Not Limited to Iron: A Cobalt Heme–NO Model Facilitates N–N Coupling with External NO in the Presence of a Lewis Acid to Generate N2O

Article abstract of DOI:10.1002/anie.201909137

Some bacterial heme proteins catalyze the coupling of two NO molecules to generate N₂O. We previously reported that a heme Fe–NO model engages in this N?N bond-forming reaction with NO. We now demonstrate that (OEP)Co^II(NO) similarly reacts with 1 equiv of NO in the presence of the Lewis acids BX₃ (X=F, C₆F₅) to generate N₂O. DFT calculations support retention of the Co^II oxidation state for the experimentally observed adduct (OEP)Co^II(NO?BF₃), the presumed hyponitrite intermediate (P^.+)Co^II(ONNO?BF₃), and the porphyrin π-radical cation by-product of this reaction, and that the π-radical cation formation likely occurs at the hyponitrite stage. In contrast, the Fe analogue undergoes a ferrous-to-ferric oxidation state conversion during this reaction. Our work shows that cobalt hemes are chemically competent to engage in the NO-to-N₂O conversion reaction.

Full text of DOI:10.1002/anie.201909137

A Journal of the Gesellschaft Deutscher Chemiker
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International Edition
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Accepted Article
Title: Not limited to Iron: A Cobalt Heme–NO Model Facilitates N–N
Coupling with External NO in the Presence of a Lewis Acid to
Generate N2O
Authors: Erwin G Abucayon, Rahul Khade, Douglas R. Powell, Yong
Zhang, and George B. Richter-Addo
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To be cited as: Angew. Chem. Int. Ed. 10.1002/anie.201909137
Angew. Chem. 10.1002/ange.201909137
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10.1002/anie.201909137
Angewandte Chemie International Edition
RESEARCH ARTICLE
Not limited to Iron: A Cobalt Heme–NO Model Facilitates N–N
Coupling with External NO in the Presence of a Lewis Acid to
Generate N2O
Erwin G. Abucayon,[a] Rahul L. Khade,[b] Douglas R. Powell,[a] Yong Zhang,*[b] and George B. Richter-
Addo*[a]
Abstract: Some bacterial heme proteins catalyze the coupling of
two NO molecules to generate N2O. We previously reported that a
heme Fe–NO model engages in this N–N bond-forming reaction with
NO. We now demonstrate that (OEP)CoII(NO) similarly reacts with 1
equiv. of NO in the presence of the Lewis acids BX3 (X = F, C6F5) to
generate N2O. DFT calculations support retention of the CoII
oxidation state for the experimentally observed adduct
(OEP)CoII(NO•BF3), the presumed hyponitrite intermediate
(por)Co(NO)-containing adduct with proximal His dissociation
from the metal center.[6-7] NO adducts of cobalt-reconstituted
heme proteins such as Mb and Hb have also been reported,[8-9]
as has the NO adduct of vitamin B12.[10-11]
There is intense interest in the N–N bond-forming reaction
where two NO molecules couple, in the presence of a biological
heme cofactor, to generate the greenhouse gas N2O, as this
reaction is
a critical component of, and of fundamental
+
II
•
(P )Co (ONNO•BX3), and the porphyrin π-radical cation by-product
of this reaction, and that the π-radical cation formation likely occurs
at the hyponitrite stage. In contrast, the Fe analogue undergoes a
ferrous-to-ferric oxidation state conversion during this reaction. Our
work shows, for the first time, that cobalt hemes are chemically
competent to engage in the NO-to-N2O conversion reaction.
importance to, the global N-cycle. Bacterial NO reductase
(bacNOR) enzymes utilize a bimetallic heme/non-heme active
site to perform this 2NO→N2O reaction.[12-13] We recently
reported that the five-coordinate heme model (OEP)Fe(NO)
engages in an N–N coupling reaction with external NO in the
presence of a boron-containing Lewis acid (BX3; X = F or C6F5)
to generate N2O.[14] In this reaction, the BX3 served to polarize
the ferrous nitrosyl moiety to possess substantial ferric nitroxyl
character (eq. 1), thus rendering it susceptible to attack by
another NO molecule. In effect, this observation lent chemical
Introduction
Cobalt-containing proteins are prevalent in biology,[1] and in
these proteins, the Co center may be part of a porphyrin-like
prosthetic group. While much attention has been focused on
vitamin B12 containing a corrin ring, other naturally occurring Co
proteins have been reported whose prosthetic groups resemble
porphyrins rather than corrins. For example, a Co porphyrin-like
enzyme, a fatty aldehyde decarboxylase, has been isolated from
the colonal alga Botyrococcus braunii.[2] Other Co porphyrins
have been isolated from the gram-negative anaerobic sulfate
reducing bacterium Desulfovibrio gigas[3] and from D.
