Lewis Acid Activation of the Ferrous Heme-NO Fragment toward the N-N Coupling Reaction with NO to Generate N2O

Article abstract of DOI:10.1021/jacs.7b13681

Bacterial NO reductase (bacNOR) enzymes utilize a heme/non-heme active site to couple two NO molecules to N₂O. We show that BF₃ coordination to the nitrosyl O-atom in (OEP)Fe(NO) activates it toward N-N bond formation with NO to generate N₂O. ¹⁵N-isotopic labeling reveals a reversible nitrosyl exchange reaction and follow-up N-O bond cleavage in the N₂O formation step. Other Lewis acids (B(C₆F₅)₃ and K⁺) also promote the NO coupling reaction with (OEP)Fe(NO). These results, complemented by DFT calculations, provide experimental support for the cis:b₃ pathway in bacNOR.

Full text of DOI:10.1021/jacs.7b13681

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Lewis Acid Activation of the Ferrous Heme–NO Fragment
2
Towards the N–N Coupling Reaction with NO to Generate NO
Erwin G. Abucayon, Rahul L. Khade, Douglas R. Powell, Yong Zhang, and George B. Richter-Addo
J. Am. Chem. Soc., Just Accepted Manuscript • DOI: 10.1021/jacs.7b13681 • Publication Date (Web): 04 Mar 2018
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Lewis Acid Activation of the Ferrous Heme–NO Fragment Towards the
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Erwin G. Abucayon,† Rahul L. Khade,‡ Douglas R. Powell,† Yong Zhang,*,‡ and George B.
Richter-Addo*,†
†
Department of Chemistry and Biochemistry, University of Oklahoma, Norman, Oklahoma 73019, United States
‡ Department of Chemistry and Chemical Biology, Stevens Institute of Technology, Castle Point on Hudson, Ho-
boken, New Jersey 07030, United States.
Supporting Information Placeholder
mechanism, the second (external) NO molecule
attacks the heme-nitrosyl N
ABSTRACT: Bacterial NO reductase (bacNOR) en-
zymes utilize a heme-nonheme active site to couple
two NO molecules to N
2
O. We show that BF coor-
3
dination to the nitrosyl O-atom in (OEP)Fe(NO)
activates it towards N–N bond formation with NO
to generate N
versible nitrosyl exchange reaction and follow-up
N–O bond cleavage in the N O formation step.
Other Lewis acids (B(C
and K+) also promote
2
O. 15N-isotopic labeling reveals a re-
Figure 1. The three common proposed mechanisms for NO
2
coupling by bacterial NO reductases.
6
F5)3
atom to form the hyponitrite intermediate. In the
the NO coupling reaction with (OEP)Fe(NO). These
results, complemented by DFT calculations, pro-
trans mechanism, both active site Fe atoms first
bind one NO each prior to N
–N bond formation. In
vide experimental support for the cis:b mechanism
3
the cis:Fe mechanism, both NO molecules bind at
B
in bacNOR.
the non-heme Fe
B
site prior to the coupling reac-
tion.
The conversion of nitric oxide (NO) to the green-
house gas nitrous oxide (N O) is an important
component of the global N cycle.1 Elucidating the
N bond forming reaction between two NO mol-
ecules to generate N O remains one of the high im-
Detailed computational investigations on the
bacNOR active site by Blomberg are in support of
2
the cis:b
stabilized by an O atom interaction with the Fe
center.5-6 Definitive experimental evidence for this
cis:b mechanism is, however, lacking. Spectroscop-
3
pathway, where the heme-NO moiety is
N
–
B
2
pact research goals in NO bioinorganic chemistry.
