A Dinuclear Ni(µ-H)Ru Complex Derived from H2

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Science  27 Apr 2007:
Vol. 316, Issue 5824, pp. 585-587
DOI: 10.1126/science.1138751


Models of the active site in [NiFe]hydrogenase enzymes have proven challenging to prepare. We isolated a paramagnetic dinuclear nickel-ruthenium complex with a bridging hydrido ligand from the heterolytic cleavage of H2 by a dinuclear NiRu aqua complex in water under ambient conditions (20°C and 1 atmosphere pressure). The structure of the hexacoordinate Ni(μ-H)Ru complex was unequivocally determined by neutron diffraction analysis, and it comes closest to an effective analog for the core structure of the proposed active form of the enzyme.

Hydrogenases are bacterial enzymes that catalyze the activation of H2 into two protons (H+) and two electrons (e) (13). Hydrogen isotope exchange experiments implicate as a first step the heterolytic cleavage of H2 into a proton and a hydride ion (H) (13). Hydrogenases are classified into two major families on the basis of the metal content of their respective dinuclear active sites—that is, [FeFe]hydrogenases (4) and [NiFe]hydrogenases (5, 6). Recent progress toward the structures and function of the hydrogenases has been provided by x-ray analysis, spectroscopic techniques, theoretical methods, and model studies (7).

X-ray crystallographic studies have shown that the resting-state core structure of [NiFe]hydrogenase from Desulfovibrio gigas consists of one nickel atom and one iron atom, which are bridged by two cysteic thiolates and one unidentified ligand (depicted as X in Fig. 1) (2, 5, 6). The bridging ligand X in the resting state is proposed to be an oxygen ligand such as H2O, OH, or O2– (8). The role of metal atoms and bridging S and X ligands in the H2 cleavage has so far been the subject of controversy (8).

Fig. 1.

Core structure of the resting form of [NiFe]hydrogenase from D. gigas, determined by x-ray analysis. [Adapted from (6)]

Many synthetic modeling efforts have been devoted to elucidating the core structure of the active form of the [NiFe]hydrogenase, such as preparation of [NiRu]complexes by Rauchfuss and others (915). A Ni(μ-S)2(μ-H)Fe species is one of the candidates for the active form (1, 5, 16, 17). However, 10M(μ-S)2(μ-H)8M complexes [where 10M = group 10 metals (Ni, Pd, and Pt) and 8M= group 8 metals (Fe, Ru, and Os)] as models for the active form of the [NiFe]hydrogenase have yet to be reported.

Here, we report the successful isolation and crystal structure of the paramagnetic Ni(μ-H)Ru complex [(NiIIL)(H2O)(μ-H)RuII6-C6Me6)](NO3) {[2](NO3)}, where L = N,N′-dimethyl-N,N′-bis(2-mercaptoethyl)-1,3-propanediamine, which we synthesized by reaction of a diamagnetic dinuclear NiRu aqua complex [(NiIIL)RuII(H2O) (η6-C6Me6)](NO3)2 {[1](NO3)2} with H2 in water under ambient conditions (20°C and 0.1 MPa) (Fig. 2).

Fig. 2.

Formation of a Ni(μ-H)Ru complex obtained from the reaction of a NiRu aqua complex with dihydrogen (H2) in water under ambient conditions (20°C and 0.1 MPa).