desulfuricans.[4] However, Battersby and Sheng have shown,
using UV-vis spectroscopy, that the latter cobalt porphyrins are
better described as CoIII-isobacteriochlorins.[5]
Importantly, substitution of Co for Fe in heme proteins and
in heme model compounds has provided useful information
regarding the function of natural heme proteins, especially in
their reactions with the signaling agent and vasodilator nitric
oxide (NO). For example, substitution of Co for Fe in the
reconstituted bona fide NO receptor soluble guanylyl cylase
(sGC) results in a higher activation of the enzyme by NO,
consistent with the ready formation of the five-coordinate
II
III
....
NO
+ LA
LA
Fe
Fe
NO
ferric nitroxyl
anion character
ferrous
nitrosyl
(1)
support for the viability of the proposed bacNOR cis:b3
mechanism for the N–N bond formation step of N2O
generation,[15-17] where the non-heme Fe in the di-Fe heme/non-
heme active site could, in principle, serve as an appropriately
positioned Lewis acid to "activate" the heme-NO fragment
towards attack by a second NO molecule. We then sought to
probe whether the related (por)Co(NO) fragment is chemically
competent to engage in this N–N coupling reaction with external
NO to generate N2O, or whether this reaction was unique to
heme Fe. In this communication, we show that N2O is indeed
generated from the reaction of (OEP)Co(NO) with external NO in
the presence of the Lewis acid BX3.
Results and Discussion
Reaction of (OEP)Co(NO) in CH2Cl2 at 0 °C with NO (in the
absence of an added Lewis acid) for 1 h, with subsequent
warming of the reaction mixture to room temperature for an
additional 2 h period, does not result in N2O formation as judged
by IR spectroscopy of the reaction headspace (not shown). The
analogous reaction with labeled 15NO (in excess), however,
reveals that an NO exchange reaction occurs (eq 2 and Fig. S1),
[a]
[b]
E. G. Abucayon, D. R. Powell, G. B. Richter-Addo
Price Family Foundation of Structural Biology
Department of Chemistry and Biochemistry
University of Oklahoma, Norman, OK 73019
E-mail: grichteraddo@ou.edu
R. L. Khade, Y. Zhang
Department of Chemistry and Chemical Biology
Stevens Institute of Technology
(OEP)Co(NO) + xs. 15NO → (OEP)Co(15NO) + NO
(2)
Castle Point on Hudson, Hoboken, NJ 07030
E-mail: yong.zhang@stevens.edu
similar to that previously observed with the Fe analog,[14] to give
(OEP)Co(15NO) (υNO 1645 cm-1 (KBr), ΔυNO –30 cm-1; Fig. S1).[18]
Supporting information for this article is given via a link at the end of
the document.
This article is protected by copyright. All rights reserved.

10.1002/anie.201909137
Angewandte Chemie International Edition
RESEARCH ARTICLE
We then examined the effect of the Lewis acid on the Co–
NO moiety in the absence of added NO. Addition of ~2 equiv. of
BF3•OEt2 to (OEP)Co(NO) in CH2Cl2 (υNO 1672 cm-1) at –45 °C
for 30 min resulted in the appearance of a new low-intensity
band in the IR spectrum at 1632 cm-1 (i.e., ΔυNO –40 cm-1; calcd.
ΔυNO –28 cm-1, see later) in addition to the starting 1672 cm-1
band; this new band shifted to 1607 cm-1 when (OEP)Co(15NO)
in energy. The associated ΔυNO of –28 cm-1 for the lowest
•
energy N-II-1 state of 1-NO BF3 correlates well with the
experimental value of –40 cm-1 for the (OEP)Co(NO BF3) adduct.
•
(υ15
1641 cm-1) was used in the reaction (Fig. 1, right). We
NO
assign this new band at 1632 cm-1 to the υNO of the
•
(OEP)Co(NO BF3) adduct.
