Nitrosyl Linkage Isomers: NO Coupling to N2O at a Mononuclear Site

Article abstract of DOI:10.1021/jacs.8b09769

Linkage isomers of reduced metal-nitrosyl complexes serve as key species in nitric oxide (NO) reduction at monometallic sites to produce nitrous oxide (N₂O), a potent greenhouse gas. While factors leading to extremely rare side-on nitrosyls are unclear, we describe a pair of nickel-nitrosyl linkage isomers through controlled tuning of noncovalent interactions between the nitrosyl ligands and differently encapsulated potassium cations. Furthermore, these reduced metal-nitrosyl species with N-centered spin density undergo radical coupling with free NO and provide a N-N coupled cis-hyponitrite intermediate whose protonation triggers the release of N₂O. This report outlines a stepwise molecular mechanism of NO reduction to form N₂O at a mononuclear metal site that provides insight into the related biological reduction of NO to N₂O.

Full text of DOI:10.1021/jacs.8b09769

Subscriber access provided by Mount Allison University | Libraries and Archives
Communication
2
Nitrosyl Linkage Isomers: NO Coupling to NO at a Mononuclear Site
Subrata Kundu, Phan N. Phu, Pokhraj Ghosh, Stosh A. Kozimor,
Jeffery A. Bertke, S. Chantal E. Stieber, and Timothy H. Warren
J. Am. Chem. Soc., Just Accepted Manuscript • DOI: 10.1021/jacs.8b09769 • Publication Date (Web): 02 Jan 2019
Downloaded from http://pubs.acs.org on January 2, 2019
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 5
Journal of the American Chemical Society
1
2
3
4
5
6
7
8
9
Nitrosyl Linkage Isomers: NO Coupling to N O at a Mononuclear
Site
2
a,b
c
a
d
a
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
Subrata Kundu, Phan N. Phu, Pokhraj Ghosh, Stosh A. Kozimor, Jeffery A. Bertke, S. Chantal E.
,c,d
,a
Stieber,* and Timothy H. Warren*
a
Department of Chemistry, Georgetown University, Box 571227-1227, Washington, D. C. 20057 United States
b
School of Chemistry, Indian Institute of Science Education and Research Thiruvananthapuram, Kerala 695551, India
California State Polytechnic University, Pomona, California 91768, United States
c
d
Los Alamos National Laboratory, MS K558, Los Alamos, New Mexico 87545, United States
Supporting Information Placeholder
ABSTRACT: Linkage isomers of reduced metal-nitrosyl com-
plexes serve as key species in nitric oxide (NO) reduction at
monometallic sites to produce nitrous oxide (N O), a potent
2
greenhouse gas. While factors leading to extremely rare side-
on nitrosyls are unclear, we describe a pair of nickel-nitrosyl
linkage isomers through controlled tuning of non-covalent
interactions between the nitrosyl ligands and differently en-
capsulated potassium cations. Furthermore, these reduced
metal-nitrosyl species with N-centered spin density undergo
radical coupling with free NO and provide a N-N coupled cis-
hyponitrite intermediate whose protonation triggers the release
of N
of NO reduction to form N
provides insight into the related biological reduction of NO to
O.
2
O. This report outlines a stepwise molecular mechanism
2
O at a mononuclear metal site that
N
2
Nitrous oxide (N
2
O) is a long-lived (ca. 114 years) greenhouse
on a
molecular basis. Enhanced through feeding of crops with
gas with a global warming potential 298 times that of CO
2
1
Figure 1. Reactivity and binding of nitrosyl ligands at transition
metal sites.
