Dihydrogen activation by sulfido-bridged dinuclear Ru/Ge complexes: Insight into the [NiFe] hydrogenase unready state

Article abstract of DOI:10.1039/c0cc03391j

A S/SH bridged hetero-dinuclear Ru/Ge complex cation reacted with H ₂ to afford the μ-S/μ-H complex. The reaction was considerably slower compared to that of the μ-S/μ-OH complex. Thus, the μ-S/μ-SH and μ-S/μ-OH complexes might provide models f

Full text of DOI:10.1039/c0cc03391j

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Dihydrogen activation by sulfido-bridged dinuclear Ru/Ge complexes:
insight into the [NiFe] hydrogenase unready statew
Tsuyoshi Matsumoto,* Naohisa Itakura, Yukiko Nakaya and Kazuyuki Tatsumi*
Received 21st August 2010, Accepted 22nd October 2010
DOI: 10.1039/c0cc03391j
A S/SH bridged hetero-dinuclear Ru/Ge complex cation reacted
with H2 to afford the l-S/l-H complex. The reaction was
considerably slower compared to that of the l-S/l-OH complex.
Thus, the l-S/l-SH and l-S/l-OH complexes might provide
models for the unready and ready states, respectively, of [NiFe]
hydrogenase.
Chart 1
[NiFe] hydrogenase, which catalyzes a reversible conversion
of dihydrogen into protons and electrons, has been recognized
as the key enzyme in hydrogen metabolism in nature.1
In the inactive form, the active site contains a hetero-dinuclear
Ni/Fe complex bridged by two cysteine thiolates and
an O-donor ligand. The O-donor ligand disappears upon
activation by H2, and the nickel approaches the iron, either
to form a direct Ni–Fe bond or a m-hydride bridged metal pair.
Recently, Ogo and co-workers have reported the conversion of
a dinuclear Ni/Ru aqua complex to the Ni(m-H)Ru complex
upon treatment with H2, modeling the activation of
[NiFe] hydrogenase.2 In the course of our [NiFe] hydrogenase
model studies,3–5 we synthesized hetero-dinuclear Ru/Ge com-
Scheme 1
plexes having S/O bridges, Dmp(Dep)Ge(m-S)(m-O)Ru(PR3)
ligand as a third bridge, states, as has been proposed as a
possible structure for the inactive state.1b,7
(1a;
R = Ph, 1b; R = Et), and S/OH bridges,
[Dmp(Dep)Ge(m-S)(m-OH)Ru(PR3)](BArF4) (2a; R = Ph, 2b;
R = Et),4 and investigated the reaction of 1a and 2a with H2
(Dmp = 2,6-dimesitylphenyl, Dep = 2,6-diethylphenyl,
ArF = 3,5-(CF3)2C6H3).5 Although this metal pair is not
identical with that of the hydrogenase, we have obtained
several important results that may provide insight into the
reaction mechanism of [NiFe] hydrogenase; (i) both 1a and 2a
activated H2 heterolytically, but the reaction of 2a proceeded
more readily under milder conditions, (ii) the reaction of 2a
with H2 afforded the m-S/m-H complex, which could model the
[NiFe] hydrogenase activation process, (iii) the reaction of H2
and 2a was reversible, and that (iv) 2a cannot merely activate
H2 heterolytically, but further convert H2 into two protons
and electrons. In order to expand the scope of this study, we
have examined the reactions of H2 and Ru/Ge complexes
having S/S bridges (3a,b) and S/SH bridges (4a,b) (Chart 1).
This study may imply that the unready Ni-B0 and Ni-‘S’ states
of [NiFe] hydrogenase6 are oxidized forms having an S-donor
The m-S/m-S complexes Dmp(Dep)Ge(m-S)2Ru(PR3)
(3a;
R = Ph, 3b; R = Et) were synthesized from
Dmp(Dep)Ge(SH)2, [RuCl2(Z6-p-arene)], and the corresponding
phosphines according to Scheme 1.4 Protonation of 3a and 3b
upon treatment with H(OEt2)2BArF gave the m-S/m-SH
4
complex cations [Dmp(Dep)Ge(m-S)(m-SH)Ru(PR3)](BArF
)
4
(4a; R = Ph, 4b; R = Et), respectively.4
As reported previously, the reaction of 3a and H2 resulted in
the recovery of the starting materials even under 10 atm H2 at
90 1C in benzene.5a Unexpectedly, complex cation 4a was also
intact under 1–5 atm H2 at 80–90 1C, while the m-S/m-OH
analogue 2a smoothly reacted with 1 atm H2 at rt within 7 h.
