Oxygen binding to sulfur in nitrosylated iron-thiolate complexes: Relevance to the Fe-containing nitrile hydratases

Article abstract of DOI:10.1021/ja035292t

Iron-nitrosyl complex containing S-bonded monosulfinate [PPN][(NO)Fe(S,SO₂-C₆H₄)(S,S-C₆H₄)] (3) has been isolated from sulfur oxygenation of complex [PPN][(NO)Fe(S,S-C₆H₄)₂] (2) which is obtained from addition of NO molecule to [PPN][(C₄H₈O)Fe(S,S-C₆H₄)₂] (1) in organic solvents. This result reveals that binding of NO to the iron center promotes sulfur oxygenation of iron dithiolates by dioxygen and stabilizes the S-bonded sulfinate iron species. Analysis of the bond angles for complexes 2 and 3 reveals that iron is best described as existing in a distorted trigonal bipyramidal coordination environment surrounded by one NO, three thiolates, and one sulfinate in complex 3, whereas the distorted square pyramidal geometry is adopted in complex 2. Complex 3 further reacts in organic solvents with molecular oxygen in the presence of [PPN][NO₂] to produce the dinuclear bis(sulfinate) complex [PPN]₂[(NO)Fe(SO₂,SO₂-C₆H₄)(S,S-C₆H₄)]₂ (4). Complex 3 showed reaction with PPh₃ in THF/CH₂Cl₂ to yield complex 2 and Ph₃PO. Upon photolysis of CH₂Cl₂ solution of complex 3 under N₂ purge at ambient temperature, the UV-vis and IR spectra consistent with the formation of complex 2 demonstrate that complex 2 and 3 are photochemically interconvertible. Obviously, complex 3 is thermally quite stable but is photochemically active toward [O] release. Also described are the X-ray crystal structures of 3 and 4. Copyright