2
nitrogen-rich fertilizers, global emission of N
2
O is mainly
attributed to the microbial and fungal denitrification processes
mediated by metalloenzymes. The most critical step for N O
2
We hypothesize that the presence of spin density at the N atom
of a metal-nitrosyl [M]-NO, perhaps enhanced by the ability to
achieve a side-on [M]-NO conformation, may facilitate N-N bond
formation between a metal-nitrosyl and nitric oxide to give cis-
3
formation is N-N bond formation that occurs via the reductive
coupling of two nitric oxide (NO) molecules. This takes place at
4
2
2
diiron sites of nitric oxide reductase (NOR) enzymes as well as at
2 2
hyponitrites [M](κ -O N ) (Figure 1e). Access to side-on [M](η -
mononuclear sites in the iron-based cytochrome P450 nitric oxide
NO) complexes may both expose the N atom for N-N coupling
5
6
reductase (NOR) or copper nitrite reductase (CuNiR) enzymes
Figure 1a). Based on numerous theoretical studies, it seems likely
and initiate a M-O interaction prior to forming mononuclear
2
(
[M](κ -O
2
N
2
) complexes. Such side-on conformations are known
2-
10
13
that an intermediate hyponitrite species (N
2
O
2
) precedes N
release. For instance, coupling of two metal-nitrosyl [M]-NO
moieties takes place upon reduction of [(TpRuNO) (µ-Cl)(µ-
Pz)] to afford the N-N reductively coupled product (TpRu) (µ-
2
O
in the photoexcited states of {Ni(NO)} complexes where the
7
10
superscript in the Enemark-Feltham formulation {Ni(NO)}
1
4
2
represents the total number of metal d and NO π* electrons. The
side-on binding of a nitrosyl ligand (Figure 1c) in a mononuclear
synthetic complex, however, has not been observed in its ground
2
+
2
2
8
Cl)(µ-Pz){µ-κ -N(=O)N(=O)}. Reductive coupling of NO at
2
2
copper(I) complexes has led to dinuclear trans-hyponitrite
3 2 2 2
state. {[(Me Si) N] (THF)Y} (µ-η :η -NO) is a singular example
II
copper(II) complexes [Cu ]
2
(O
2
N
2
) that release N
2
O either upon
that possesses a side-on NO achieved via bridging between two
transition or rare earth metal centers that possesses a highly
9
10
acidification or thermal decay;
the later also produces
II
10
2-
15
[
[
Cu ](NO
2
)
via disproportionation.
phen)NiNO][PF
The nickel nitrosyl
reduced NO ligand. Crystallographic studies revealed side-on
2
(bipy)(Me
2
6
] mediates NO disproportionation in
O via a mononuclear cis-
). The factors that lead to N-N bond
formation at a monometallic site, however, have not been
η -NO binding in fully reduced bovine cytochrome c oxidase
1
6
17
the presence of NO and yields N
2
(CcO) and copper nitrite reductase (CuNiR) that feature
2
11
11
hyponitrite [Ni](κ -O
2
N
2
mononuclear {Cu(NO)} sites, though solution spectroscopic
studies suggest end-on binding.
side-on and end-on {Cu(NO)} species suggest that each
possesses a Cu (•NO) electronic formulation with a considerable
1
8,19
DFT calculations for both
1
2
11
explicitly documented.
I
20
ACS Paragon Plus Environment

Journal of the American Chemical Society
Page 2 of 5
2
24
amount of spin density at the nitrosyl N atom, reinforced by EPR
studies of the reduced {Cu(NO)} intermediate of CuNIR.
served in a related [Ni](η -ONPh) complex. The nitrosyl ligand
1
1
18,21
11
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
in the {Ni(NO)} species 2a (molecule 1: 1.270(6) Å; molecule
Furthermore, differential H-bonding and/or steric interactions
from second-sphere protein residues may play a vital role in the
determining the conformation of {Cu(NO)} species.
