Sulfur-Supported Iron Complexes for Understanding N₂ Reduction

Abstract

This chapter focuses on the use of synthetic complexes for modeling iron sites in the iron-molybdenum nitrogenase enzyme, particularly on those with sulfur donors in the coordination sphere. This is an under-explored area that has promise to elucidate the way that Fe–S bonds contribute to N₂ binding and activation. We review iron complexes with sulfide, thiolate, and thioether-containing supporting ligands and discuss the binding of N₂ as well as reduced species such as hydrazine and diazene. The structures, spectroscopy, reactions, and other properties of key complexes are described, including recent results.

1 N₂ Reduction in Biological Systems

Nitrogen atoms are essential building blocks of biomacromolecules. Although atmospheric dinitrogen is a plentiful source of N atoms, N₂ is relatively inert and only specialized organisms are capable of “fixing” N₂ to a bioavailable form such as ammonia or nitrate [1]. In these nitrogen-processing (“diazotrophic”) bacteria and archaea, biological nitrogen fixation is catalyzed by nitrogenase enzymes according to the overall idealized reaction stoichiometry [2]:

$${\mathrm{N}}_2+8{\mathrm{H}}^{+}+8{\mathrm{e}}^{-}+16\mathrm{ATP}➔2{\mathrm{NH}}_3+{\mathrm{H}}_2+16\mathrm{ADP}+16\text{phosphate}$$

Nitrogenase enzymes are complicated multicomponent systems, and the reader may look elsewhere for detailed descriptions of their enzymology [3,4,5]. Here, we focus on the inorganic chemistry at the N₂-binding cofactors, which are metalloclusters called the FeMoco (in molybdenum-dependent nitrogenases), the FeVco (in vanadium-dependent nitrogenases), or the FeFeco (in iron-only nitrogenases). Thus far, the only structurally characterized one of these cofactors is the FeMoco, which is an unusual [Fe₇MoS₉C] cluster (Fig. 1). In alternative nitrogenases, the molybdenum center is replaced by vanadium or iron, but the overall shape of the cofactor is thought to be similar [6, 7]. Based on the shared reactivity of all nitrogenase variants, as well as mutagenesis studies that show loss of N₂ reduction ability upon mutation of His¹⁹⁵ and Val⁷⁰ (Fig. 1; numbering is for Azotobacter vinelandii FeMo-nitrogenase), the central iron atoms are most strongly implicated as the site of N₂ binding [8].

Fig. 1

Structure of the resting state of the FeMoco. (Top) Crystal structure of the FeMoco (PDB ID 4TKU) shown with key residues near the active site. (Bottom) The proposed oxidation state assignments for the iron and molybdenum ions based on spatially resolved anomalous dispersion refinement [9] and Mo K-edge X-ray absorption spectroscopy [10], respectively