On the other hand, the PEt3 analogue 4b was found to react
with 1 atm H2 gradually in refluxing benzene, and was
converted to the m-S/m-H complex 5b in 83% yield in 3 days
with concomitant formation of H2S (Scheme 2).8 The enhanced
reactivity of the PEt3 adduct was also observed for the m-S/m-OH
complexes, so that the reaction of 2b and 1 atm H2 was
completed within 5 min.9 The reaction of 4b is considerably
Department of Chemistry, Graduate School of Science,
Research Center for Materials Science, Nagoya University,
Furo-cho, Chikusa-ku, Nagoya 464-8602, Japan.
E-mail: i45100a@nucc.cc.nagoya-u.ac.jp; Fax: +81 52-789-2943;
Tel: +81 52-789-2474
w Electronic supplementary information (ESI) available: Experimental
details and spectroscopic data. CCDC 789927 (5b) and 789928 (6b).
For ESI and crystallographic data in CIF or other electronic format
see DOI: 10.1039/c0cc03391j
Scheme 2
c
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Scheme 3
slower compared to that of 2b. Thus sluggishness indicates the
reverse reaction for 4b is faster than for 2b. Indeed, addition of
1.1 equiv. H2S to 5b gave 4b quantitatively within 5 min at rt
with concomitant formation of H2. Complex 5a, synthesized
by the reaction of 2a and H2, was also converted to 4a
immediately upon a similar treatment with H2S. Thus, in
order to promote the forward H2 activation reaction, the
removal of H2S is indispensable, and thus solvent-reflux
conditions are required.
Fig. 1 ORTEP drawings of 5b. Selected bond distances (A) and
angles (deg): Ru(1)–S(1) 2.4565(15), Ru(1)–P(1) 2.3176(12),
Ge(1)–S(1) 2.1486(12), Ru(1)–Ge(1) 2.5659(9), Ru(1)–H(1) 1.67(5),
Ge(1)–H(1) 1.97(6), Ru(1)–S(1)–Ge(1) 67.34(4), Ge(1)–H(1)–Ru(1)
90(2).
Interestingly, the m-S/m-SH and m-S/m-OH complexes were
interconverted in the presence of H2O or H2S. When complex
4a was treated with 20 equiv. H2O in THF-d10 at 293 K,
complexes 4a and 2a were observed in a 98 : 2 ratio according
to the 1H NMR spectra, and thus the equilibrium constant Keq
for Scheme 3 can be estimated to be B10ꢀ4. It is of note that
interconversion was not observed between the m-S/m-S com-
plexes 3a,b and the m-S/m-O complexes 1a,b, where proto-
nation of m-S or m-O would be essential for these conversions.
Our detection of the 4a 2 2a equilibrium prompted us to
re-examine the reaction of 4a and H2 in the presence of H2O.
When a THF solution of 4a was refluxed under 1 atm H2 with
10 equiv. H2O for 1 day, the reaction proceeded as expected,
and complex 5a was obtained in 68% yield. In this reaction,
complex 2a was generated from 4a and H2O in situ, which then
reacted with H2.
Fig. 2 ORTEP drawings of 6b. Selected bond distances (A) and
angles (deg): Ru(1)–S(1) 2.4757(14), Ru(1)–P(1) 2.2952(15),
Ge(1)–S(1) 2.1871(14), Ru(1)–Ge(1) 2.4157(6), Ru(1)–S(1)–Ge(1)
62.04(3), Ge(1)–Ru(1)–S(1) 53.10(3), Ru(1)–Ge(1)–S(1) 64.85(3).
It can be demonstrated that the m-hydride of 5b shows
protonic behavior as observed for 5a. Thus treatment of 5b
with tetraethylammonium hydroxide resulted in quantitative
shortened by 0.15 A compared to 5b becoming a common
Ru–Ge s-bond distance, and accordingly the bond angle around
S(1) becomes smaller by 5.31 from that of 5b.
formation of Dmp(Dep)Ge(m-S)Ru(PEt3) (6b) (Scheme 4).
Conversely, the protonation of 6b by H(OEt2)2BArF in
4
toluene gave 5b, quantitatively.