2: 1.284(6) Å) is significantly more activated than in the
1
0
{Ni(NO)} analogue 1 (1.1602(15) Å), despite N/O positional
1
1
21,22
15
disorder that likely underestimates the N-O distance. Disorder
models that allow pairs of N/O atoms to refine lead to slightly
longer N-O distances of 1.28 - 1.32 Å but with a wider spread of
Ni-N/O distances (Figures S23c and S23d). Thus, 2a possesses a
nitrosyl ligand with a N-O distance longer than in most metal-
To synthetically outline factors that control metal-nitrosyl
bonding modes and NO coupling reactivity, we targeted low
1
0/11
coordinate {M(NO)}
pairs that could accommodate both side-
on NO and cis-hyponitrite ligands (Figures 1d and 1e). The salt
2
5
2
2
nitrosyls
3 2 2 2
except {[(Me Si) N] (THF)Y} (µ-η :η -NO) which
metathesis reaction between equimolar amounts of the β-
1
5
i
also features a side-on NO ligand (N-O: 1.390(4)Å). Coordina-
tion of the potassium cation to both the nitrogen and oxygen at-
oms of the reduced nitrosyl ligand in the {[Ni](η -NO)} anion of
a gives K-N/O distances in the range 2.826(5) Å - 2.869(5) Å
diketiminato
(THF)
Ni(NO)} complex [ Pr
potassium
salt
[ Pr
2
NNF6]K(THF)
and
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
2
Ni(NO)I in tetrahydrofuran (THF) affords the diamagnetic
2
-
1
0
i
{
2
NNF6]NiNO (1) isolated as dark green
2
crystals in 76% yield (Figure 2a). The X-ray structure of 1 reveals
a trigonal-planar Ni center with an end-on nitrosyl ligand (Ni1-
N3-O1 = 174.47(11)°) with a N3-O1 distance of 1.1602(15) Å
…
that leads to Ni K separations of 4.417 Å (molecule 1) and 4.467
Å (molecule 2). The infrared spectra of two isotopologues 2a and
1
5
14
15
-1
(
Figure S22). The infrared spectrum of 1 indicates a nitrosyl
2a- N exhibit N/ N isotope sensitive bands at 894 cm and
-1
-1
878 cm , respectively. This is the lowest νNO reported for a
transition metal nitrosyl complex, lower than 951 cm in
[(Me
stretch (νNO) at 1825 cm , similar to values reported for other
three-coordinate neutral nickel-nitrosyl complexes (νNO =1817-
1
-
1
2
2
15
-1 23
{
3 2 2 2
Si) N] (THF)Y} (µ-η :η -NO).
779 cm ). Notably, the cyclic voltammogram of 1 in
tetrahydrofuran at room temperature exhibits reversible
a
More completely encapusulating the K+ cation changes the ni-
-
reduction wave centered at -1.89 V (vs ferrocenium/ferrocene),
trosyl bonding mode of the {[Ni](NO)} anion. Reduction of
10 11
i
attributed to the {Ni(NO)} / redox couple (Figure S6).
[
[
[
Pr
2
NNF6]NiNO (1) with KC
(1 equiv)
2
NNF6]Ni(µ-NO)K[2.2.2-cryptand] (2b) (Figures 2c, S24). By
8
(1.2 equiv) in the presence of
in tetrahydrofuran gives
1
0
2.2.2]-cryptand
One-electron reduction of the {Ni(NO)} complex 1 with
potassium-graphite (KC ) (1.2 equiv) in tetrahydrofuran in the
i
Pr
8
…
significantly lengthening the Ni K separation (5.466 Å), the ni-
trosyl ligand exhibits both linear (77%) and side-on (23%)
conformations in the solid state. The linear NO ligand (Ni1-N3A-
O1A, 165.8(3)°) is more highly reduced than of 1 with a N-O
distance of 1.198(4) Å. The minor side-on conformer exhibits
N/O positional disorder whose principle component possesses a
N-O distance of 1.274(19) Å similar to 2a. The IR spectrum of a
presence of 18-crown-6 (1 equiv) leads to a rapid color change
from green to purple (Figure 2a). Single crystal X-ray diffraction
analysis of the purple complex 2a reveals two independent
i
2
2
[
2
Pr NNF6]Ni(µ-η :η -NO)K(18-crown-6)(THF) moieties. Each
nickel exhibits square planar coordination that features a side-on
NO ligand between the Ni and K centers. Although disorder from
interchange of N/O positions precludes a detailed assessment of
metrical parameters, refinement of the NO ligand into a single
orientation (Figure 2b) gives short Ni-N (1.853(5) Å; 1.866(5) Å)
and Ni-O (1.839(5) Å; 1.868(5) Å) distances similar to those ob-
-1
-1
solid sample of 2b reveals an NO stretch at 1555 cm (1525 cm
1
5
for 2b- NO) that is consistent with a highly reduced linear NO
2
5
ligand (Figure S10).