Bacterial NO reductases (bacNOR) utilize a di-Fe
3
ic studies on heme models have suggested the trans
mechanism as a viable mechanism for NO coupling
by bacNOR.7 The operative mechanism for NO re-
duction by the di-Fe bacNOR enzyme is, however,
still under active debate.3,8-9 Importantly, outstand-
ing work by Lu8, 10 and Karlin11 on engineered my-
heme/non-heme active site (heme b
to couple two NO molecules to generate N
the -oxo (heme)Fe Fe that is reused in the re-
action cycle.2-3 X-ray crystal structures of bacNOR
enzymes are available,2-4 and provide a framework
for the elucidation of the NO coupling reaction.
3
:non-heme Fe
B
)
2
O and
ꢀ
–
O–
B
oglobins
and
on
synthetic
dinitrosyl
Three mechanisms for the NO coupling reaction
catalyzed by bacNOR have been proposed (Figure
(por)Fe(NO)
2
/CuI/acid systems, respectively, have
established the requirement for the second non-
heme metal to enable N O formation.
1), and all involve the formation of a new N
–N
2
bond and a hyponitrite intermediate. In the cis:b
3
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It is interesting to note that two of the three pro-
posed mechanisms for NO reduction by bacNOR
(the cis:b and trans mechanisms) involve the fer-
O atom.19-21 A smaller yet still significant negative
ꢁυNO shift of ~50 cm-1 has been documented for the
1
2
3
4
5
6
7
8
3
engineered mononitrosyl di-Fe myoglobin mutant,
rous (por)Fe(NO) fragment, whose participation is
central to both these mechanisms. Curiously, how-
ever, the (por)Fe(NO) compounds in isolation are
FeII-Fe Mb(NO).22
B
Table 1.
NO stretching frequencies (cm-1) for
(OEP)Fe(NO)•BF
rins.
3
and anionic {FeNO}8 iron porphy-
unreactive towards external NO for N O genera-
2
tion.11-14 We thus sought to probe experimental fac-
a
9
system
υ
NO
ꢁυNO
ref
tors that could activate the isolated (por)Fe(NO)
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(OEP)Fe(NO)
•
BF
3
1425 –241
1445 –228
1496 –185
~1450 –165
~1466 –218
1473 –214
t.w.
fragment towards N
–
N bond formation with exter-
O. In this article, we demon-
[(OEP)Fe(NO)]–
[(TPP)Fe(NO)]–
15
nal NO to generate N
2
16
17
18
18
[(TFPPBr
8
)Fe(NO)]–
strate experimentally, complemented by DFT calcu-
lations, that Lewis acid addition to a synthetic
(por)Fe(NO) compound activates the FeNO moiety
for engagement in a three-way synergistic reaction
[(3,5-Me-BAFP)Fe(NO)]–
[(To-F
PP)Fe(NO)]–
2
a
ꢁυNO with respect to the neutral {FeNO}7 precursors.
with external NO for the critical N
mation step to generate N O.
