Dithiolato-bridged dinuclear iron-nickel complexes [Fe(CO) 2(CN)2(μ-SCH2CH2CH 2S)Ni(S2CNR2)]- modeling the active site of [NiFe] hydrogenase

Article abstract of DOI:10.1021/ja051590+

[NiFe] hydrogenase, the enzyme of which catalyzes the reversible oxidation of molecular hydrogen to protons and electrons, contains a unique heterodinuclear thiolate-bridged Ni-Fe complex in which the iron center is coordinated by CO and CN. We have synthesized dithiolate-bridged Ni-Fe complexes bearing CO and CN ligands to model the active center of [NiFe] hydrogenase. The Ni-Fe complexes containing a [(CN)₂(CO)₂Fe(μ-S₂)NiS₂] framework are the closest yet structural models of [NiFe] hydrogenase. Copyright

Full text of DOI:10.1021/ja051590+

Published on Web 06/04/2005
Dithiolato-Bridged Dinuclear Iron-Nickel Complexes
[Fe(CO)2(CN)2(µ-SCH2CH2CH2S)Ni(S2CNR2)]- Modeling the Active Site of [NiFe]
Hydrogenase
Zilong Li, Yasuhiro Ohki, and Kazuyuki Tatsumi*
Research Center for Materials Science and Department of Chemistry, Graduate School of Science, Nagoya
UniVersity, Furo-cho, Chikusa-ku, Nagoya 464-8602, Japan
Received March 12, 2005; E-mail: i45100a@nucc.cc.nagoya-u.ac.jp
Hydrogenase is essential to hydrogen metabolism by catalyzing
the reversible interconversion of proton and molecular hydrogen.1
The enzyme has been found in many microorganisms of biotech-
nological interest, which can be grouped into two classes based on
the type of metal-containing active sites, namely, [Fe]-only2 and
[NiFe]3 hydrogenases. For the [NiFe] hydrogenase, X-ray structure
determination has been carried out for DesulfoVibrio (D.) gigas,3a,b
D. fructosoVorans,3c D. Vulgaris (Miyazaki),3d,e and Desulfomicro-
bium (Dm.) baculatum.3f Two forms of the active sites are known.
One is referred to as the oxidized form, where Fe and Ni are bridged
by two cysteine S and one O atoms with relatively long Fe-Ni
distances of ca. 2.9 Å. The other is the reduced form, with short
Fe-Ni bonds of 2.5-2.6 Å and only two bridging cysteine S atoms
or perhaps with an additional H-bridge. An exception may be the
oxidized form of D. Vulgaris (Miyazaki), in which the triply bridged
Fe-Ni distance is as short as 2.6 Å. Despite the geometrical
diversity, interesting common features can be seen in the structure
of [NiFe] hydrogenases; the Fe center carries both CO and CN
ligands, and the four cysteine S atoms (or three cysteine S atoms
and one selenocysteine Se for Dm. baculatum) are coordinated to
Ni in a distorted tetrahedral geometry.
The reaction of (PPh4)[Fe(CO)3(CN)2Br]10c with 1 equiv of K2-
(pdt) (pdt ) 1,3-propanedithiolate) afforded (PPh4)[Fe(CO)2 (CN)2-
(pdt)K] (1) (Scheme 1). Complex 1 was characterized by means
of ESI-MS and IR spectroscopy. Although crystallization of 1 was
not successful, further treatment with 0.5 equiv of PPh4Br gave
(PPh4)3[Fe2(CO)4(CN)4(pdt)2K] (2) in 88% yield. The IR spectrum
of 2 in KBr consists of two relatively weak bands at 2102 (w) and
2085 cm-1 (m), assignable to CN stretching vibrations, and two
intense CO stretching bands at 2002 and 1938 cm-1. These IR
signals closely resemble those of 1. The Raman spectrum of 2, in
the solid state, shows one CN band at 2101 cm-1 and two CO bands
at 2002 and 1936 cm-1. The disappearance of one CN band in the
Raman spectrum indicates a trans configuration of two CN ligands,
in accordance with the X-ray derived structure.
Treatment of a CH3OH solution of 1 with Ni(PPh3)Br(S2CNR2)11
(S2CNR2 ) dithiocarbamate) in acetone led to an immediate color
change from light red to greenish brown. After stirring for 3 h at
-40 °C and for further 1 h at 0 °C, the thiolate-bridged dinuclear
Ni-Fe complexes (PPh4)[(CO)2(CN)2Fe(µ-pdt)Ni(S2CNR2)] (3a;
R ) Et, 3b; R2 ) -(CH2)5-) were obtained in 74 and 90% yields,
respectively. Alternatively, complex 3a was also prepared from 2,
but due to a necessary crystallization step, the yield was 31%. In
solution, both 3a and 3b are thermally unstable at ambient
temperature and moderately sensitive to oxygen. Thus, maintain-
ing an acetonitrile solution of 3a at room temperature resulted in
the precipitation of a brown solid and gradual formation of
[Ni(CN)2(S2CNEt2)]- in the solution, as monitored by ESI-MS.