Full text of DOI:10.1021/ja035292t

Published on Web 08/30/2003
Oxygen Binding to Sulfur in Nitrosylated Iron-Thiolate Complexes:
Relevance to the Fe-Containing Nitrile Hydratases
Chien-Ming Lee,† Chung-Hung Hsieh,† Amitava Dutta,†,§ Gene-Hsiang Lee,‡ and Wen-Feng Liaw*,†
Department of Chemistry, National Tsing Hua UniVersity, Hsinchu 30043, Taiwan, and Instrumentation Center,
National Taiwan UniVersity, Taipei 10764, Taiwan
Received March 24, 2003; E-mail: wfliaw@mx.nthu.edu.tw
Nitrile hydratase (NHase) is a metalloenzyme which catalyzes
the hydrolysis of a variety of nitriles to the corresponding amides.1-3
Recent X-ray crystallographic studies on the inactive form of the
Fe-containing nitrile hydratase (Fe-NHase) from Rhodococcus sp.
N-771 revealed that the iron center is coordinated by two depro-
tonated carboxamido nitrogens, three Cys-S residues with two of
them posttranslationally modified to Cys-sulfinic (Cys-SO2) and
Cys-sulfenic (Cys-SO) groups, and a NO molecule.4 The iron site
of the Fe-NHase coordinated by the modified cysteines residues
-
(sulfinate RSO2 and sulfenate RSO- groups) through the sulfur
atoms is unprecedented.1-4 An inactive, NO-bound form is gener-
ated in cells grown in the dark, and the active form of the Fe-
NHase is regenerated with release of NO molecule upon exposure
to light.5,6 The role/function of the NO ligand, NO binding to the
iron active site before or after Cys-S oxygenation, the oxidant(s)
responsible for the posttranslational modifications of the bound
Cys-S donors at the active site of the enzyme, the biogenic
mechanism and the functional role of the modified cysteine-sulfinic
and -sulfenic groups, and the reason(s) for the asymmetric
oxygenation of the two Cys-S ligands are the principal questions
to be raised in the chemistry of the Fe-NHase.7-9 Herein, we report
an iron NO-bound complex [(NO)Fe(S,S-C6H4)2]- (2) which reacts
with molecular oxygen to afford the corresponding S-bonded
monosulfinate [(NO)Fe(S,SO2-C6H4)(S,S-C6H4)]- (3) (Figure 1) and
the dimeric S-bonded bis(sulfinate) species [(NO)Fe(SO2,SO2-
C6H4)(S,S-C6H4)]22- (4), respectively. Also, photolysis study reveals
that complexes 2 and 3 are photochemically interconvertible.
When [PPN][(CO)2(CN)Fe(S,NH-C6H4)] (0.4 mmol)10 was re-
acted directly with 1,2-benzenedithiol (0.8 mmol) in tetrahydrofuran
(THF) at room temperature, the pentacoordinate Fe complex [PPN]-
[(C4H8O)Fe(S,S-C6H4)2] (1) was isolated as a dark red-brown solid
after recrystallization from THF/hexane (yield 80%).11 Subsequent
addition of NO gas to complex 1 in THF/CH2Cl2 produced the
thermally stable, dark reddish brown [PPN][(NO)Fe(S,S-C6H4)2]
(2) complex (Scheme 1a).12 Obviously, complex 1 serves as an
efficient NO trapping agent. Complex 2 (0.1 mmol, 0.0902 g)
reacted slowly with molecular oxygen in THF/CH2Cl2 solution at
room temperature for one week to yield the S-bonded monosulfinate
[PPN][(NO)Fe(S,SO2-C6H4)(S,S-C6H4)] (3) complex (Scheme
1b).13-15 The dark purple solid 3 was isolated in 21% yield (0.02
g) after the mixture solution was separated by silica gel chroma-
tography with THF and CH2Cl2 as eluant and recrystallized with
THF/CH2Cl2 and diethyl ether (On the basis of the UV-vis
electronic absorption, the actual yield of conversion of 2 to 3 is
calculated as 35%.).15 Preliminary study shows that complex 1 does
not initiate O2 activation to yield iron-sulfinate/-sulfenate com-
pound identified by IR ν(SO) spectra; instead, a trace amount of
an insoluble yellow solid occurs after the reaction solution is stirred
Figure 1. ORTEP drawing and labeling scheme of the [(NO)Fe(S,SO2-
C6H4)(S,S-C6H4)]- anion. Fe-N(1), 1.629(3); Fe-S(av), 2.219(2); N(1)-
O(1), 1.169(4) Å.
Figure 2. ORTEP drawing and labeling scheme of the [(NO)Fe(SO2,SO2-
2-
C6H4)(S,S-C6H4)]2 anion. Fe(1)-N(1), 1.647(3); Fe-S(av), 2.2785(9);
N(1)-O(1), 1.153(3) Å.
in THF/CH2Cl2 for 6 days. Thus, the presence of NO binding to
the Fe center appears crucial in promoting oxygenation at sulfur
and resulting in the formation of the thermally stable iron-
monosulfinate complex 3.
The infrared spectrum of complex 3 shows strong bands at 1779
and 1196, 1060 cm-1 (KBr), corresponding to the ν(NO) and ν-
(SO) stretching frequencies of the S-bonded sulfinate group,
respectively.13 Reactions carried out by using 18O2 demonstrate that
O2 is the source of the sulfinate oxygen atoms. Infrared spectrum
displays ν(SO) vibrational bands at 1154, 1019 cm-1 (KBr) in the
18O-labeled complex 3. Uptake of oxygen atoms by complex 2, to
yield complex 3, was followed by UV-vis spectrophotometry.
Complex 2 has bands in the electronic absorption spectrum at 497
nm (THF). Upon sulfur oxygenation, the color of the complex
solution changed from dark reddish brown to purple, and the band
† Department of Chemistry, National Tsing Hua University.
‡ Instrumentation Center, National Taiwan University.
§ Current address (Dr. Amitava Dutta): Department of Chemistry, Bangabasi
Morning College, 19, Scott Lane, Calcutta-700009, India.
9
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J. AM. CHEM. SOC. 2003, 125, 11492-11493
10.1021/ja035292t CCC: $25.00 © 2003 American Chemical Society