Addition of 2.5 equiv. of the Lewis acid BF
to an anaerobic CH Cl solution of (OEP)Fe(NO)
(υNO 1664 cm-1) at 0 °C results in a ~32
35% de-
–N bond for-
We then proceeded to evaluate the effect of the
Lewis acid addition on the reaction of
(OEP)Fe(NO) with external NO. When the 15N-
labeled (OEP)Fe(15NO) is reacted with 14NO in the
absence of Lewis acid, a nitrosyl exchange reaction
occurs (eq 1) as determined by IR spectroscopy,
consistent with an earlier report.23 Further,
2
3
•OEt
2
2
2
–
crease in υNO intensity and the appearance of a new
IR band at 1425 cm-1 (sh) that shifts to 1406 cm-1
when (OEP)Fe(15NO) is used (Figure 2). It is intri-
guing to note that the large
(OEP)Fe(15NO) + NO
(1)
(OEP)Fe(NO) + 15NO
and consistent with previous results for related
13-14
(por)Fe(NO) compounds,11,
we find that
(OEP)Fe(NO) does not react with NO to generate
O.12
When (OEP)Fe(NO) is reacted with NO in the
presence of BF OEt , however, we observed the
ready formation of the N N coupled product N
N
2
3
•
2
Figure 2. IR spectra showing the reduction in intensity of
the υNO band of the starting (OEP)Fe(NO) (υNO 1664 cm-1) in
–
2
O
(υN O 2237/2212 cm-1; Figure 3A top) in 55-63%
2
CH
the product mixture (as a NaCl plate) when (OEP)Fe(NO)
(solid line) is reacted with BF . The corresponding IR
2
Cl
2
upon reaction with BF
3
•Et
2
O. Inset: IR spectrum of
yields as determined by IR spectroscopy.24 When
15N-labeled (OEP)Fe(15NO) is reacted with unla-
3
•OEt
2
beled 14NO in the presence of BF
labeled 15N14NO and 14N15NO products form in
addition to 14N O and 15N O (Figure 3A bottom),25
due to the exchange process in eq. 1. In this reac-
tion, [(OEP)Fe(NO)]BF
OH (υNO 1839 cm-1) is iso-
3
•Et
2O, the mixed
spectrum for the (OEP)Fe(15NO) reaction is shown as a
dashed line. The new bands are obscured in the reaction
solvent (CH
2
Cl2) mixture.
2
2
υ
NO shift of
acid is added to the {FeNO}7 precursor
(OEP)Fe(NO) to form the (OEP)Fe(NO)•BF adduct
–
241 cm-1 that occurs when the Lewis
3
lated as the byproduct in 59-64% unoptimized iso-
lated yield.26
3
is similar to those observed for the 1-electron re-
duced {FeNO}8 anions (Table 1) whose υNOs are also
of weak-to-medium intensities.15-18 This large υNO
shift in (OEP)Fe(NO)•BF is suggestive of a signifi-
3
cant increase in backdonation of electron density
from the Fe center to the nitrosyl ligand as a result
of Lewis acid coordination to the terminal nitrosyl
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Journal of the American Chemical Society
in the precursor 1-NO. This helps explain the sig-
nificant lowering of the experimental υNO by 241
cm-1 (Table 1) upon BF
coordination to the FeNO
moiety in (OEP)Fe(NO)•BF
with substantial FeIII
and nitroxyl character (Tables S1 and S2). We note
that a related ꢁυNO of
228 cm-1 was observed for
the 1-electron reduced anion
{FeNO}8
[(OEP)Fe(NO)]– (as its K+(2.2.2) salt), whose N
1
2
3
4
5
6
7
8
–
3
3
–
–
O
9
bond length increased by ~0.02-0.04 Å from that of
the neutral precursor.15 A similar nitroxyl character
was proposed for the protein model FeII-
10
11
12
13
Fe
Mb(NO).22 Importantly, the spin density on the
B
Figure 3. (A) Top: IR spectrum of the headspace from the
reaction of (OEP)Fe(NO) with BF •OEt and NO, showing
the formation of N
O (2237/2212 cm-1). Bottom: Headspace
IR spectrum when (OEP)Fe(15NO) is reacted with BF
•Et
14
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3
2
nitrosyl N atom of
2
3
2
O
and unlabeled 14NO, to give the mixed labeled 15N14NO
(~2212/2194 cm-1) and 14N15NO (~2194/2170 cm-1) products as
well as 14N
also form when (OEP)Fe(14NO) is reacted with 15NO. (B)
Corresponding spectra when [K(2.2.2)]OSiMe was used
instead of BF •Et O. NO
(υNO ~1618 cm-1) was not formed
in these reactions. The isotopic N
fied by their characteristic IR spectra.25
2
O and 15N
2
O (~2167/2145 cm-1). These products
3
3
2
2
2
2
O products were identi-
The requirement for BF in the reaction suggests
3
that the Lewis acid plays an important role in acti-
vating (OEP)Fe(NO) towards reactivity with NO,
most likely via the pathway shown in Figure 4.