Given the importance of nitrogenases in the global nitrogen cycle, and the prospect of unusual chemistry at the FeMoco, the mechanism of nitrogen reduction in the molybdenum-dependent nitrogenases has been a topic of great interest in the bioinorganic chemistry community. Substantial recent advances on the mechanism of N₂ reduction by the FeMoco come from pulsed EPR studies on trapped intermediates from Seefeldt, Hoffman, Dean, and coworkers [5, 11,12,13,14]. They have constructed models that are based on the Lowe–Thorneley kinetic scheme [2, 15], which specifies that from the resting state (E₀), four electrons and four protons are added to give the intermediate E₄, which is the state that binds N₂. Electron-nuclear double resonance (ENDOR) studies indicate that E₄ has two hydrides bridging between iron centers, implying that the other two H atoms are probably protonated sulfides [16,17,18]. According to the Lowe–Thorneley model, the reversible reductive elimination of H₂ is accompanied by N₂ binding to iron [15]. Seefeldt and Hoffman propose that the bound N₂ is immediately converted to a species at the diazene redox level, although the steps in this transformation and the structure of the resulting “N₂H₂” species are not clear. The sites of subsequent protonation are also unclear, but the possibilities are typically categorized as distal and alternating (see Fig. 2). In the distal pathway, proposed by analogy to small molecule molybdenum complexes [19, 20], the first molecule of ammonia is released following three protonations at the distal nitrogen. This results in the formation of a nitride that can accept three more protons and electrons to release a second equivalent of ammonia. In the alternating pathway, each N atom is protonated in turn to eventually yield a hydrazine species that undergoes N–N bond cleavage. The alternating mechanism has generally been favored for the FeMoco on the basis that diazene and hydrazine (which are intermediates unique to the alternating pathway) are also nitrogenase substrates, and that hydrazine is released from the enzyme during turnover under some conditions [5]. Although species following N–N cleavage (which are common to both the alternating and distal pathways) have been trapped and characterized by pulsed EPR [5], no intermediate that is unique to the distal or alternating pathway has been observed in the FeMoco. Furthermore, a recent study of a model complex suggests that crossover between intermediates in the distal and alternating pathways should also be considered [21]. Within each limiting mechanism, there are additional ambiguities to be resolved because the intermediates may be terminally bound or bridging between metal centers, and their coordination modes could change throughout the catalytic cycle. Thus, many questions remain about the mechanism of NH₃ formation, even in the best-understood nitrogenase.

Fig. 2

Distal and alternating pathways for N₂ reduction. Although all intermediates are drawn as terminally coordinated, bridging coordination modes are also plausible

Only the resting state of the FeMoco has been structurally characterized. Rearrangement of synthetic iron–sulfur clusters upon ligand binding or redox changes is known [22,23,24], and therefore it is reasonable to predict that internal bond cleavage might occur upon reduction and N₂ binding in the FeMoco. Additional evidence for this hypothesis comes from experimental studies of nitrogenase. For example, in the crystal structure of the CO-inhibited form of nitrogenase, one of the central bridging sulfides (S2B; see Fig. 1) is replaced by CO [25]. When CO is removed and the enzyme is exposed to catalytic conditions, the bridging sulfide is reincorporated and the enzyme regains full activity. In another example, Rees and coworkers replaced S2B with a selenide. Crystallographic studies demonstrated that the selenide migrates to the other central “belt” sites and is eventually extruded from the active site (with reincorporation of a sulfide) during acetylene reduction [26]. The fate of the released S²⁻ or Se²⁻ and the mechanism of the exchange processes in these experiments are not yet clear. Nevertheless, these studies demonstrate that sulfide dissociation and cluster rearrangement certainly can occur during turnover. However, ¹³C and ¹⁴C labeling studies confirm that the central carbide does not exchange during reduction of C₂H₂, CO, or N₂ [27].

Given the uncertainty surrounding the mechanism of nitrogenase and its structure during turnover, many different intermediates could be postulated. A wide variety of mechanistic steps have been proposed based on DFT calculations [28,29,30,31,32,33,34,35,36,37,38,39]. Synthetic model compounds have been used to test the feasibility of some of these proposed chemical transformations. Iron complexes that cleave N₂ [40,41,42,43] as well as iron complexes that catalytically reduce N₂ to ammonia and/or silylamine [44,45,46,47,48,49] have been reported. However, these compounds and others that bind N₂ and/or partially reduced N₂ species (N _x H _y ; x = 1–2, y = 1–4) typically contain phosphorus, nitrogen, and/or carbon donors and it is unclear what effects these abiological ligands have on catalysis. Nitrogenase-relevant compounds with these types of ligand frameworks have been reviewed elsewhere [20, 50,51,52,53,54,55,56].

Iron complexes with sulfur supporting ligands that bind N _x H _y fragments can give distinctive insight into the reactivity patterns that can be expected in the FeMoco [57]. As shown in the examples below, the sulfur donors may serve as functional models for sulfides, for example, by facilitating proton delivery or by stabilizing N _x H _y species through hydrogen bonding interactions. Furthermore, these complexes can replicate the weak ligand field, the low coordination number, and the high-spin electronic configuration of the iron sites in the FeMoco. Complexes containing sulfides are the most relevant to nitrogenase, but more often thiolates are used as anionic donors. A number of iron complexes with thioether ligands, which model protonated sulfides in nitrogenases, are also known. Here, we discuss these iron complexes with sulfur-containing ligands that bind N₂ and N _x H _y fragments in the context of nitrogenase modeling.