1
According to the H NMR spectrum, 3a and 3b are diamagnetic,
presumably consisting of low-spin NiII and FeII ions. The six
methylene protons of the pdt ligand are observed as four sets of
1H NMR signals (2:2:1:1), indicating the formation of a thiolate-
bridged dinuclear structure. The Raman spectrum of 3a in CH3OH
reveals one CN stretching band at 2113 cm-1 and two relatively
broad CO stretching bands (ν(CO)) at 2040 and 1991 cm-1. The
IR spectrum in CH3OH shows two CN bands at 2110 and 2094
cm-1, and this together with the Raman signature suggests a trans
disposition of two CN ligands on Fe. The ν(CO) region of the IR
spectrum is somewhat complicated, exhibiting two intense bands
The intriguing dinuclear structure of [NiFe] hydrogenases has
been a challenging target for inorganic/organometallic chemists,4
and several thiolate-bridged dinuclear Ni-Fe complexes have been
prepared: [Ni{1,5-bis(mercaptoethyl)-1,5-diazacyclooctane}Fe-
(CO)4],5 [{Fe{N(CH2CH2S)3}(CO)2-S,S′}NiCl(dppe)],6a [{Fe{N(CH2-
CH2S)3}(CO)-S,S′}Ni(S2CNiPr 2)],6b [(C6H4S2)Ni(µ-S(C6H4)2S2)-
Fe(CO)(PMe3)2],7 [{Ni(N,N′-diethyldiazanonane-1,9-dithiolate)}-
Fe(NO)2],8 and [(NO)Ni(µ-S(CH2)2S(CH2)2S)Fe(NO)2].9 However,
these complexes do not possess the crucial CO/CN ligand set on
iron. The reason for this is the absence of CO/CN complexes of
iron, which are suitable for construction of Fe-Ni dinuclear
structures. Difficulty also comes from the strong affinity of nickel
for CN-, and therefore, a new synthetic method is required to link
the [Fe(CO)x(CN)y] fragments to appropriate Ni complexes. The
recent synthesis of FeII carbonyl/cyanide/thiolate complexes, for
example,[Fe(CO)(CN)2(bdt)]2-(bdt)benzenedithiolate),[Fe(CO)2(CN)3(SR)]2-,
and [Fe(CO)3(CN)2(SR)]-,10 prompted us to examine the reactions
of preformed FeII precursors with NiII complexes. Herein, we report
the first synthesis of the dithiolato-bridged Fe-Ni complexes, in
which Fe carries both CO and CN ligands.
at 2044 and 1994 cm-1, one with moderate intensity at 2031 cm-1
,
and a shoulder on the low-energy side of the 1994 cm-1 band.
Likewise, there are four CO bands in the IR spectrum in KBr; 2031
(s), 2015 (m), 1977 (s), 1959 (m) cm-1. The reason for the extra
pair of CO bands is not clear, but the systematic shift to higher
wavenumbers, relative to those of 2 (2002 and 1938 cm-1 in KBr),
points to S-bridging between Fe and Ni, by which π-donation from
S to Fe, and then to CO, is weakened.
X-ray analyses of 3a and 3b confirmed that the two S atoms of
pdt bridge iron to nickel, and that two CN ligands on Fe are trans
to each other. Since the coordination geometries of 3a and 3b are
9
8950
J. AM. CHEM. SOC. 2005, 127, 8950-8951
10.1021/ja051590+ CCC: $30.25 © 2005 American Chemical Society

C O M M U N I C A T I O N S
Scheme 1
Table 1. Comparison of Selected Bond Distances (Å) and the
Fe-S-Ni Angle of 3a, 3b, and the Oxidized Form of D. gigas and
D. fructosovorans
3a
3b
D gigas
D. fructosovorans
Fe-Ni
3.0587(6)
84.43
2.337
2.213
2.206
3.0364(8)
84.71
2.338
2.111
2.209
2.9
73.7
2.2
2.6
2.2
2.9
b
2.4
2.4
2.3
Fe-S-Nia
Fe-S(bridge)a
Ni-S(bridge)a
Ni-S(terminal)a
a Averaged. b Data not deposited in the protein data bank (PDB).
for the Promotion of Science (JSPS) for a fellowship. We thank
Prof. Josef Takats at University of Alberta for his comments.
Supporting Information Available: Details of synthesis and
characterization and crystallographic data for 2‚2THF, 3a, and 3b (PDF
and CIF). This material is available free of charge via the Internet at
http://pubs.acs.org.