BF3
O
BF3
N
O
O
O
N
N
N
Figure 5. Calculated geometries (in Å and deg) and selected
NPA charges (in e units) of the optimized precursor
(P)Fe(NO) (1-NO) and products from its reactions with NO
N2O
BF3.OEt2
(-OEt2)
NO
Fe
Fe
Fe
+
other pdts
1-NO BF3
1-(NO)2 BF3
1-NO
and/or BF
3.
Bond distances are in italics-underline, and
proposed
atomic charges in bold font.
Figure 4. Proposed pathway for the N–N coupling reaction
enabled by the Lewis acid BF
1-NO•BF is –1.108e, which is substantially in-
3
3
.
creased from that of its precursor 1-NO (+0.401e)
(Table S2), rendering it susceptible to attack by ex-
ternal NO.
We employed density functional theory calcula-
tions using an unsubstituted porphine macrocycle
(P; see SI for details) to probe the proposed in-
As mentioned above, (OEP)Fe(NO) in the ab-
volvement of 1-NO•BF
3
and 1-(NO)
2
•BF in the N–
3
sence of the Lewis acid BF
N coupling reaction with external NO to gener-
ate N O. Likely structures of 1-(NO) (bottom left
3
does not engage in the
N coupling reaction depicted in Figure 4. The op-
N
–
timized structures are shown in Figure 5 (right),
2
2
and are compared with those for the non-BF con-
3
of Figure 5) were probed. The reaction ꢁG of 11.90
kcal/mol (Table S4) for NO coupling essentially
shows no catalytic role of the (P)Fe unit alone for
NO coupling.27-28
taining analogs (left).
The interaction of BF
in 1-NO•BF results in a lengthening of both the
Fe NO (from 1.718 Å to 1.911 Å) and FeN O (1.157
Å to 1.225 Å) bonds. Interestingly, the NO moiety
in 1-NO•BF becomes partially anionic ( 0.239e),
compared with a partially cationic charge (+0.131e)
3
with the terminal O atom
3
–
–
Inclusion of BF
with external NO leads to the successful generation
of N O which necessitates the consideration of the
N bond-forming step. The optimized structure
3
in the reaction of (OEP)Fe(NO)
3
–
2
N
–
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O
of 1-(NO)
In the presence of BF
has a large decrease in ꢁG from ~12 kcal/mol
(without BF present) to 0.54 kcal/mol (with BF
present). The reductions in other energy terms are
also pronounced and result in 13.53, 10.60, and
2
•BF
3
is shown in Figure 5 (bottom right).
O
B
1
2
3
4
N
N
3
, the N N coupling reaction
–
B
O
N
*
O
N
*
_
NNO
*
Fe
Fe
OR
3
–
3
trace H+
5
6
(OEP)Fe(HOB(C6F5)3)
–
–
–
7
8
9
11.62 for reaction ꢁE, zero-point-energy-corrected
ꢁE, and ꢁH, respectively. The data clearly show a
strong enthalpic driving force to help overcome the
Figure 6. Proposed pathway for the formation of N O.
2
proximal N
mediate can explain both the facile N
and formation of the (OEP)Fe( -OH)B(C
uct (isolated in ~55% yield when B(C
–
O bond (by 0.081 Å). This latter inter-
O cleavage
prod-
was used
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–
big entropy drop due to NO coupling. Both the Fe
N and (Fe)N O(B) distances become longer in 1-
(NO) •BF (by 0.284 and 0.122 Å, respectively) than
those in the precursor 1-NO•BF , thus weakening
these interactions upon binding of the second NO.
