenols with a Copper Superoxide Complex. J.
Am. Chem. Soc. 2019, 141, 5470-5480.
(
9) (a) Stenkamp, R. E. Dioxygen and Hemerythrin. Chem.
Rev. 1994, 94, 715-726; (b) Takano, Y.; Isobe, H.; Yamaguchi, K.
Theoretical Studies on Electronic Structures and Chemical
Indices of the Active Site of Oxygenated and Deoxygenated
Hemerythrin. Bull. Chem. Soc. Jpn. 2008, 81, 91-102; (c)
Howard, J. B.; Rees, D. C. Perspectives on Non-Heme Iron
Protein Chemistry. Adv. Protein Chem. 1991, 42, 199-280; (d)
Reem, R. C.; McCormick, J. M.; Richardson, D. E.; Devlin, F. J.;
Stephens, P. J.; Musselman, R. L.; Solomon, E. I. Spectroscopic
Studies of the Coupled Binuclear Ferric Active Site in
Methemerythrins and Oxyhemerythrin: The Electronic
Structure of Each Iron Center and the Iron-Oxo and Iron-
Peroxide Bonds. J. Am. Chem. Soc. 1989, 111, 4688-4704; (e)
Nocek, J. M.; Kurtz, D. M.; Sage, J. T.; Debrunner, P. G.;
Maroney, M. J.; Que, L. Nitric oxide Adduct of the Binuclear
Iron Center in Deoxyhemerythrin from Phascolopsis gouldii.
Analog of a Putative Intermediate in the Oxygenation
Reaction. J. Am. Chem. Soc. 1985, 107, 3382-3384.
ACS Paragon Plus Environment

Page 7 of 7
Journal of the American Chemical Society
For Table of Contents Only
1
2
3
4
5
6
7
8
9
ν
O-O = 1125, 1145 cm-1
ν
O-O = 860 cm-1
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
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
ACS Paragon Plus Environment