The room temperature EPR spectrum of [ Pr
NO)K[18-crown-6](THF) (2a) in tetrahydrofuran indicates a S =
species with a giso value of 2.0008 very close to that of the free
electron (g = 2.0023). This three line spectrum of 2a is due to
strong coupling with the N nucleus of the bound NO ligand
i
2
2
2
NNF6]Ni(µ-η :η -
½
e
14
15
(
(
A
A
14N = 28.9 MHz) which shifts to a two line pattern for 2a- N
15N = 40.1 MHz) (Figures 3a and 3b). These data are very
2
-
similar to the highly reduced, radical NO
dianion in
2
2
15
{[(Me Si) N] (THF)Y} (µ-η :η -NO). In both THF solution and
3 2 2 2
frozen glass (20 K), EPR spectra of 2a and 2b are nearly indistin-
guishable (Figures S20 and S21). Modeling of the low T EPR
spectra of 2a was guided by DFT calculations and required the
use of two separate components, suggesting that THF solutions of
2
a and 2b may contain a mixture of side-on and linear nitrosyls.
Ni K-edge X-ray absorption spectroscopy (XAS) probes the Ni
oxidation state by exciting a Ni 1s electron to valence Ni 3d
orbitals (pre-edge, ~8330-8335 eV) and Ni 4p orbitals (edge,
Figure 3. (a, b) X-band EPR spectra (black trace) of 2a and 2a-
1
5
N in tetrahydrofuran at 293 K. Simulations (red trace) provide
1
4
15
g
iso = 2.0008, Aiso( N) = 28.9 MHz (for 2a), and Aiso( N) = 40.1
15
MHz (for 2a- N). (c) Ni K-edge X-ray absorption spectra of 1,
a, and 2b.
2
1
1
Figure 2. Synthesis (a) and X-ray structures (b,c) of {NiNO}
anions 2a (side-on) and 2b (77 / 23 end-on / side-on).
ACS Paragon Plus Environment

Page 3 of 5
Journal of the American Chemical Society
2
-
>
8345 eV) (Figure 3c). The pre-edge features of 1 (8332.1(0) eV),
{[Ni](κ -O
2
N
2
)} moiety that is coordinated to only one cis-
+
1
2
3
4
5
6
7
8
9
2a (8332.3(1) eV), and 2b (8332.3(0) eV) are at a similar energy
to the closely related Ni complex [ Pr
hyponitrite N atom by the {K[2.2.2-cryptand]} cation (K-N =
3.274 Å) (Figure S26). Capture of NO by a reduced NO ligand in
{[Ni](NO)} to form cis-hyponitrites {[Ni](κ -O N )} mirrors the
2 2
II
i
II
2
NNF6]Ni (µ-Br)
2 2
Li(THF) ,
2
4
-
2
-
(
8331.6 eV), suggesting that complexes 1, 2a, and 2b are best
II
i
2
described as Ni , with the slight shift to higher pre-edge energies
attributed to NO backbonding. Calculated TDDFT XAS assign
the rising edge feature in 2a and 2b at ~ 8335 eV is a Ni to ligand
π* transition that has much weaker intensity in 1 (Figure S38).
reactivity of NO with [ Pr NN ]Ni(η -ONPh) to form
2
F6
i
2
-
[
Pr
2
NNF6]Ni(η -O
2
N
2
Ph). In both anionic {[Ni](NO)} and neu-
2
tral [Ni](η -ONPh), there is significant unpaired electron density
at the reduced NO moiety. Notably, the {Ni(NO)} complex 1
does not react with nitric oxide.
2
4
10
1
0
These results suggest that reduction of {Ni(NO)} species 1 to
1
1
anionic {Ni(NO)} species 2a and 2b occurs primarily at the NO
ligand. Complexes 2a (side-on) and 2b (principally end-on) have
nearly identical XAS spectra and cannot be readily distinguished
by this technique.