The effect of BF addition on the nature of the NO-
coupled intermediate is even more striking when
one considers that without BF (i.e., in 1-(NO) ),
both the proximal NO ( 0.338e charge; directly
bound to Fe) and distal NO ( 0.257e charge) groups
–
ꢀ
6
F
5)3
–
6
F
5)3
2
3
as the Lewis acid) whose X-ray structure was ob-
tained. Such a cis-hyponitrite isomerization has
recently been proposed for bacNOR based on DFT
calculations.6
3
3
In summary, our experimental results, supported
by DFT calculations, demonstrate for the first time
that Lewis acid activation of a synthetic mono-
heme-NO model, via coordination of the Lewis ac-
id to the terminal nitrosyl O-atom, renders the
FeNO moiety susceptible to attack by external NO
3
2
–
–
are negatively charged, which hinders NO cou-
pling due to Coulombic repulsion and explains the
lack of NO coupling determined experimentally. In
to generate a new N
–
N bond en route to N O for-
2
contrast, however, when BF
proximal O atom in 1-(NO) •BF
negative charge of 0.539e to this proximal NO
3
is attached to the
mation. Importantly, we show that it is the synergis-
tic and not the separate effects of (por)Fe and Lewis
2
3
, it induces a large
–
acid BF
tion. Our preliminary extensions to other Lewis
acids such as [K(2.2.2)]OSiMe (Figure 3B) and
B(C (Figure S2) show that they also enable the
3
that is critical for the NO coupling reac-
moiety, whereas the distal NO moiety changes to
be positively charged (+0.146e), which results in a
strong favorable Coulombic attraction to facilitate
the NO coupling reaction as observed experimen-
3
6
F
5)3
stoichiometric {heme-15NO + 14NO} coupling reac-
tion. Indeed, our results suggest that a redox-
active (second) metal is not necessarily required for
tally. The resulting short N
1.240 Å in 1-(NO) •BF is indicative of a strong N
N bond typical of that determined in hyponitrite
[O N=N
O]-salts.29-30 Additional results in the SI
show that BF alone does not enable NO coupling
–N bond distance of
2
3
–
the first but critical stoichiometric N–N bond for-
–
–
mation step for NO coupling with the (por)Fe(NO)
fragment. However, in bacNOR catalysis, a second
redox center in the active site would be required to
3
(nor does NO by itself),31 so it is the synergistic effect
of both iron porphyrin and Lewis acid that is criti-
cal for NO coupling, which may help understand
the biological NOR mechanism in systems where
both heme and nearby Lewis acid are available.
complete the reaction to generate both N O and
2
water, and be catalytically competent while main-
taining strict control of this biological heme-NO
activation. These results lend the first chemical
Our results provide experimental support for the
support for the proposed cis-b mechanism as a vi-
3
cis:b
where it is the original heme nitrosyl FeN
acid) bond in the 1-(NO) •BF intermediate that, is
cleaved to give N O. The observed N O may derive
3
mechanism for the NO-coupling reaction,
able, but not necessarily exclusive, pathway for NO
coupling by the bacterial NO reductase enzymes
and related systems.
–
O(Lewis
2
3
2
2
from two isomers of the cis-hyponitrite intermedi-
ate, with the second (O-coordinated) form (Figure
6; middle) having a slightly lower energy (by ~1
kcal/mol; Table S1 footnote) but a clearly longer
ASSOCIATED CONTENT
Supporting Information.
The Supporting Information is available free of charge
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13. Wayland, B. B.; Olson, L. W., J. Am. Chem. Soc. 1974, 96,
Experimental, crystallography details (CCDC
1
2
3
6037-6041.
1813020), additional figures, tables, and computation-
al details (PDF)
14. Lorkovic, I.; Ford, P. C., J. Am. Chem. Soc. 2000, 122, 6516-
6517.
4
5
6
7
8
9
15. Kundakarla, N.; Lindeman, S.; Rahman, M. H.; Ryan, M. D.,
Inorg. Chem. 2016, 55, 2070-2075.