•
Figure 1. IR spectra from the reaction of (OEP)Co(NO) with BF3 OEt2 in CH2Cl2
-1
at –45 °C. (Left) IR spectra of the starting (OEP)Co(NO) (υNO 1672 cm ) and
15
-1
•
(OEP)Co( NO) (υNO 1641 cm ). (Right) IR spectra after addition of BF3 OEt2 to
15
Figure 2. Calculated geometries (in Å and deg) and selected NPA charges (in e
units) of the optimized precursor (P)Co(NO) (1-NO) and products from its
reactions with NO and/or BF3. Bond distances are in italics-underline, and
atomic charges are in regular font. The atomic charges and spin densities (in e
units) for the Co and P units are shown below the structures.
(OEP)Co(NO) (solid line trace) and (OEP)Co( NO) (dashed line trace); the
14/15
•
assigned υNO bands for the (OEP)Co(
NO BF3) products are underlined. The
-1
low-intensity band at ~1700 cm is near-coincident with a similar weak band in
our BF3 Et2O/CH2Cl2 control solution (Fig. S2b) and in the final product after
•
addition of external NO (Fig. S3).
...
•
The calculated long O B distance of 2.726 Å in 1-NO BF3 and
Density functional theory (DFT) calculations were employed
to probe possible spin state interaction patterns for the starting
near-planarity of the BF3 moiety (top right of Fig. 2) point to a
weak CoNO BF3 interaction in this adduct. Importantly, no N2O
...
neutral (P)Co(NO) compound (1-NO;
P
=
unsubstituted
formation was detected in the headspace of the
"(OEP)Co(NO)/BF3" reaction in the absence of added NO (Fig. 3,
top).
porphinato dianion) and other species mentioned in this work
(see Tables 1 and S2).[19] In a typical (P)Co(NO) system,
valence electrons can be distributed between the metal center
(e.g., Co2+ or Co3+), the porphyrin (e.g., P2– or P– (π cation)) or
the NO ligand (NO, NO+, or NO–) (Fig. S14). The allowable
combinations of these options, including additional options for
spin-state variations, were studied for such systems in Table 1
(see SI for details). For 1-NO (S = 0), both open-shell and closed
shell singlet states with, respectively, Co2+ and Co3+ were
studied and successfully optimized. 1-NO is best described as a
Interestingly, however, when (OEP)Co(NO) was reacted with
•
NO (~1 equiv) at 0 °C in the presence of BF3 OEt2 (~2 equiv.) for
1 hr, and then at room temperature for an additional 2 hr, the
gas-phase IR spectrum of the headspace of the reaction mixture
revealed the formation of N2O in ~12% yield, together with
unreacted NO (middle of Fig. 3).[21-22] Sampling the headspace
of the reaction after 1 hr at 0 °C (or –45 °C) revealed N2O
(P2–)CoII(NO) species (N-II-1 in Table 1) with antiferromagnetic
formation in lower (3-5%) yields. The related reaction of 15N-
2+
•
coupling between Co (S = ½) and NO (S = –½), consistent with
15
•
labeled (OEP)Co( NO) with NO in the presence of BF3 OEt2
an earlier formulation.[20] The alternate N-III-1 state with CoIII (S
= 0) and NO– (S = 0) is calculated to be 6.02 kcal/mol higher in
energy.
generated an isotopic mixture of 14N2O, 14N15NO, 15N14NO and
15N2O (Fig. S4),[23] consistent with the exchange reaction shown
•
in eq 2. The use of excess NO (and excess BF3 OEt2) did not
result in an increased yield of N2O. As we reported previously,[14]
As BF3 is diamagnetic, the overall spin state of the 1-
•
•
BF3 OEt2 alone does not couple two molecules of NO to give
NO BF3 adduct is still singlet. However, we investigated
additional fragment spin states with both Co2+ and Co3+ as well
(Tables 1 and S4) to examine if there could be any differences in
electronic state due to interaction with BF3. The calculated
N2O under these reaction conditions (bottom of Fig. 3), nor does
(OEP)Co(NO) by itself as noted earlier.