In this study, we report that the m-S/m-SH complex was
converted to the m-S/m-H complex upon treatment with H2, as
was observed for the m-S/m-OH complex. This reaction was
considerably slower compared to that of the m-S/m-OH
complex. However, in the presence of H2O, the m-S/m-SH
complex equilibrates with the m-S/m-OH complex, and
then it appeared to react with H2 more smoothly to form the
m-S/m-H complex, although it is still slower than the case of
the m-S/m-OH complex (Scheme 5). The different reactivity of
the m-S/m-OH and m-S/m-SH complexes toward H2 reminds us
The molecular structures of 5b and 6b, determined by X-ray
analysis, are shown in Fig. 1 and 2, respectively.z The structural
properties and the metric parameters of 5b and 6b are quite
similar to those of the previously reported PPh3 analogues of
5a and 6a, respectively, irrespective of the different phosphines.5b
While their Ru–S and Ge–S bond distances are typical,4,10 the
Ru(1)–H(1) distance of 5b is elongated compared to terminal
Ru–H bonds,5a and is similar to those of m-hydride complexes.11
The Ge(1)–H(1) distance is even longer than the Ru(1)–H(1)
bond, but is shorter than that of (depe)2(CO)Mo(Z2-H–GePh2H)
[2.08(6) A],12 indicating a weak bonding interaction between Ge
and the hydride on Ru. The Ru(1)–Ge(1) distance of 2.5659(9) A
is also longer than those of the Ru–Ge s-bonds of
(C6H6)Ru(CO)(GeCl3)2 [2.408(2) A] and cis-Ru(CO)4(GeCl3)2
[2.481(5) A].13 Upon deprotonation, the Ru–Ge distance of 6b is
Scheme 4
Scheme 5
c
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of the ready states (Ni-B or Ni-SIr) and the unready states
(Ni-B0, Ni-‘S’, Ni-A, or Ni-SU) of [NiFe] hydrogenase,6 in
which the ready Ni-B state is easily activated within a few
minutes under a hydrogen atmosphere, whereas the unready
Ni-A state requires longer activation times of up to hours.1
While the protein crystallographic analysis suggested that the
Ni-A state contains m-OOH as the third bridge, the Ni-B0 or
Ni-‘S’ states having a m-SH6 may be important states showing
a reactivity like the unready Ni-A state.1b,7 Considering that
sulfate-reducing bacteria produce a large amount of H2S in
their metabolism, the active site may be converted by H2S into
the Ni-B0 or Ni-‘S’ states having a m-SH, similar to our results
reported here, which show the m-S/m-OH complexes 2a,b and
the m-S/m-H complexes 5a,b quickly react with H2S and are
converted into the m-S/m-SH complexes 4a,b.
1 Recent reviews: (a) W. Lubitzs, M. van Gastel and W. Gartner, in
¨
Metal Ions in Life Sciences, ed. A. Sigel, H. Sigel, R. K. O.
Sigel, John Wiley & Sons, Ltd, New York, 2006, vol. 2,
pp. 279–322; (b) H. Ogata, W. Lubitz and Y. Higuchi, Dalton
Trans., 2009, 7577; (c) P. M. Vignais and B. Billoud, Chem. Rev.,
2007, 107, 4206; (d) J. C. Fontecilla-Camps, A. Volbeda,
C. Cavazza and Y. Nicolet, Chem. Rev., 2007, 107, 4273;
(e) A. L. De Lacey, V. Fernandez, M. Rousset and
´
R. Cammack, Chem. Rev., 2007, 107, 4304; (f) W. Lubitz,
E. Reijerse and M. van Gastel, Chem. Rev., 2007, 107, 4331;
(g) P. E. M. Siegbahn, J. W. Tye and M. B. Hall, Chem. Rev.,
2007, 107, 4414; (h) D. J. Evans and C. J. Pickett, Chem. Soc. Rev.,
2003, 32, 268.
2 (a) S. Ogo, R. Kabe, K. Uehara, B. Kure, T. Nishimura,
S. C. Menon, R. Harada, S. Fukuzumi, Y. Higuchi, T. Ohhara,
T. Tamada and R. Kuroki, Science, 2007, 316, 585; (b) B. Kure,
T. Matsumoto, K. Ichikawa, S. Fukuzumi, Y. Higuchi, T. Yagi
and S. Ogo, Dalton Trans., 2008, 4747; (c) T. Matsumoto, B. Kure
and S. Ogo, Chem. Lett., 2008, 970.
3 (a) Y. Ohki, K. Yasumura, M. Ando, S. Shimokata and
K. Tatsumi, Proc. Natl. Acad. Sci. U. S. A., 2010, 107, 3994;
(b) Y. Ohki, M. Sakamoto and K. Tatsumi, J. Am. Chem. Soc.,
2008, 130, 11610; (c) Y. Ohki, K. Yasumura, K. Kuge, S. Tanino,
M. Ando, Z. Li and K. Tatsumi, Proc. Natl. Acad. Sci. U. S. A.,
2008, 105, 7652; (d) S. Tanino, Z. Li, Y. Ohki and K. Tatsumi,
Inorg. Chem., 2009, 48, 2358; (e) Z. Li, Y. Ohki and K. Tatsumi,
J. Am. Chem. Soc., 2005, 127, 8950.
This work was supported by Grant-in-Aid for Scientific
Research on Priority Areas (No. 18GS0207) from Ministry of
Education, Culture, Sports, Science and Technology, Japan.