i
2
NMR spectra of {[ Pr
in THF-d exhibits sharp resonances characteristic of diamagnetic
β-diketiminato Ni complexes (Figures S12-S14). Notably, the
2 2 2
NNF6]Ni(κ -O N )}K[18-crown-6] (3a)
8
II
24
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
15
15
15 15
N NMR spectrum of a N enriched sample of 3a (3a- N N) in
THF-d shows a sharp singlet at 244.7 ppm (vs. liquid NH ) indi-
cating symmetric κ -O,O binding of the hyponitrite ligand to the
DFT calculations (Supporting Information) provide insight into
electronic structure of the NO complexes and the secondary
sphere interactions that control the NO bonding mode. DFT
geometry optimizations of 1 and 2a and 2b without counterions
using the ORCA program (B3LYP, TZVP/SV(P)) reveal spin
density at the NO ligand in the 2a side-on (1.25 e ) and 2b end-on
conformations (1.52 e ) that are almost identical in energy. Similar
to TpNiNO with a linear NO ligand, complex 1 is best described
as high spin Ni(II) antiferromagnetically coupled to NO while
the anionic complexes 2a and 2b are low spin Ni(II) with an NO
ligand (Figures S33 and S35). Full molecule calculations could
energetically distinguish the end-on and side on conformations by
fixing the Ni-K distance to 5.466 Å. This revealed the side-on
conformation to be only 2.3 kcal/mol more stable, consistent with
the linear / side-on disordered observed in the solid state structure
of 2b.
8
3
2
i
[
2
Pr NNF6]Ni core in solution at room temperature. The
[ Pr NNF6]Ni(κ -O N )} anion in 3b exhibits identical NMR
2 2 2
features as found in 3a.
i
2
-
{
2
6
-
-
Hyponitrite complexes are known to release N O upon heating
2
9,10,12
i
2
-
2
7
or protonation.
3b) is thermally stable up to 60 °C with no evidence of N
Protonation of 3a or 3b by 1 equiv. trifluoroacetic acid, however,
The {[ Pr
2
NNF6]Ni(κ -O
2
N
2
)} anion (in 3a or
1
-
2
O loss.
2
-
15
triggers the instantaneous release of N
Figures 4c and S17) and IR spectroscopy (2227 cm ) (Figure
S16). Protonation with HBF •OEt produces N O in 76% yield
and allows for isolation of the nickel(II) hydroxide
2
O observed by N NMR
-1
(
4
2
2
i
dimer{[ Pr
2 2 2
NNF6]Ni} (µ-OH) (4) in 66% yield that exhibits a
II
structure similar to other β-diketiminato [Ni ]
Figure S27).
Spectroscopic and computational insights reveal that one-
electron reduction of the {Ni(NO)} complex 1 largely takes
place at the NO ligand, leading to side-on and end-on {Ni(NO)}
species 2a and 2b, respectively. Regardless of the nitrosyl binding
mode, these {Ni(NO)} complexes possess a significant amount
of unpaired electron density at the nitrosyl N atom and undergo
2
2
(µ-OH) complexes
2
8
(
The reduced NO ligands that bear significant unpaired electron
density in 2a and 2b are primed for coupling with •NO to form
cis-hyponitrite ligands in complexes {[Ni](κ -O
1
0
2
-
2 2
N )} (3a and
1
1
3
b). Addition of 1 equiv NO(g) to 2a in tetrahydrofuran at room
i
2
temperature affords diamagnetic {[ Pr
crown-6) (3a) in 72% yield (Figure 4a). X-ray diffraction analysis
of 3a reveals a square planar Ni center with short Ni-N
1.8895(15), 1.8936(15) Å and Ni-O 1.8241(13), 1.8187(13) Å)
distances clearly indicating coupling between the two NO ligands
2
NNF6]Ni(κ -O
2
N
2
)}K(18-
11
β
-dik
2
facile coupling with NO to give the cis-hyponitrite {[Ni](κ -
-
O
2
N
2
)} which releases N
2
O upon protonation. Controlled tuning
of the second coordination sphere interactions between the
nitrosyl ligand of the {Ni(NO)} anion and a potassium cation
modifies the metal-nitrosyl bonding mode, favoring side-on
(
N3-N4 = 1.235(2) Å) (Figures 4b, S24). The cis-hyponitrite
ligand exhibits an otherwise symmetric structure (O1-N3 =
.370(2), O2-N4 = 1.367(2) Å) similar to those previously
1
1
1
2
…
12
[M](η -NO) at shorter Ni K distances. Especially since the
observed despite unsymmetrical coordination of {K[18-crown-
6]} cation to both the N atoms of the hyponitrite ligand (K1-N4,
2.7519(17), K1-N3, 3.0584(18) Å). Addition of NO to 2b
similarly provides {[ Pr
1
0
+
corresponding {Ni(NO)} species does not react with NO, these
findings underscore electronic and conformational factors that
favor NO coupling via N-N bond formation at monometallic sites.