The observed N2O generation necessitates consideration of
the crucial N–N bond formation step, which we probed by DFT
methods. We first considered the BF3-free NO-coupled
hypothetical product (P)Co(ONNO) (i.e., 2-(NO)2, bottom left of
Fig. 2). As (P)Co(NO) has S = 0 and NO has S = ½, the product
•
lowest energy formulation of the 1-NO BF3 adduct is the singlet
2–
II
•
(P )Co (NO BF3) retaining the N-II-1 spin state feature of 1-NO
with antiferromagnetic coupling between Co2+ and NO; the
alternate Co3+-based N-III-1 formulation is 4.38 kcal/mol higher
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10.1002/anie.201909137
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RESEARCH ARTICLE
Table 1. Selected Fragment Spin States Studied, and the Spin Densities and Relative Electronic Energies of the Optimized Geometries [a]
[d]
[e]
system[b]
Spin
0
State[c]
N-II-1
Co
P
axial (NO)n
NO (S = –½)
ρ
Co[d]
αβ
ρ
P [d]
αβ
ρ
NO [d]
αβ
ρ
N'O' [d]
αβ
ρ
BF3
αβ
ΔESCF
0.00
6.02
0.00
4.38
0.00
0.05
11.25
12.80
9.25
0.00
0.36
1.84
1.51
0.69
1.25
0.00
7.09
1-NO
Co2+ (S = ½)
Co3+ (S = 0)
Co2+ (S = ½)
Co3+ (S = 0)
Co2+ (S = ½)
Co3+ (S = 0)
Co3+ (S = 1)
P2– (S = 0)
P2– (S = 0)
P2– (S = 0)
P2– (S = 0)
P2– (S = 0)
P2– (S = 0)
P2– (S = 0)
0.895
0.000
0.876
0.000
0.899
–0.179
1.878
2.768
1.808
0.984
–0.956
–0.010
1.964
1.964
2.780
–0.900
0.014
–0.064
0.000
–0.067
0.000
–0.111
0.075
–0.071
1.147
–0.038
–1.005
1.000
0.035
–0.087
–0.051
1.163
1.056
0.989
–0.831
0.000
–0.802
0.000
0.056
0.722
–0.430
–0.561
0.824
0.041
0.000
0.036
0.039
0.095
–0.018
0.844
–0.003
0
N-III-1
NO– (S = 0)
•
1-NO BF3
0
N-II-1
NO (S = –½)
NO– (S = 0)
–0.067
0
N-III-1
0.000
2-(NO)2
½
NN-II-4
NN-III-1
NN-III-2
NN-II-9
NN-III-3
NN-II-6
NN-II-7
NN-III-1
NN-III-2
NN-III-3
NN-II-9
C-II-1
(NO)2 (S = 0)
(NO)2– (S = ½)
(NO)2– (S = –½)
(NO)2– (S = –½)
(NO)2– (S = ½)
(NO)2– (S = ½)
(NO)2– (S = ½)
(NO)2– (S = ½)
(NO)2– (S = –½)
(NO)2– (S = ½)
(NO)2– (S = –½)
NO (S = ½)
0.156
0.381
-0.378
-0.354
0.406
0.980
0.948
0.932
–0.911
0.990
–0.923
½
½
3/2
3/2
½
Co2+ (S = 3/2) P– (S = ½)
Co3+ (S = 1)
Co2+ (S = ½)
P2– (S = 0)
P– (S = –½)
•
2-(NO)2 BF3
0.001
0.008
0.006
–0.006
0.002
–0.003
½
Co2+ (S = –½) P– (S = ½)
½
Co3+ (S = 0)
Co3+ (S = 1)
Co3+ (S = 1)
P2– (S = 0)
P2– (S = 0)
P2– (S = 0)
½
3/2
3/2
½
Co2+ (S = 3/2) P– (S = ½)
Co2+ (S = –½) P– (S = ½)
[1-NO]+
½
C-III-1
Co3+ (S = 0)
P– (S = ½)
NO– (S = 0)
•
[a] See SI for full listing of spin states studied. [b] 2-(NO)2 = (P)Co(ONN'O'), and 2-(NO)2 BF3 = (P)Co(ONN'O').BF3, where the distal (i.e., added/second) NO
group is labeled N'O'. [c] A single "N" represents a mono-NO system; "NN" represents NO-coupling products, and "C" represents the cation. The "II" and "III" refer
to the Co oxidation states. [d] in e units. [e] kcal/mol.
hence we also investigated the overall intermediate-spin state
for 2-(NO)2. The lowest energy state (see more detailed
discussion of the studied spin states in the Supporting
Information) was determined to be NN-II-4 with the radical
feature concentrated on the Co center, with Co2+ (S = ½), P2– (S
= 0), and ONNO (S = 0), in essence retaining the N-II-1 spin
feature of 1-NO. Although this NN-II-4 state is only slightly more
favorable (by 0.05 kcal/mol) than NN-III-1 at the electronic level,
its Gibbs free energy is more stable by 2.17 kcal/mol.