C O M M U N I C A T I O N S
Scheme 1
oxygenation of iron-dithiolates by molecular oxygen and stabilizes
the S-bonded monosulfinate iron species, as observed in the inactive,
NO-bound form of the Fe-NHase, and the iron-NO-sulfinate
species exhibit the photolabilization of sulfur-bound [O] moiety
under mild conditions. Studies of the NO/Fe oxidation state(s) of
this series of {Fe(NO)}6-type iron-NO-sulfinate species by XAS,19
the influence of {Fe(NO)}n electronic structure on the Fe-N-O
bond angle as well as sulfinate ligand(s) on the electronic
environment of iron center,19 the effect of S atom electron density
on the sulfur oxygenation of the analogous iron-thiolate-nitrosyl
compounds, and mechanistic studies of sulfur oxygenation are
ongoing.20
Acknowledgment. We greatly acknowledge financial support
from the National Science Council (Taiwan).
Supporting Information Available: Crystallographic data in CIF
format and additional figures and experimental details (PDF). This
material is available free of charge via the Internet at http://pubs.acs.org.
References
at 497 nm disappeared with the formation of two intense absorption
bands at 525 and 980 nm. The H NMR spectrum of complex 3,
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1
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V (E1/2) (vs Ag/AgClO4), as compared to -0.81 and -1.16 V (E1/2
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for complex 2.13
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The S-bonded monosulfinate complex 3 undergoes oxygen
transfer reaction in THF/CH2Cl2 solution with 2 equiv of PPh3
(expected to be O-atom abstracting agent) over the course of 5 days
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NMR spectroscopy (Scheme 1b′).16 The conversion of complex 3
to complex 2 was also displayed when CH2Cl2 solution (10 mL)
of complex 3 (0.05 mmol) was photolyzed under N2 purge at
ambient temperature for 60 min; the shift in electronic absorptions
at 525 and 980 nm to 497 nm is accompanied by a change in color
of the solution from purple to dark reddish brown which is in accord
with the formation of complex 2 (Scheme 1b′). During this
transformation, no intermediate was detected spectrally. The
reversibility of [O] atom binding demonstrates that complexes 2
and 3 are photochemically interconvertible.17
Subsequent reaction of complex 3 (0.939 g, 1 mmol) with [PPN]-
[NO2] (0.584 g, 1 mmol) in the presence of O2 in THF/CH2Cl2
(1:1 ratio) for 10 days at room temperature, as shown in Scheme
1c, produced the dark blue, thermally unstable dimeric bis(sulfinate)
[PPN]2[(NO)Fe(SO2,SO2-C6H4)(S,S-C6H4)]2 (4) crystals (yield 3%)
after washed with THF and recrystallized from CH2Cl2.18 Complex
4 displayed three distinct peaks at 1212, 1067, 1057 cm-1 (KBr)
in the IR ν(SO) spectrum, consistent with the presence of
bis(sulfinate) groups coordinated to iron.16
Structures of complexes 3 and 4 are presented in Figures 1 and
2, respectively. Analysis of the bond angles for complexes 2 and 3
reveals that iron is best described as existing in a distorted trigonal
bipyramidal coordination environment with NO and sulfinate groups
occupying equatorial and axial positions, respectively, in complex
3, whereas the distorted square pyramidal geometry is adopted in
complex 2. Consistent with other published transition-metal sulfinate
complexes,13 the S-O bond lengths average to ca. 1.464(2) and
1.462(2) Å in complexes 3 and 4, respectively. The O‚‚‚O distance
is measured at 2.468 Å, while the S(1)‚‚‚S(2) distance is 3.072 Å
(S(1)‚‚‚S(3), 3.030 Å) in complex 3.
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(11) Complex 1: 1H NMR (CD2Cl2): δ 3.84 (br), 1.98 (br) (C4H8O), -3.01
(br), -36.79 (br) (S,S-C6H4) ppm. Absorption spectrum (THF) [λmax, nm
(ꢀ, M-1 cm-1)]: 560(11469), 360(16658), 329(17441), 302(17991). Anal.
Calcd for C52H46ONP2S4Fe: C, 65.96; H, 4.90; N, 1.48. Found: C, 66.31;
H, 4.92; N, 1.79.
(12) Complex 2: IR: 1789 s (THF) (νNO) cm-1 1H NMR (CDCl3): δ 6.87
.
(m), 7.55 (m) (S,S-C6H4) ppm. Absorption spectrum (THF) [λmax, nm (ꢀ,
M-1 cm-1)]: 320(34925), 497(4400), 610(1010). Anal. Calcd for C48H38
-
ON2P2S4Fe: C, 63.71; H, 4.23; N, 3.09. Found: C, 63.49; H, 4.70; N,
3.38. The X-ray structure of 2 will be published in the full report.
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(15) Complex 3: IR: 1789 s (THF), 1791 s (CH2Cl2) (νNO); 1779 (KBr) (νNO),
1196, 1060 (KBr) (νSO) cm-1 1H NMR (CDCl3): δ 8.026 (dd), 7.765
.
(d), 7.17 (dd), 7.08 (t), 6.985 (t) (S,S-C6H4, S, S(O)2-C6H4) ppm.
Absorption spectrum (THF) [λmax, nm (ꢀ, M-1 cm-1)]: 312(23829), 525-
(4750), 625sh(2600), 980(3900). Anal. Calcd for C48H38O3N2P2S4Fe: C,
61.54; H, 4.09; N, 2.99. Found: C, 62.28; H, 4.37; N, 3.15.
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T.; Darensbourg, M. Y. J. Am. Chem. Soc. 1995, 117, 963-973.
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C, 60.20; H, 4.37; N, 2.60.
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In summary, the results obtained from this work implicate that
binding of one NO molecule to the Fe center promotes sulfur
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