Separation of NO-based reduction and NO coupling steps pro-
vides important context for the biologically important reduction of
i
2
2 2 2
NNF6]Ni(κ -O N )}K[2.2.2-cryptand]
(
3b) in 89% yield with very similar metrical parameters for the
NO that results in N
2
O formation via protonation of cis-
hyponitrite intermediates.
ASSOCIATED CONTENT
Supporting Information. This material is available free of charge via
the Internet at http://pubs.acs.org.
Experimental, characterization, and computational details (PDF)
X-ray crystallographic data of 1, 2a, 2b, 3a, 3b, and 4 (CIF).
AUTHOR INFORMATION
Corresponding Authors
thw@georgetown.edu (T.H.W.); sestieber@cpp.edu (S.C.E.S)
Figure 4. (a) Formation of cis-hyponitrite intermediate 3a and its
ACKNOWLEDGMENT
transformation to nitrous oxide. (b) X-ray crystal structure of 3a.
1
5
(c) Comparison of N NMR spectra (41 MHz, 298 K,
T.H.W. acknowledges the NSF (CHE-1459090), the NIH
(R01GM126205), and the Georgetown Environment Initiative.
S.C.E.S. acknowledges the CPP College of Science, a CSUPERB
2
15
15 15
tetrahydrofuran-d
blue trace) and the crude reaction mixture (red trace) obtained
upon addition of 1 equiv trifluoroacetic acid to a solution of 3a-
8 2 2
) of [Ni](κ -O N )K[18-crown-6] (3a- N N)
(
1
5
15
8
N N in tetrahydrofuran-d .
ACS Paragon Plus Environment

Journal of the American Chemical Society
Page 4 of 5
New Investigator Grant, and NSF XSEDE (CHE160059). S.A.K.
(14) Enemark, J. H.; Feltham, R. D. Principles of Structure, Bond-
ing, and Reactivity for Metal Nitrosyl Complexes. Coord.
Chem. Rev. 1974, 13, 339–406.
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
acknowledges the Heavy Element Chemistry Program by the
Division of Chemical Sciences, Geosciences, and Biosciences,
Office of Basic Energy Sciences (BES), U.S. Department of En-
ergy, and Seaborg Institute Postdoctoral Fellowship (S.C.E.S.).
LANL is operated by Los Alamos National Security, LLC, for the
National Nuclear Security Administration of U.S. DOE (DE-
AC52-06NA25396). Use of Stanford Synchrotron Radiation Light
source, SLAC National Accelerator Laboratory, supported by
DOE, Office of Science, BES (DE-AC02-76SF00515).
(
15) Evans, W. J.; Fang, M.; Bates, J. E.; Furche, F.; Ziller, J. W.;
Kiesz, M. D.; Zink, J. I. Isolation of a radical dianion of nitro-
2-
gen oxide (NO) . Nat. Chem. 2010, 2, 644–647.
(16) Ohta, K.; Muramoto, K.; Shinzawa-Itoh, K.; Yamashita, E.;
Yoshikawa, S.; Tsukihara, T. X-Ray Structure of the NO-
Bound CuB in Bovine Cytochrome c Oxidase. Acta Crystal-
logr. Sect. F. 2010, 66, 251–253.
(
17) Tocheva, E. I.; Rosell, F. I.; Mauk, A. G.; Murphy, M. E. P.
Side-on Copper-Nitrosyl Coordination by Nitrite Reductase.
Science 2004, 304, 867–870.
REFERENCES
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
(
(
(
1)
2)
3)
Ravishankara, A. R.; Daniel, J. S.; Portmann, R. W. Nitrous
Oxide (N O): The Dominant Ozone-Depleting Substance Emit-
ted in the 21st Century. Science 2009, 326, 123–125.
Reay, D. S.; Davidson, E. A.; Smith, K. A.; Smith, P.; Melillo,
J. M.; Dentener, F.; Crutzen, P. J. Global agriculture and ni-
trous oxide emissions. Nat. Clim. Change 2012, 2, 410–416.
