A stable hyponitrite-bridged iron porphyrin complex

Full text of DOI:10.1021/ja809781r

Published on Web 02/03/2009
A Stable Hyponitrite-Bridged Iron Porphyrin Complex
Nan Xu, Adam L. O. Campbell, Douglas R. Powell, Jana Khandogin,* and George B. Richter-Addo*
Department of Chemistry and Biochemistry, UniVersity of Oklahoma, 620 Parrington OVal,
Norman, Oklahoma 73019
Received December 15, 2008; E-mail: jana.k.shen@ou.edu; grichteraddo@ou.edu
Heme-assisted coupling of nitric oxide (NO) to form Fe{N2O2}n-
intermediates plays an important part in the reduction of NO to
N2O.1,2 In transition-metal chemistry, such metal{N2O2}n- moieties
can be generated from attack of NO on a metal-NO group,3,4 from
metal-induced coupling of NO,5 or from transfer of an intact
(N2O2)n- from a diazeniumdiolate to a metal.6 It is interesting to
note that only a small number of metal{N2O2}-containing com-
pounds have been structurally characterized, and the {N2O2} binding
modes determined to date are sketched below as structures A (M
) Pt, Ni),5,6 B (M ) M′ ) Co),7 C (M ) Ru),8 and D (M ) Co).9
Figure 1. Molecular structure of [(OEP)Fe]2(µ-ONNO) (1). Hydrogen
atoms and the dichloromethane solvates have been omitted for clarity.
Selected bond lengths (Å) and angles (deg): Fe-O ) 1.889(2), O-N )
1.375(2), N-N ) 1.250(3), Fe-N(por) ) 2.049(2)-2.064(2), FeON )
118.56(12), NNO ) 108.5(2).
Enzymes such as the NO reductase (NOR) from Paracoccus
denitrificans, cyt ba3 and caa3 from Thermus thermophilus, and
cyt cbb3 from Paracoccus stutzeri catalyze the conversion of NO
to N2O using bimetallic active sites.1,2 For these biological systems,
intermediates resembling structure B have been proposed, where
the metal{N2O2} moiety is N-bound to heme Fe (M), and where
M′ (nonheme Fe or Cu) may contact both O atoms.1,10 Collman et
al. have proposed, using results from the reaction of a diferrous
synthetic model of NOR with NO, that a trans-bis-nitrosyl
intermediate forms at the active site of NOR followed by NO
coupling (structure E) to give N2O and a bis-ferric product.11
Resonance Raman spectroscopy has been employed to assign a
HONNO-bridged Fe-Cu species (i.e., a protonated analogue of
E) during NO reduction by T. thermophilus cyt ba3.12 To the best
of our knowledge, however, no adduct of heme and an N2O2 moiety
has been structurally characterized.
moiety is trans (Figure 1). The N-N bond length of 1.250(3) Å
suggests double bond character (cf., 1.256(2) Å in crystalline
Na2N2O2).15 The distance between the two Fe centers is 6.7 Å and
is longer than the 4.4 Å distance between the Fe and Cu centers in
T. thermophilus cyt ba3 that exhibits NOR activity.16 The magnitude
of the Fe-N(por) bond lengths in 1 and the apical displacement of
Fe from the 4N-atom porphyrin mean plane (∆Fe ) 0.40 Å) are
indicative of H.S. ferric centers. It follows that the N2O2 ligand in
1 must have significant hyponitrite (i.e., dianionic) character.
To characterize the electronic structure and properties of 1, we
performed calculations using density functional theory (DFT) on
the model compound [(porphine)Fe]2(η1,η1,µ-N2O2) (1-calc) in the
trans and cis configurations. The DFT calculations were based on
the B3LYP exchange-correlation functional and a triple-ꢀ polariza-
tion basis set. In both trans and cis configurations, the H.S. species
is calculated to be lower in energy relative to the intermediate-
(I.S.) and low-spin (L.S.) variants by 8 and 19 kcal/mol, respectively
(Table S2). The calculated geometry of the trans H.S. species most
closely reproduces the crystal structural data (Table 1). Curiously,
the different spin states of the trans isomer are calculated to be ∼2
kcal/mol higher in energy than the respective cis variants. This small
difference lies within the typical error of 3-5 kcal/mol estimated
for B3LYP calculations of transition-metal complexes. Thus, the
DFT calculations are consistent with the EPR and structural data
in establishing the identity of a stable H.S. trans species. The small
energy gap between the trans and cis configurations suggests that
isolation of the cis derivative of 1 might be attainable.
The title compound was obtained from the reaction of [(OEP)-
Fe]2(µ-O) in anhydrous toluene with an in situ-generated ether
solution of hyponitrous acid (Supporting Information) (eq 1).
Workup gave the product [(OEP)Fe]2(µ-N2O2) (1) as dark purple
microcrystals in 52% isolated yield.
[(OEP)Fe]2(µ-O) + H2N2O2 f [(OEP)Fe]2(µ-N2O2) + H2O
(1)
The IR spectrum of 1 reveals a band at 982 cm-1 assigned to υas
of the N–O group υas(15NO) 973 cm-1). This band is lower than
that reported for H2N2O2 at 1014/1003 cm-1 (υas(15NO) 991/980
cm-1).13 The υs(NO) and υ(NN) bands were not observed in the
IR spectrum, presumably due to the symmetry of 1. The EPR
spectrum of 1 as a CH2Cl2/toluene glass (77 K) shows g ) 5.74
and 2.03; similar data were obtained for two high-spin (H.S.) ferric
hydroxo porphyrins.14
The X-ray crystal structure of 1 reveals that the N2O2 ligand is
To probe the charge distribution in 1, we used multipole-derived
population analysis for the trans H.S. form of 1-calc. The atomic
bound to each Fe via the η1-O binding mode and that the ONNO
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2460 J. AM. CHEM. SOC. 2009, 131, 2460–2461
10.1021/ja809781r CCC: $40.75
2009 American Chemical Society