We obtained the highly water-soluble NiRu aqua complex [1](SO4) by reaction of the ruthenium triaqua complex [Ru(η6-C6Me6)(H2O)3](SO4) {[3](SO4)} (18) with the nickel complex [NiIIL] [4] (19) in aqueous solution (20). Complex [1]2+ was characterized by nuclear magnetic resonance (NMR) (figs. S1 to S3) and infrared (IR) spectroscopy (fig. S4), as well as by electrospray mass ionization spectrometry (ESI-MS) (figs. S5 to S7) and x-ray photoelectron spectroscopy (XPS) (fig. S8, A and C). Magnetic susceptibility measurements confirmed that the complex was diamagnetic (fig. S9A). The solid state structure of [1]2+ was characterized by x-ray diffraction from a red crystal of [1](OTf)2 (where OTf = CF3SO3), obtained from an aqueous solution of [1](OTf)2, prepared by an anion exchange [1](SO4) with NaOTf in water (fig. S10). A variety of anions (such as SO42–, OTf, or NO3) were investigated with regard to their ability to induce isolation of the complexes as crystals (fig. S11). The Ni center of [1](OTf)2 sits in the pocket of the tetradentate ligand in a square planar arrangement (fig. S10). The Ru1–O1 (aqua ligand) bond length is 2.154 ± 0.003 Å (where 0.003 is SD), whereas the Ni1···O1 distance is 2.858 ± 0.003 Å. (Further parameters are given in tables S1 and S2.)

The dinuclear NiRu aqua complex [1](NO3)2 was quantitatively obtained from anion exchange of [1](SO4) in water at approximately pH 7 (fig. S11). H2 (0.1 MPa) was bubbled through the phosphate buffer solution (pH 6.8) of [1](NO3)2 at 25°C to gradually precipitate dark-red crystals of [2](NO3), which were isolated by filtration {34% isolated yield based on [1](NO3)2}. As the reaction progressed (without the addition of the phosphate buffer), the pH of the solution steadily decreased (from pH 6.4 to pH 4.6), indicating the heterolytic H2 cleavage (21), which generated H+ as a co-product. The H2O ligand of [1](NO3)2 may act as a base to release H3O+ (H2 + H2O → H + H3O+) (22). We characterized [2](NO3) by IR (fig. S12), ESI-MS (fig. S13), XPS (fig. S8, B and D), NMR (fig. S14), electron spin resonance (ESR) spectroscopy (fig. S15), and magnetic susceptibility measurements (fig. S9B).

Dark-red crystals of [2](NO3) obtained from the aqueous solution of [2](NO3) were characterized by x-ray (fig. S16) as well as neutron diffraction analysis, the latter chosen for its sensitivity to hydrides (Fig. 3 and fig. S17). The Ru–H distance (1.676 ± 0.008 Å by neutron diffraction analysis) in the Ni(μ-H)Ru moiety of [2](NO3) is substantially shorter than the Ru–H distances (averaging 1.755 Å by neutron diffraction analysis) in the Ru(μ-H)Ru moiety of [{(η5-C5H3)2(SiMe2)2}]Ru2(CO)4(μ-H)](BF4) with a bulky dimethylsilyl linker (23). The Ni atom of [2](NO3) adopts a distorted octahedral coordination geometry with the tetradentate ligand, one aqua ligand, and one hydrido ligand (Fig. 3). The bridging H atom is closer to the Ru atom (Ru–H = 1.676 ± 0.008 Å, Ni–H = 1.859 ± 0.007 Å) in the Ni(μ-H)Ru moiety. The Ru–H unit may serve as a two-electron donor to the Ni unit through the bridging H atom (24), much as in M(μ-H)B complexes (where M is a transition metal), in which the B–H unit acts as a two-electron donor to M (25). In this context, there are three examples of hexacoordinate Ni(μ-H)B complexes with S ligands whose structures have been determined by x-ray analysis (Ni–H = 1.83 to 1.98 Å) (2628). The Ni–S–Ru angles (70.7° ± 0.3° and 70.4° ± 0.2°) for [2](NO3) are substantially smaller than the Ni–S–Ru angles (86.81° ± 0.04° and 87.20° ± 0.05°) for [1](NO3)2. The tunable Ni–S–Ru angles allow such structural changes in these dinuclear complexes. The Ni···Ru distance (2.739 ± 0.003 Å) of [2](NO3) is shorter than that (3.1611 ± 0.0006 Å) of [1](OTf)2. A similar tendency has been observed in the [NiFe]hydrogenase; i.e., extended x-ray absorption fine-structure studies on the [NiFe]hydrogenase have shown that the Ni···Fe distance in the active form is 2.512 ± 0.007 Å, which is shorter than the Ni···Fe distance (2.906 ± 0.014 Å) in the resting form (29).