Thomson, A. J.; Giannopoulos, G.; Pretty, J.; Baggs, E. M.;
Richardson, D. J. Biological sources and sinks of nitrous oxide
and strategies to mitigate emissions. Phil. Trans. R. Soc. B
2012, 367, 1157–1168.
(18) Usov, O. M.; Sun, Y.; Grigoryants, V. M.; Shapleigh, J. P.;
Scholes, C. P. EPR-ENDOR of the Cu(I)NO Complex of Nitrite
Reductase. J. Am. Chem. Soc. 2006, 128, 13102–13111.
(19) Fujisawa, K.; Tateda, A.; Miyashita, Y.; Okamoto, K.; Paulat,
F.; Praneeth, V. K. K.; Merkle, A.; Lehnert, N. Structural and
Spectroscopic Characterization of Mononuclear copper(I)
Nitrosyl Complexes: End-on versus Side-on Coordination of
NO to copper(I). J. Am. Chem. Soc. 2008, 130, 1205–1213.
(20) Wasbotten, I. H.; Ghosh. A. Modeling Side-on NO
2
Coordination to Type
2 Copper in Nitrite Reductase:
(4)
Shiro, Y.; Sugimoto, H.; Tosha, T.; Nagano, S.; Hino, T.
Structural Basis for Nitrous Oxide Generation by Bacterial
Nitric Oxide Reductases. Phil. Trans. R. Soc. B 2012, 367,
Structures, Energetics, and Bonding. J. Am. Chem. Soc. 2005,
127, 15384-15385.
(21) Ghosh, S.; Dey, A.; Usov, O. M.; Sun, Y.; Grigoryants, V. M.;
Scholes, C. P.; Solomon, E. I. Resolution of the Spectroscopy
versus Crystallography Issue for NO Intermediates of Nitrite
Reductase from Rhodobacter Sphaeroides. J. Am. Chem. Soc.
2007, 129, 10310–10311.
(22) Merkle, A. C.; Lehnert, N. The Side-on copper(I) Nitrosyl
Geometry in Copper Nitrite Reductase Is due to Steric
Interactions with Isoleucine-257. Inorg. Chem. 2009, 48,
11504–11506.
(23) Puiu, S. C.; Warren, T. H. Three-Coordinate-Diketiminato
Nickel Nitrosyl Complexes from Nickel(I)-Lutidine and
Nickel(II) - Alkyl Precursors. Organometallics 2003, 22 3974–
3976.
(24) Kundu, S.; Stieber, S. C. E.; Ferrier, M. G.; Kozimor, S. A.;
Bertke, J. A.; Warren, T. H. Redox Non-Innocence of
Nitrosobenzene at Nickel. Angew. Chem. Int. Ed. 2016, 55,
10321–10325.
1
195–1203.
(
(
(
5)
6)
7)
McQuarters, A. B.; Wirgau, N. E.; Lehnert, N. Model
Complexes of Key Intermediates in Fungal Cytochrome P450
Nitric Oxide Reductase (P450nor). Curr. Opin. Chem. Biol.
2
014, 19, 82–89.
Merkle, A. C.; Lehnert, N. Binding and Activation of Nitrite
and Nitric Oxide by Copper Nitrite Reductase and
Corresponding Model Complexes. Dalton Trans. 2012, 41,
3355–3368.
(a) Blomberg, M. R. A.; Siegbahn, P. E. M. Mechanism for
N
2
O Generation in Bacterial Nitric Oxide Reductase: A Quan-
tum Chemical Study. Biochemistry 2012, 51, 5173-5186. (b)
Metz, S. N O Formation via Reductive Disproportionation of
2
NO by Mononuclear Copper Complexes: A Mechanistic DFT
Study. Inorg. Chem. 2017, 56, 3820-3833. (c) Suzuki, T.;
Tanaka, H.; Shiota, Y.; Sajith, P. K.; Arikawa, Y.; Yoshizawa,
K. Proton-Assisted Mechanism of NO Reduction on
a
(25) (a) Hayton, T. W.; Legzdins, P.; Sharp, W. B. Coordination and
Organometallic Chemistry of Metal-NO Complexes. Chem.