We are grateful to Prof. Roger E. Cramer for discussions and
careful reading of the manuscript.
Notes and references
4 T. Matsumoto, Y. Nakaya and K. Tatsumi, Organometallics, 2006,
25, 4835.
5 (a) T. Matsumoto, Y. Nakaya and K. Tatsumi, Angew. Chem., Int.
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ꢀ
z Crystal data for 5b: C72H66BF24GePRuS; triclinic; P1 (No. 2); a =
12.057(3),
b
=
16.670(4),
c
=
20.047(3) A;
a
=
68.826(12),
b = 70.639(11), g = 79.729(13)1, V = 3536.9(14) A3; Z = 2;
F(000) = 1650; m = 7.955 cmꢀ1; rcalc = 1.534 g cmꢀ3; 29 042
reflections (2y o 54.91); 15 512 unique (Rint = 0.029); R1 = 0.055
(I > 2s(I)), wR2 = 0.1597 (all data), GoF = 1.085. For 6b:
C40H53GePRuS; monoclinic; P21/c (No. 14); a = 16.292(2), b =
9.2011(14), c = 24.751(4) A; b = 91.198(2)1, V = 3709.4(9) A3; Z =
4; F(000) = 1600; m = 13.43 cmꢀ1; rcalc = 1.380 g cmꢀ3; 29 413
reflections (2y o 55.01), 8474 independent (Rint = 0.077); R1 = 0.057
(I > 2s(I)), wR2 = 0.158 (all data), GoF = 0.954. Single crystals were
mounted on a loop using oil (CryoLoop, Paratone-N, HR2-643,
Hampton Laboratories, Inc.). Diffraction data were collected at
ꢀ100 1C under a cold nitrogen stream on a Rigaku AFC8 equipped
with a Saturn 70 CCD area detector, equipped with a graphite
monochromatized MoKa source (l = 0.71070 A). Data were collected
for 720 images with an oscillation range of 0.51, and were integrated
and corrected for absorption using the Rigaku/MSC CrystalClear
program package. The structures were solved by a direct method
(SIR-97), and were refined by full-matrix least squares on F2 using
SHELXL-9714 in the Rigaku/MSC CrystalStructure program package.
Anisotropic refinement was applied to all non-hydrogen atoms. The
hydrogen atom H(1) of 5b was assigned from the Fourier map and
refined isotropically. The other hydrogen atoms were put at the
calculated positions.
6 See ref. 1d for the notation of each state of [NiFe] hydrogenase.
7 (a) Y. Higuchi and T. Yagi, Biochem. Biophys. Res. Commun.,
1999, 255, 295; (b) H. Ogata, S. Hirota, A. Nakahara, H. Komori,
N. Shibata, T. Kato, K. Kano and Y. Higuchi, Structure (London),
2005, 13, 1635.
8 The reaction was monitored by 1H NMR spectra, and the product
ratio was analyzed accordingly.
9 T. Matsumoto, Y. Nakaya and K. Tatsumi, unpublished results.
10 K. M. Baines and W. G. Stibbs, Coord. Chem. Rev., 1995,
145, 157.
11 (a) M. V. Ovchinnikov, X. Wang, A. J. Schultz, I. A. Guzei and
R. J. Angelici, Organometallics, 2002, 21, 3292; (b) G. Suss-Fink,
¨
E. G. Fidalgo, A. Neels and H. Stoeckli-Evans, J. Organomet.
Chem., 2000, 602, 188.
12 J. L. Vincent, S. Luo, B. L. Scott, R. Butcher, C. J. Unkefer,
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C. J. Burns, G. J. Kubas, A. Lledos, F. Maseras and J. Tomas,
Organometallics, 2003, 22, 5307.
13 (a) L. Y. Y. Chan and W. A. G. Graham, Inorg. Chem., 1975, 14,
1778; (b) R. Ball and M. J. Bennett, Inorg. Chem., 1972, 11, 1806.
14 G. M. Sheldrick, SHELX97, University of Gottingen, Germany,
1997.
c
1032 Chem. Commun., 2011, 47, 1030–1032
This journal is The Royal Society of Chemistry 2011