References
(1) (a) Cammack, R. Nature 1999, 397, 214-215. (b) Adams, M. W. W.;
Stiefel, E. I. Science 1998, 282, 1842-1843. (c) Thauer, R. K.; Klein, A.
R.; Hartmann, G. C. Chem. ReV. 1996, 96, 3031-3042. (d) Albracht, S.
P. J. Biochim. Biophys. Acta 1994, 1188, 167-204. (e) Evans, D. J.;
Pickett, C. J. Chem. Soc. ReV. 2003, 32, 268-275.
(2) (a) Peters, J. W.; Lanzilotta, W. N.; Lemon, B. J.; Seefeldt, L. C. Science
1998, 282, 1853-1858. (b) Nicolet, Y.; Piras, C.; Legrand, P.; Hatchikian,
C. E.; Fontecilla-Camps, J. C. Structure 1999, 7, 13-23. (c) Lemon, B.
J.; Peters, J. W. Biochemistry 1999, 38, 12969-12973.
Figure 1. Anion part of 3a with thermal ellipsoids at 50% probability level.
(3) (a) Volbeda, A.; Charon, M. H.; Piras, C.; Hatchikian, E. C.; Frey, M.;
Fontecilla-Camps, J. C. Nature 1995, 373, 580-587. (b) Volbeda, A.;
Garcin, E.; Piras, C.; de Lacey, A. L.; Fernandez, V. M.; Hatchikian, E.
C.; Frey, M.; Fontecilla-Camps, J. C. J. Am. Chem. Soc. 1996, 118,
12989-12996. (c) Rousset, M.; Montet, Y.; Guigliarelli, B.; Forget, N.;
Asso, M.; Bertrand, P.; Fontecilla-Camps, J. C.; Hatchikian, E. C. Proc.
Natl. Acad. Sci. U.S.A. 1998, 95, 11625-11630. (d) Higuchi, Y.; Yagi,
T.; Yasuoka, N. Structure 1997, 5, 1671-1680. (e) Higuchi, Y.; Ogata,
H.; Miki, K.; Yasuoka, N.; Yagi, T. Structure 1999, 7, 549-556. (f)
Garcin, E.; Vernede, X.; Hatchikian, E. C.; Volbeda, A.; Frey, M.;
Fontecilla-Camps, J. C. Structure 1999, 7, 557-566.
practically the same, only the ORTEP drawing of 3a is shown in
Figure 1. A distinction between CO and CN was unequivocally
made by a clear difference in Fe-CN and Fe-CO distances (av
1.927 versus av 1.779 Å). Complexes 3a and 3b reproduce well
the structural feature of the active site of [NiFe] hydrogenase in
that the two thiolate S atoms link Fe and Ni, the Ni is coordinated
by four S atoms, and the Fe carries both CO and CN ligands.
Important geometrical parameters of 3a and 3b are compared with
those of the oxidized forms of D. gigas and D. fructosoVorans in
Table 1. The Fe(Ni)-S and Fe-Ni distances are all comparable,
except for the unusually long Ni-S(bridge) bond length in D. gigas.
One obvious difference between our model complexes and the
oxidized forms is the number of bridging ligands. The triply bridged
structure of the oxidized form of D. gigas results in a smaller Fe-
S-Ni angle, and yet the Fe-Ni distance remains long, whereas
the doubly bridged Fe-Ni bond of the reduced form of either D.
Vulgaris (Miyazaki) or Dm. baculatum is substantially short. It is
not likely that the Ni-Fe distance is dictated by the number of
bridging atoms, but is rather controlled by the oxidation state and/
or spin state of metal centers. The coordination geometry of Ni in
3a and 3b is close to square planar with the dihedral angles of 8.0
and 4.0 (av)°, respectively, between the [NiS1S2] and [NiS3S4]
planes. This is in contrast to the highly distorted NiS4 geometry of
the oxidized and reduced forms of [NiFe] hydrogenases.
It is known that carbon monoxide acts as a reversible inhibitor
of hydrogenases,12 and the incoming CO is thought to be bound to
Ni, on the basis of spectroscopic and X-ray crystallographic study.13
However, the six-coordinate nature of Fe in 3a,b with two CO
ligands implies that extra CO on iron could be another possibility.
Although there are some discrepancies between the structures of
3a,b and the active sites of [NiFe] hydrogenases, they are the closest
yet structural models containing many important features, and this
should facilitate better understanding of physicochemical properties
and the structure-function relationship of hydrogenases.
(4) Happe, R. P.; Roseboom, W.; Pierik, A. J.; Albracht, S. P. J.; Bagley, K.
A. Nature 1997, 385, 126.
(5) Lai, C.-H.; Reibenspies, J. H.; Darensbourg, M. Y. Angew. Chem., Int.