Fig. 3.

Structure of [2](NO3) as determined by neutron diffraction analysis. The ellipsoids are cut open to reveal the three principal axes and are drawn to include 30% probability density. Selected bond lengths (l/Å) and angles (ϕ/deg): Ni1–H1, 1.859 ± 0.007; Ni1–O1, 2.122 ± 0.005; Ni1–S1, 2.359 ± 0.010; Ni1–S2, 2.362 ± 0.009; Ni1–N1, 2.119 ± 0.003; Ni1–N2, 2.117 ± 0.004; Ru1–H1, 1.676 ± 0.008; Ru1–S1, 2.375 ± 0.011; Ru1–S2, 2.388 ± 0.007; Ni1–H1–Ru1, 101.47 ± 0.043; Ni1–S1–Ru1, 70.7 ± 0.3; and Ni1–S2–Ru1, 70.4 ± 0.2.

A positive-ion ESI mass spectrum of [2](NO3) in H2O is consistent with the above formulation and dinuclearity (fig. S13). A prominent signal at a mass-to-charge ratio (m/z) of 543.2 [relative intensity = 100% in the m/z range from 200 to 1000] has a characteristic distribution of isotopomers that matches well with the calculated isotopic distribution for [2-H2O]+. To confirm the origin of the hydrido ligand of [2](NO3), we synthesized D-labeled [2](NO3) by reaction of [1](NO3)2 with D2 in H2O for 10 min. In ESI mass spectra, the signal at m/z 543.2 shifts to 544.2 (fig. S18). This result indicates that the deuterium atom is incorporated into [2](NO3). We have confirmed that there is no H/D exchange between D2 and H2O under the conditions of this experiment (at pH 7 to 9 in H2O for 1 hour at 25°C at 0.1 MPa of D2). An IR spectrum of [2](NO3) in the region of 1000 to 2000 cm–1 shows a peak shift from 1740 to 1248 cm–1 after isotopic substitution of H by D in the hydrido ligand position. Magnetic susceptibility measurements of [2](NO3) yield χM = 1.5×10–3 electromagnetic units (emu) mol–1 at 300 K, corresponding to a magnetic moment of 2.32 BM. 1H NMR and ESR measurements also indicate paramagnetism in [2](NO3). The reason for paramagnetism is explained on the basis of the transformation of the nickel(II) spin state between a singlet (S = 0) square planar of [1]2+ and a triplet (S = 1) pseudo-octahedral of [2]+, triggered by the coordination of H and H2O to the nickel ion. Complex [2](NO3) is one of a few examples of stable paramagnetic metal hydride complexes (30). The binding energy of Ni 2p3/2 for XPS of [2](NO3) indicates that a Ni atom has a similar charge (883.2 eV) to that of [1](OTf)2 (882.9 eV), which corresponds to a Ni(II) species.

Previous studies of dinuclear transition metal complexes with two bridging sulfido ligands, M(μ-S)2M (where M = Ru or Ir), that activate H2 to give M(μ-S)2(μ-H)M species have been reported (31, 32). However, in those reported studies, the reactions have been carried out in organic solvent such as toluene. We attached an aqua ligand to the Ni(μ-S)2Ru unit not only to gain water solubility but also to act as a base to form the Ni(μ-S)2(μ-H)Ru species in water, because we assumed that the hydrogenases require the X ligand (H2O, OH, or O2–) in the resting state to activate H2 in aqueous media in the same manner of this study.

Supporting Online Material

Materials and Methods

Figs. S1 to S18

Tables S1 and S2


References and Notes

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