...
Importantly, the calculated long N N distance of 1.832 Å in the
NN-II-4 state of 2-(NO)2 (Fig. 2 and Table S8) is suggestive of a
weak interaction and is consistent with our observation that no
N2O was formed under our experimental conditions.
•
Addition of NO (S = ½) to the bound NO in 1-NO BF3 (S = 0)
Figure 3. Gas phase infrared spectra of the headspace from the reaction of: (Top)
(OEP)Co(NO) with BF3•OEt2 showing no N2O formation. (Middle) (OEP)Co(NO)
•
likely yields the initial hyponitrite-like adduct 2-(NO)2 BF3, and
the coupling products with total spin S = ½ were investigated
with NO in the presence of BF3•OEt2 showing the formation of N2O (2237/2212
first. Of the several spin-state combinations considered for this
-1
cm ). (Bottom) BF3•OEt2 with NO showing no N2O formation. No NO2 gas (υNO
~
2
adduct (Tables
1
and S5), the Co2+-based states were
-1
1618 cm ) formed in these reactions in the absence of air.
determined to be more favorable than the Co3+-based states and
the states with total spin of S = 3/2 are of higher energies than
the most favorable S = ½ state (see more detailed discussion of
the studied spin states in the Supporting Information), which are
similar to the case of BF3-free 2-(NO)2 but with relatively smaller
with total spin state of ½ was studied first, with various fragment
spin state options and with both Co2+ and Co3+ centers (Tables 1
and S5). The recent theoretical study of Fe-based N–N coupling
showed a spin state change from low-spin to intermediate-spin,
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10.1002/anie.201909137
Angewandte Chemie International Edition
RESEARCH ARTICLE
+
•
energy differences. These results suggest an important role of
BF3 on NO coupling as described below. As a result, the lowest
energy state of 2-(NO)2.BF3 changes to the NN-II-6 state
the (OEP )Co(NO) π-radical cation product and those of the
neutral (OEP)Co(NO) are summarized in Figure 4 and Table S1.
–
possessing Co2+ (S = ½), P– (S = –½), and (NO)2 (S = –½)
characters, based on the calculated spin densities (Table 1).
•
The calculated structure and selected data for 2-(NO)2 BF3 in the
NN-II-6 state are shown at the bottom right of Fig. 2. The data
are reflective of the formation of both a porphine π-radical cation
and a hyponitrite (NO)2– radical bonded to a formally Co2+ center.
...
•
In this 2-(NO)2 BF3 structure, the O BF3 distance is significantly
•
reduced to 1.503 Å from 2.726 Å in 1-NO BF3, and the ON–NO
interaction becomes stronger with a bond distance of 1.237 Å
(from 1.832 Å in the BF3-free 2-(NO)2). Further, in 2-(NO)2, the
proximal NO (i.e., directly bonded to Co) charge of –0.013e and
the distal NO charge of +0.045e indicates a weak attraction for
•
NO coupling. However, in the case of 2-(NO)2 BF3, the Lewis
acid induces much larger opposite charges for the proximal NO
(–0.547e) and distal NO (+0.124e) moieties, significantly
enhancing their attraction to facilitate N–N bond formation.
•
These calculated features in 2-(NO)2 BF3 vs. 2-(NO)2 clearly
demonstrate the role of the Lewis acid BF3 in facilitating the
experimental NO coupling reaction with (OEP)Co(NO).
II
Figure 4. (Left) X-ray crystal structures of (left) (OEP)Co (NO) and (right) the
+
II
•
cation of [(OEP )Co (NO)][HO(B(C6F5)3)2] (CCDC 1939777). The bottom panels
The analogous reaction of (OEP)Co(NO) with 1 equiv. of NO
in the presence of the related Lewis acid B(C6F5)3 (2.2 equiv.)
also resulted in the generation of N2O in ~10% yield (Fig. S5).
The use of excess NO and B(C6F5)3 (10 equiv.) in this reaction
resulted in a higher yield of N2O (~22%). The use of excess NO
in this reaction allowed us, fortunately, to isolate the cobalt-
containing product in ~30% yield which we identified to be the
show the edge-on views of the π-π interactions and associated mean plane
separations (M.P.S.) and lateral shifts (L.S.).