Rev. 2002, 102, 935-991. (b) Böhmer, J.; Haselhorst, G.;
Wieghardt, K.; Nuber, B. The First Mononuclear
Dinuclear Ruthenium Complex. Inorg. Chem. 2015, 54, 7181–
7191.
(
8)
Arikawa, Y.; Asayama, T.; Moriguchi, Y.; Agari, S.; Onishi,
M. Reversible N-N Coupling of NO Ligands on Dinuclear Ru-
Nitrosyl(oxo)molybdenum Complex: Side-On Bonded and µ
3
-
2
thenium Complexes and Subsequent N O Evolution: Relevance
to Nitric Oxide Reductase. J. Am. Chem. Soc. 2007, 129,
14160–14161.
bridging NO Ligands in [{MoL(NO)(O)(OH)} NaPF •H O.
2
6
2
Angew. Chem. Int. Ed. 1994, 20, 1473–1476.
(26) Neese, F. Orca: an ab initio, DFT and Semiempirical Electronic
Structure Package, Version 3.0.3; Max Planck Institute for
Chemical Energy Conversion; Mülheim an der Ruhr, Germany.
(27) (a) Tomson, N. C.; Crimmin, M. R.; Petrenko, T.; Rosebrugh,
L. E.; Sproules, S.; Boyd, W. C.; Bergman, R. G.; Debeer, S.;
Toste, F. D.; Wieghardt, K. A Step Beyond the Feltham-
Enenark Notation: Spectroscopic and Correlated ab Initio
Computational Support for an Antiferromagnetically Coupled
(9)
Lionetti, D.; de Ruiter, G.; Agapie, T. A Trans-Hyponitrite
Intermediate in the Reductive Coupling and Deoxygenation of
Nitric Oxide by a Tricopper-Lewis Acid Complex. J. Am.
Chem. Soc. 2016, 138, 5008-5011.
(
10) Wijeratne, G. B.; Hematian, S.; Siegler, M. A.; Karlin, K. D.
Copper(I)/NO(g)Reductive Coupling Producing Trans-
a
Hyponitrite Bridged Dicopper(II) Complex: Redox Reversal
Giving Copper(I)/NO(g)Disproportionation. J. Am. Chem. Soc.
-
M(II)-(NO) Description of Tp*M(NO)(M = Co, Ni). J. Am.
2
017, 139, 13276–13279.
11) Wright, A. M.; Zaman, H. T.; Wu, G.; Hayton, T. W. Mecha-
nistic Insights into the Formation of N O by a Nickel Nitrosyl
Complex. Inorg. Chem. 2014, 53, 3108–3116.
12) (a) Wright, A. M.; Hayton, T. W. Understanding the Role of
Hyponitrite in Nitric Oxide Reduction. Inorg. Chem. 2015, 54,
Chem. Soc. 2011, 133, 18785-18801. (b) Soma, S.; Van Stap-
pen, C.; Kiss, M.; Szilagyi, R. K.; Lehnert, M.; Fujisawa, K.
Distorted tetrahedral nickel-nitrosyl complexes: spectroscopic
characterization and electronic structure. J. Biol. Inorg. Chem.
2016, 21, 757-775.
(
(
2
(28) Yao, S.; Bill, E.; Milsmann, C.; Wieghardt, K.; Driess, M. A
9
330–9341. (b) Arikawa, Y.; Onishi, M. Reductive N-N Cou-
pling of NO Molecules on Transition Metal Complexes Lead-
ing to N O. Coord. Chem. Rev. 2012, 256, 468–478.
“side-On” superoxonickel Complex [LNi(O )] with a Square-
2
Planar Tetracoordinate Nickel(II) Center and Its Conversion in-
2
to [LNi(µ-OH) NiL]. Angew. Chem. Int. Ed. 2008, 47, 7110–
2
(
13) Fomitchev, D. V.; Furlani, T. R.; Coppens, P. Combined X-
7113.
5
Ray Diffraction and Density Functional Study of [Ni(NO)(η -
Cp*)] in the Ground and Light-Induced Metastable States. In-
org. Chem. 1998, 37, 1519–1526.
ACS Paragon Plus Environment

Page 5 of 5
Journal of the American Chemical Society
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
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
5
ACS Paragon Plus Environment