2 Fe–N₂ Complexes with S Ligands

A variety of coordination modes have been proposed for N₂ in the FeMoco [30, 33, 58]. These include bridging, terminal, and side-on coordination, in some cases involving rearrangement of the cofactor. Model complexes can illustrate the plausibility of N₂ binding in these coordination modes in a sulfur-rich coordination environment.

The interaction of N₂ with transition metals consists primarily of π-backbonding from filled iron d-orbitals into the empty π* orbitals of N₂, which results in a weakening of the N–N triple bond [50, 59]. The deviation of the N–N bond length and/or N–N stretching frequency from the values for free N₂ can be used as measures of the degree of activation of the N–N bond. The parameters for structurally characterized N₂ complexes with sulfur supporting ligands are given in Table 1. These complexes, along with other species that can be shown by reactivity or spectroscopic studies to bind N₂, are discussed below.

Table 1 Key bond lengths and N≡N stretching frequencies of N₂ complexes with sulfur donors

2.1 N₂ Complexes with Thioether-Containing Ligands

The first structurally characterized iron–N₂ complex with any type of sulfur donor was the tetrahydrothiophene (THT) adduct of the complex [Fe(^iPrPDI)(N₂)] (1) [61] (Fig. 3). Peters and coworkers later reported a set of thioether derivatives of the complex [Fe(SiP^iPr)₃(N₂)]⁺ (2) [62, 63]. When a thioether was incorporated in place of one of the phosphine ligands in 2, the complex was still able to bind N₂, although the replacement of the phosphine with thioether made the N₂ more labile and slightly less activated, as demonstrated by the increase in ν _NN from 2,143 cm⁻¹ in the parent complex 2 to 2,156 cm⁻¹ in 3. When a second phosphine was replaced with a thioether, N₂ binding was no longer observed. Addition of a hydride led to N₂ binding to both the mono and bis(thioether) complexes and a more activated N₂ ligand as compared to analogous complexes without a hydride ligand, as shown by the 101 cm⁻¹ decrease in ν _NN in 4 (ν _NN = 2,055 cm⁻¹) as compared to 3. The formation of hydrides could play a similar role in promoting N₂ binding and activation in the FeMoco. Although it could not be crystallographically characterized, the mixed-valence iron(I)/iron(II) bridging N₂ complex 6 was also accessible via treatment of the solvent adduct [Fe(SiP^iPrS^Ad ₂)(Et₂O)]⁺ with 0.5 equivalents of CrCp₂ or CoCp₂. Complex 6 exhibits an N–N stretching vibration at 1,881 cm⁻¹, significantly lower than any of the monometallic complexes with this ligand, which illustrates how N₂ binding and activation could be facilitated by multimetallic cooperativity [66].

Fig. 3

N₂ complexes with thioether-containing ligands. Ad = adamantyl

2.2 N₂ Complexes with Thiolate Ligands

There are also examples of thiolate complexes with N₂ ligands. Peters and coworkers generated a series of thiolate-bridged terminal N₂ complexes in three different oxidation states (7–9) [64] (Fig. 4). Terminal hydride analogs of complexes 8 and 9 (10 and 11) were also reported. Complex 9 catalyzed low turnovers of NH₃ formation from N₂ but was much more effective for hydrazine disproportionation into NH₃ and N₂. Interestingly, under the same conditions the analogous monometallic complex 3 did not perform either of these reactions efficiently, suggesting that the thiolate plays an important role in catalysis, perhaps by allowing cooperativity between the iron centers and/or acting as a proton shuttle during turnover.