Our DFT results for [(P)Co(NO)]+ ([1-NO]+; bottom of Table 1)
substantiated the relative stability of the Co2+ π-radical cation
31-34]
product over its Co3+-based analogues.[20,
The structural
model used for [1-NO]+ was based on the X-ray structure, with
several possible spin state interaction patterns examined
(Tables 1 and S2). For this [1-NO]+ (S = ½) product, both low-
spin Co2+ and Co3+ initial states were studied. We determined
that the π-radical cation state C-II-1 with antiferromagnetic
coupling between Co2+ and NO was ~7 kcal/mol lower in energy
than the Co3+-based C-III-1 valence isomer. We thus conclude
+
II
•
porphyrin
π-radical
cation
[(OEP )Co (NO)]-containing
derivative by its IR spectrum with a new band at 1715 cm-1
assigned to υNO (ΔυNO +45 cm-1; calcd. ΔυNO +58 cm-1) and a
new band at 1581 cm-1 assigned to the π-radical cation
macrocyle (Fig. S6).[24-27]
The identity of the Co-containing product was further
that
the
Co-containing
product
from
the
characterized
by
X-ray
crystallography
as
"(OEP)Co(NO)+NO+BX3" coupling reaction was indeed the π-
radical cation.
+
•
[(OEP )Co(NO)][HO(B(C6F5)3)2] whose crystal structure is
shown in Fig. 4 (right) and Fig. S8A-B. The ∠Co–N–O angle of
121.3(2)° for the major disordered nitrosyl O-atom (71%
occupancy) is similar to that of the neutral (OEP)Co(NO)
precursor (at 122.70(8)°),[28] consistent with the positive charge
being remote from the CoIINO moiety and the low ΔυNO of +45
cm-1 observed in the π-radical cation. Its identity as a π-radical
cation is further substantiated by the following observations: (i)
the porphyrin macrocycle is significantly distorted from planarity
(Fig. S8D) when compared with its neutral (OEP)Co(NO)[28]
precursor, (ii) the N–Cα and N–Cm bond lengths within the 16-
membered porphyrin core display alternating short-long
distances (Fig. S8E) characteristic of some (but not all)
porphyrin π-radical cations,[29] and (iii) adjacent porphyrin
macrocycles form an almost completely overlapping π-π dimer
(right of Fig. 4) with a mean plane separation (M.P.S.) and
lateral shift of 3.16 Å and 0.21 Å, respectively. These latter
The observation that (OEP)Co(NO) couples with external
NO in the presence of BF3 to generate N2O necessitates a
comparison with the previously reported Fe system.[14, 35] In this
regard, there are several interesting points to note. First, the
small ΔNO shift of –40 cm-1 observed in (OEP)Co(NO BF3) (c.f., –
•
247 cm-1 in the related (OEP)Fe(NO BF3)) is consistent with the
•
...
•
longer calculated NO BF3 distance of 2.726 Å in 1-NO BF3 vs.
1.675 Å in the Fe analog (left of Fig. 5). This weak interaction
allows the (P)Co(NO) unit to essentially retain its initial CoII
state; the calculated Co charge increases by only +0.138e upon
BF3 addition. In contrast, the relatively strong "NO-BF3"
interaction in the Fe analog induces electron density transfer to
the NO unit to give it ferric-nitroxyl (i.e., FeIII–NO–) character (the
calculated Fe charge increases by +0.650e upon BF3 addition).
•
Second, interactions of external NO with the (P)M(NO BF3) (M =
Co, Fe) adducts result in the presumed formation of hyponitrite
–
values are characteristic of "classical" porphyrin π-radical
(NO)2 radical anion intermediates, with formal oxidation of the
cations.[30] Further,
a
twist angle (∠(por)N–Co Co–N(por)
...
"(P)M" units as shown in the middle of Fig. 5. In the (P)Co case,
the calculated lowest energy structure is the one in which the
electron was removed from the porphine macrocycle while
torsion angle of 34°, Fig. S8C) of the π-π interacting dimers is
observed. Selected comparisons between the structural data of
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10.1002/anie.201909137
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retaining the low-spin CoII (S = ½) state, whereas for Fe, the
metal was oxidized to an intermediate-spin FeIII state. In 2-
report describes a 1-electron pathway by a heme/non-heme
engineered Mb (e.g., ZnII-FeBMb1) that was sufficient for NO
coupling and N2O generation.[46] A more in-depth analysis of the
reaction pathways, including assessment of transition states, is
needed to elucidate the complete mechanism of N2O formation
from this experimentally observed NO coupling reaction by Co
and Fe heme models facilitated by Lewis acids. We are pursuing
such studies and we will report the results in a future paper.