C O M M U N I C A T I O N S
Table 1. Selected Crystal Data for 1, and Calculated Geometry
Data (in Å and deg) for [(Porphine)Fe]2(η1,η1,µ-N2O2) (1-calc)
combinations of the ligand σ orbitals. The frontier spin orbitals
from the unrestricted open-shell calculation are shown in Figure 3.
The highest occupied R spin orbital exhibits more porphine
character while the lowest unoccupied spin ꢁ orbital displays more
metal character. The N atoms of the hyponitrite bridge form a
bonding interaction in both highest occupied spin orbitals.
Protonation of a toluene solution of 1 at 0 °C using HCl results
in the formation of N2O and (OEP)FeCl (eq 2).
Fe-O
O-N
N-N
NNO
∆Fe
1 (crystal; trans)
1-calc
trans-H.S.
trans-I.S.
trans-L.S.
cis-H.S.
1.889
1.375
1.250
108.5
0.402
1.909
1.951
1.831
1.899
1.945
1.831
1.376
1.364
1.398
1.390
1.379
1.403
1.269
1.280
1.266
1.254
1.262
1.258
108.9
109.3
107.4
117.0
117.9
116.5
0.482
0.272
0.249
0.485
0.279
0.232
cis-I.S.
cis-L.S.
[(OEP)Fe]2(µ-ONNO) + 2HCl f N2O + 2(OEP)FeCl + H2O
(2)
charges on the Fe, O, and N atoms are shown in Figure 2. To further
understand the charge distribution in the FeONNOFe moiety, we
used the Nalewajski-Mrozek scheme to calculate the bond orders.
Accordingly, the bond orders for Fe-O, O-N, and N-N in 1-calc
trans-H.S. (Figure 2) are 0.79, 1.25, and 1.84, respectively, which
supports the notion of an NdN double bond in the hyponitrite
bridge.
An IR spectrum of the headspace reveals new bands at 2236/2213
and 1298/1266 cm-1 assigned to υas and υs of N2O, respectively.
The use of the 15N-labeled 1 (labeled at hyponitrite) shifts the υas
bands to 2167/2144 cm-1; the corresponding υs bands were not
observed due to its occurrence outside the detection window.
We hypothesized that the protonation reaction is initiated by H+
attack on one of the O atoms of the hyponitrite bridge followed by
O-N bond cleavage to give N2O. This is supported by the
pronounced negative charge on the hyponitrite O atom in trans-
H.S. 1-calc obtained from the DFT calculation. Further studies are
underway to uncover the mechanism of the protonation reaction.
In summary, we have prepared and characterized the first isolable
hyponitrite iron porphyrin complex and describe the first established
hyponitrite O-bonding mode to a heme model.
Figure 2. Calculated atomic charges and bond orders (bo) for the
FeONNOFe moiety.
The Kohn-Sham orbitals of the trans H.S. species of 1-calc are
expected to be similar to those of square pyramidal metal
complexes, for which the highest occupied orbital and the lowest
unoccupied orbital are the result of antibonding interactions between
Acknowledgment. We are grateful to the National Institutes
of Health for funding (GM076640; GBR-A).
2
2
2
Supporting Information Available: Experimental procedure, com-
putational details, additional references, and CIF file for 1. This material
is available free of charge via the Internet at http://pubs.acs.org.
dz as well as d(x -y ) orbitals of the metal and the symmetrized
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