Fig. 4

N₂ complexes incorporating a bridging thiolate

In complexes 3–11, N₂ binding is in part promoted by the presence of phosphine ligands. More recently, it has been possible to observe N₂ binding using a supporting ligand that contains only sulfur and carbon donors [65]. Reduction of the tris(thiolate) complex 12 yielded the terminal N₂ complex 13, in which the iron center is coordinated to two thiolates and has an η² interaction with the central arene ring (Fig. 5), which models a potential S₂C donor set in the FeMoco. The observation of Fe–S bond cleavage upon reduction and N₂ binding shows that dissociation of a sulfide is a chemically reasonable step for N₂ binding and activation in the FeMoco. The relatively low ν _NN of this complex (1,880 cm⁻¹) is indicative of an N₂ unit that is quite weakened, despite the high-spin electronic configuration of the complex. This demonstrates that a low-coordinate iron center with weak-field ligands can lead to substantial weakening of N₂ and suggests that the electron-rich thiolates lead to strong backbonding.

Fig. 5

N₂ binding to an iron site containing exclusively sulfur and carbon donors. Ar = 2,4,6-triisopropylphenyl

2.3 Interaction of N₂ with Iron–Sulfide Clusters

The study of synthetic iron–sulfur clusters in the context of nitrogenase has also been the topic of a significant body of work [22,23,24, 67, 68]. Although there are no structurally characterized iron–sulfur clusters with bound N₂ ligands, catalytic and spectroscopic studies have demonstrated that N₂ can bind to synthetic iron–sulfur clusters. Electrochemical reduction of N₂ to NH₃ is catalyzed by [Fe₄S₄(SPh)₄]²⁻ and [Mo₂Fe₆S₈(SPh)₉]³⁻ clusters, albeit with very low Faradaic efficiency [69]. More recently, the photochemical conversion of N₂ to NH₃ by chalcogenide aerogels (chalcogels) containing Mo₂Fe₆S₈(SPh)₃ and Fe₄S₄ clusters has been reported [70, 71]. Using infrared spectroscopy, N–N stretching bands were observed at 1,746 and 1,753 cm⁻¹ upon irradiation of these chalcogels with visible light under N₂ atmosphere. The N–N stretching frequencies are even lower than the S₂C supported complex above and are indicative of some form of reduced N₂ species, but the redox and protonation state of this species are not known. Nevertheless, these data provide evidence for the formation of a cluster-bound N _x H _y species during turnover. N₂ binding to Fe₂S₂ ⁺, Fe₃S₃ ⁺, and Fe₄S₄ ⁺ clusters in the gas phase has also been observed by mass spectrometry in ion-trapping experiments [72]. The structures of the N₂ adducts are not known experimentally but were suggested from DFT calculations.

Finally, in a recent study, a diferrous iron sulfide hydride complex with a β-diketiminate coligand was reduced under N₂ to give a diiron(0) N₂ complex in 24% spectroscopic yield [73]. Gas chromatography indicates that H₂ is produced during this process. The reactivity of this complex thus models the E₄ state of the FeMoco, in which H₂ loss from an iron hydride sulfide core results in N₂ binding [14, 74,75,76]. However, in the model complex the H₂ production results from a bimolecular reaction, the N₂-containing product did not also contain a sulfide, and mechanistic studies of the reaction leading to sulfide extrusion and N₂ binding were precluded by the presence of a significant number of unidentified byproducts in the reaction mixture.

3 Fe Complexes with N _x H _y Ligands

There are no examples of N₂ functionalization giving a well-defined N _x H _y complex for iron complexes with sulfur supporting ligands. However, a number of diazene (HN=NH) and hydrazine (NH₂–NH₂) complexes are known with sulfur-based supporting ligands, as are alkyl- or aryl-substituted diazene and hydrazine derivatives. Generation of the hydrazine species typically proceeds in a straightforward manner by addition of hydrazine to precursor complexes. In some cases, hydrazine addition instead results in isolable diazene complexes accompanied by formation of amines, implying that the diazene was generated via hydrazine disproportionation. The generation of diazene complexes via direct addition of diazene to a precursor is more problematic because diazene is unstable in solution [77,78,79], but there are examples where diazene is generated and trapped in situ by iron complexes. Isolated diazene complexes are most commonly synthesized by hydrazine disproportionation or by oxidation of corresponding hydrazine species. In this section, we discuss the generation, structural characterization, and reactivity of these N _x H _y compounds.