Ed. 1996, 35, 2390-2393.
(6) (a) Smith, M. C.; Barclay, J. E.; Cramer, S. P.; Davies, S. C.; Gu, W.-
W.; Hughes, D. L.; Longhurst, S.; Evans, D. J. J. Chem. Soc., Dalton
Trans. 2002, 2641-2647. (b) Smith, M. C.; Barclay, J. E.; Davies, S. C.;
Hughes, D. L.; Evans, D. J. Dalton Trans. 2003, 4147-4151.
(7) Sellmann, D.; Geipel, F.; Lauderbach, F.; Heinemann, F. W. Angew.
Chem., Int. Ed. 2002, 41, 632-634.
(8) Osterloh, F.; Saak, W.; Hasse, D.; Pohl, S. Chem Commun. 1997, 979-
980.
(9) Liaw, W.-F.; Chiang, C.-Y.; Lee, G.-H.; Peng, S.-M.; Lai, C.-H.;
Darensbourg, M. Y. Inorg. Chem. 2000, 39, 480-484.
(10) (a) Rauchfuss, T. B.; Contakes, S. M.; Hsu, S. C. N.; Reynolds, M. A.;
Wilson, S. R. J. Am. Chem. Soc. 2001, 123, 6933-6934. (b) Sellmann,
D.; Geipel, F.; Heinemann, F. W. Chem.sEur. J. 2002, 8, 958-966. (c)
Liaw, W.-F.; Lee, N.-H.; Gau, H.-B.; Chen, C.-H.; Jung, S.-J.; Hung, C.-
H.; Chen W.-Y.; Hu, C.-H.; Lee, G.-H. J. Am. Chem. Soc. 2002, 124,
1680-1688. (d) Chen, C.-H.; Chang, Y.-S.; Yang, C.-Y.; Chen, T.-N.;
Lee, C.-M.; Liaw, W.-F. Dalton Trans. 2004, 137-143. (e) Liaw, W.-F.;
Lee, N.-H.; Chen, C.-H.; Lee, C.-M.; Lee, G.-H.; Peng, S.-M. J. Am. Chem.
Soc. 2000, 122, 488-494. (f) Hsu, H.-F.; Koch, S. A. J. Am. Chem. Soc.
1997, 119, 8371-8372.
(11) (a) Nikolov, G. S.; Tyutyulkov, N. Inorg. Nucl. Chem. Lett. 1970, 6, 697-
700. (b) Pastorek, R.; Kamenicek, J.; Brezina, F.; Hamrusova, M.; Sindelar,
Z.; Lasovaky, J. Chem. Pap. 1993, 47, 210-214.
(12) (a) Thauer, R. K.; Kaufer, B.; Zahringer, M.; Jungermann, K. Eur. J.
Biochem. 1974, 42, 447-452. (b) Yagi, T.; Honya, M.; Tamiya, N.
Biochim. Biophys. Acta 1968, 153, 699-705. (c) Daday, A.; Lambert, G.
R.; Smith, G. D. Biochem. J. 1979, 177, 139-144. (d) Adams, M. W.;
Hall, D. O. Biochem. J. 1979, 183, 11-22. (e) Yagi, T.; Kimura, K.;
Daidoji, H.; Sakai, F.; Tamura, S. J. Biochem. 1976, 79, 661-671.
(13) (a) Van der Zwaan, J. W.; Coremans, J. M.; Bouwens, E. C.; Albracht, S.
P. Biochim. Biophys. Acta 1990, 1041, 101-110. (b) Ogata, H.; Mizogu-
chi, Y.; Mizuno, N.; Miki, K.; Adachi, S.; Yasuoka, N.; Yagi, T.;
Yamauchi, O.; Hirota, S.; Higuchi, Y. J. Am. Chem. Soc. 2002, 124,
11628-11635. (c) Frey, M.; Fontecilla-Camps, J. C. In Handbook of
Metalloproteins; Messerschmidt, A., Huber, R., Poulos, T., Wieghardt,
K., Eds.; John Wiley & Sons: Chichester, U.K., 2001; Volume 2, pp
880-896. (d) DeLacey, A. L.; Stadler, C.; Fernandez, V. M.; Hatchikian,
E. C.; Fan, H.-J.; Li, S.; Hall, M. B. J. Biol. Inorg. Chem. 2002, 7,
318-326.
Acknowledgment. This research was financially supported by
Grant-in-Aids for Scientific Research (Nos. 14078211, 16350031,
and 17036020) from the Ministry of Education, Culture, Sports,
Science, and Technology, Japan. Z.L. is grateful to the Japan Society
JA051590+
9
J. AM. CHEM. SOC. VOL. 127, NO. 25, 2005 8951