AUTHOR INFORMATION
Corresponding Authors: yong.zhang@stevens.edu (DFT),
16. Wei, Z. C.; Ryan, M. D., Inorg Chem 2010, 49, 6948-6954.
17. Pellegrino, J.; Hubner, R.; Doctorovich, F.; Kaim, W., Chem.
Eur. J. 2011, 17, 7868-7874.
and grichteraddo@ou.edu (experimental)
Notes
18. Goodrich, L. E.; Roy, S.; Alp, E. E.; Zhao, J. Y.; Hu, M. Y.;
Lehnert, N., Inorg. Chem. 2013, 52, 7766-7780.
19. Similar υNO shifts of –118 to –261 cm-1 have been noted for
crystallographically characterized coordination compounds
The authors declare no competing financial interest.
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ACKNOWLEDGMENT
with metal-NO-BX
linkages.20-21
3
We are grateful to the National Science Foundation
(CHE-1566509 to GBR-A) and the National Institutes
of Health (GM085774 to YZ) for funding for this
work.
20. Lee, K. E.; Arif, A. M.; Gladysz, J. A., Chem Ber 1991, 124,
309-320.
21. Choualeb, A.; Blacque, O.; Schmalle, H. W.; Fox, T.;
Hiltebrand, T.; Berke, H., Eur. J. Inorg. Chem. 2007, 5246-
5261, and refs therein.
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26. This [(OEP)Fe(14NO)]BF
attack of excess added 14NO on an [(OEP)Fe](O(H)BF
3
OH product likely forms from the
) in-
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3
termediate after
[(OEP)Fe(NO)](B(C
analogous B(C
N
2
O
6
F
5
6F5
6. Blomberg, M. R. A.; Siegbahn, P. E. M., J. Comput. Chem.
2016, 37, 1810-1818.
6
F5
)
3
reaction has been characterized by X-ray
crystallography (Figure S5).
7. Collman, J. P.; Dey, A.; Yang, Y.; Decreau, R. A.; Ohta, T.;
Solomon, E. I., J. Am. Chem. Soc. 2008, 130, 16498-16499.
8. Chakraborty, S.; Reed, J.; Sage, J. T.; Branagan, N. C.; Petrik,
I. D.; Miner, K. D.; Hu, M. Y.; Zhao, J. Y.; Alp, E. E.; Lu, Y.,
Inorg. Chem. 2015, 54, 9317-9329.
27. Yi, J.; Morrow, B. H.; Campbell, A. L. O. C.; Shen, J. K.;
Richter-Addo, G. B., Chem. Commun. 2012, 48, 9041-9043.
28. Heinecke, J. L.; Khin, C.; Iretskii, A. V.; Ford, P. C., Poster
presentation INOR-465 at the 237th National Meeting of the
American Chemical Society, Salt Lake City, UT, USA,
March 2009.
9. Blomberg, M. R. A., Biochemistry 2017, 56, 120-131.
10. Lin, Y.-W.; Yeung, N.; Gao, Y.-G.; Miner, K. D.; Tian, S.;
Robinson, H.; Lu, Y., Proc. Natl. Acad. Sci. USA 2010, 107,
8581-8586.
29. Arulsamy, N.; Bohle, D. S.; Imonigie, J. A.; Sagan, E. S.,
Inorg. Chem. 1999, 38, 2716-2725.
30. Feldmann, C.; Jansen, M., Z. Kristallogr. 2000, 215, 343-345.
31. Dimerization of NO has been discussed extensively in the
literature: Urban, B.; Strobel, A.; Bondybey, V. E., J. Chem.
Phys. 1999, 111, 8939-8949, and references therein.
11. Wang, J.; Schopfer, M. P.; Pulu, S. C.; Sarjeant, A. A. N.;
Karlin, K. D., Inorg. Chem. 2010, 49, 1404-1419.
12. Wayland,13 Ford,14 and Karlin11 have shown that
(por)Fe(NO) compounds react with NO to generate the
trans dinitrosyls (por)Fe(NO) .
2
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