3.1 N _x H _y Complexes with Iron–Sulfide Clusters

An early report demonstrated that the electrochemical reduction of hydrazine is catalyzed with high Faradaic efficiency by [Fe₄S₄(SPh)₄]²⁻ and [Mo₂Fe₆S₈(SPh)₉]³⁻ clusters, but the mechanism of NH₃ formation was not examined [80]. Chemical reduction of vanadium- and molybdenum-containing iron–sulfur cubanes also generates ammonia from hydrazine, but in all of these cases the V or Mo centers were implicated as the sites of hydrazine binding and reduction [81,82,83,84,85,86,87,88,89].

The only examples of structurally characterized iron N _x H _y complexes incorporating sulfides are the β-diketiminate supported complexes 14–16 [90, 91] (Fig. 6). Reaction of the diferrous monosulfide-bridged precursor with ammonia, methylhydrazine, or 1,1-dimethylhydrazine yielded 2:1 complexes in which one of the N-donors is bound to each iron center (14). In contrast, reaction with the parent hydrazine yielded complex 15 in which an N₂H₄ ligand bridges between the iron centers. Treatment of the diferrous precursor with 1.5 equivalents of phenylhydrazine resulted in the formation of the mixed-valence iron(II)/iron(III) phenylhydrazido-bridged complex 16 via the overall reaction:

$$2{\mathrm{LFe}}^{\mathrm{II}}\left(\mathrm{\mu }-\mathrm{S}\right){\mathrm{LFe}}^{\mathrm{II}}+3\text{PhNH}-{\mathrm{NH}}_2➔2\mathbf{16}+{\text{PhNH}}_2+{\mathrm{NH}}_3$$

Fig. 6

Sulfide-bridged β-diketiminate complexes with nitrogenase-relevant N _x H _y fragments. Ar = 2,6-diisopropylphenyl

This reactivity demonstrates that sulfide-bridged iron centers are capable of N–N bond cleavage. The phenylhydrazido species 16 was also the subject of a detailed ENDOR study, which enabled the first determination of the hyperfine coupling parameters of a well-defined bridging hydrazido species that could be compared to the ENDOR parameters of nitrogenase intermediates [92].

3.2 N _x H _y Complexes with Thioether/Thiolate Ligands

Sellmann and coworkers reported a series of complexes with supporting ligands containing two thiolate donors with additional thioether, amine, and/or pyridine groups [93,94,95]. Of particular note are several trans diazene complexes (two representative examples are shown in Fig. 7), which were generated either by air oxidation of a corresponding hydrazine species [96, 97] or by trapping of diazene generated in situ from potassium azodicarboxylate or benzenesulfonic acid hydrazide [98, 99]. In these complexes, the diazene ligand bridges between two iron centers, with the protons of the diazene forming one long (~2.8 Å) and one short (~2.2 Å) hydrogen bond to the thiolate moieties of the supporting ligand [96, 97, 99]. DFT calculations suggest that the strong hydrogen-bonding interaction contributes significantly to the overall stability of the complex [100, 101]. The sulfides in the FeMoco, as well as adjacent amino acids, may play a similar role in stabilizing intermediates during N₂ reduction. A further contribution to the stability of these complexes arises from the strong π-backbonding interaction between the iron center and the diazene ligand, as demonstrated by their intense blue color that arises from an iron to diazene charge transfer transition [102, 103]. This interaction leads to slight weakening of the N–N bond as compared to free diazene: for example, in complex 17, the N–N bond length [96] is 1.301(5) Å compared to 1.252 Å in free diazene [104]. The N–N stretching frequency is 1,382 cm⁻¹ [103], which falls between the values for free diazene (ν _NN = 1,529 cm⁻¹ [105]) and free hydrazine (ν _NN = 876 cm⁻¹ [106]). Using normal coordinate analysis, Lehnert and coworkers determined an N–N bond order of 1.6 for this complex indicating partial reduction to a hydrazido(2−) species [103]. SCF-Xα-SW calculations indicated that the LUMO of this complex consists primarily of a diazene π* orbital, which implies that reduction of the complex should further weaken the N–N bond of the diazene moiety [102]. However, in practice the reduction occurred at an extremely negative potential and led instead to decomposition of the complex.