•
(NO)2 BF3, the proximal (i.e., the NO group directly bonded to
1.503
BF3
_
BF3
2.726
O
Co
O
N
N
O
O
N
N
1.237
II
Co
II
Co
II
Co
1-NO BF3
2-(NO)2 BF3
1.525
BF3
Acknowledgements
1.675
BF3
_
O
_
+
O
N
Fe
O
N
O
We are grateful to the U.S. National Science Foundation
(CHE-1566509 and CHE-1900181 to GBR-A) and the U.S.
National Institutes of Health (GM085774 to Y.Z.) for funding this
work, and to the NSF MRI program (CHE-1726630 to GBR-A)
for funds to purchase the X-ray diffractometer.
N
N
1.240
III
III
Fe
III
Fe
Fe
Figure 5. Comparison of key features in the NO coupling reaction for Co (top) and
Fe (bottom) starting from the respective (P)M (NO) (M = Co, Fe) precursors.
II
Co) and distal (i.e., the added NO group) have calculated
opposite charges of –0.547e and +0.124e, respectively (the Fe
values are, respectively, –0.539e and +0.146e), significantly
enhancing their attraction to facilitate the N–N bond formation
step. Third, the isolation of the final products, when excess NO
was used, displaying formal porphyrin oxidation for Co (i.e.,
Conflict of interest
The authors declare no conflict of interest
Keywords: cobalt • nitrogen oxides • density functional
+
II
•
(OEP )Co (NO)) vs. formal metal oxidation for Fe (i.e.,
[(OEP)FeIII(NO)]+) (shown on the right of Fig. 5) is consistent
with the calculated lowest energy structures for their respective
calculations • porphyrinoids • X-ray diffraction
[1]
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•
2-(NO)2 BF3 intermediates (middle of Fig. 5). Finally, the
•
determination that the weak interaction in (OEP)Co(NO BF3)
was sufficient to enable reaction with external NO is consistent
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In summary, we demonstrate for the first time that a cobalt-
containing heme model, (OEP)Co(NO), is chemically competent
to couple with external NO in a synergistic interaction with the
Lewis acids BX3 (X = F, C6F5) to generate the greenhouse gas
N2O. Our results thus show that this 2NO→N2O reaction is not
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(~12%) from the Co reaction with ~1 equiv. of NO were lower
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•
respective calculated 2-(NO)2 BF3 structures, contributes to a
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–
more favorable hyponitrite (NO)2 radical anion intermediate[40-45]
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•
that a relatively weak (P)M(NO LA) interaction can activate the
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10.1002/anie.201909137
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RESEARCH ARTICLE
6-311++G(2d,2p) for 1st shell atoms (atoms bonded to Co, NO, and
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+
•
[25] These data are close to those of the related [(OEP )Co(NO)]ClO4 (υNO
1700 cm-1 (Nujol), υOEP•+ 1560 cm-1).[27] The π-radical cation product
+
[(OEP )Co(NO)]BF3OH (υOH ~3525 cm-1 (KBr, br)) is kinetically
•
unstable, readily converting to the neutral (OEP)Co(NO) during
attempts to isolate it, with a total (OEP)Co(NO) recovery of 49–60%.
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•
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•
[35] The analogous reaction of (OEP)Fe(NO) with 2 equiv. of BF3 OEt2 and
1 equiv. of NO gave N2O in ~16% yield (based on Fe). This same
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previously.[14]
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–
[40] The free (NO)2 anion has been reported to be capable of decomposing
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A
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Entry for the Table of Contents
Layout 2:
RESEARCH ARTICLE
Erwin G. Abucayon, Rahul L. Khade,
Douglas R. Powell, Yong Zhang,* and
George B. Richter-Addo*
Page No. – Page No.
Not limited to Iron: A Cobalt Heme–
NO Model Facilitates N–N Coupling
with External NO in the Presence of a
Lewis Acid to Generate N2O
The biological conversion of NO to N2O is important to the global N-cycle. We show
that a cobalt heme model couples NO in the presence of a Lewis acid. DFT
calculations provide insight into the role of the Lewis acid in activating the bound
NO towards this N–N bond forming reaction.
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