Fig. 7

Structure of diazene-bridged complexes 17 and 18

Although structurally characterized monometallic iron complexes that bind hydrazine [107,108,109] and ammonia [107] are also known in these systems, a corresponding N₂ species could not be generated. Interestingly, however, oxidation of the diazene complex 18 with two equivalents of ferrocenium at −78 °C caused a color change from blue to purple [110, 111]. Since the HOMO of complex 18 is primarily an iron orbital [102], this oxidation was expected to result in the formation of a diferric diazene species. Warming the purple oxidized species above −40 °C resulted in N₂ evolution and formation of a green ferrous product. This implies that the purple species may be a ferrous N₂ complex, which is a valence tautomer of the expected diferric diazene complex (Fig. 8). This process would model the reverse of N₂ binding in the FeMoco and illustrate how sulfides could facilitate proton transfer. Unfortunately, the instability of the purple oxidized species prevented further characterization and its identity remains unclear.

Fig. 8

Two-electron oxidation of diazene complex 18, with the presumed product shown in two tautomeric forms: a diferric diazene complex and a diferrous dinitrogen adduct. The supporting ligands have been omitted for clarity

3.3 N _x H _y Complexes with Thiolate Ligands

Other complexes containing thiolate donors are also known to bind N₂H₄ and NH₃. In these systems, like those described above, the hydrazine ligands often form extensive hydrogen-bonding networks with the thiolates and/or solvents of crystallization. For example, Sellmann and coworkers crystallized iron bis(benzenedithiolate) complexes with hydrazine bound in bridging [112] and terminal [113] coordination modes. The terminal complex in particular contains an extensive hydrogen-bonding network between the metal-bound hydrazine and N₂H₄ and N₂H₅ molecules in the crystal lattice.

Upon reaction of the sterically hindered thiolate-bridged dimer Fe₂(μ-STriph)₂(STriph)₂ (STriph = 2,4,6-triphenylbenzenethiolate) with hydrazine, rearrangement to the hydrazine-bridged dimer Fe₂(μ-N₂H₂)₂(N₂H₂)₂(STriph)₄ (19) was observed [114] (Fig. 9). The precursor complex Fe₂(μ-STriph)₂(STriph)₂ also reacted with amines to yield mono- and bimetallic coordination compounds and was observed to catalyze the disproportionation of 1,2-diphenylhydrazine to aniline and azobenzene (PhN=NPh). Complex 20 also coordinates ammonia and hydrazine [115]. The NH₃ and N₂H₄ ligands in 20 are labile in solution but are stabilized in the solid state by hydrogen-bonding interactions to solvent molecules. This complex catalyzes hydrazine reduction, but the number of turnovers is low and no intermediates could be observed during the reaction.

Fig. 9

Complexes generated by the addition of hydrazines to iron precursors with sterically bulky thiolate ligands

Hydrazine cleavage at iron sites has also been observed in other systems. A series of ferric iron-imide heterocubanes (21) were generated by the reaction of ferrous complexes containing sterically hindered thiolate ligands with 1,2-diarylhydrazines [116, 117]. The mechanism of the N–N bond cleavage step leading to imide formation is not clear but was proposed to occur through formation of a diferrous complex containing an arylhydrazine bound in a μ-η²:η² fashion, followed by electron transfer from the ferrous centers to the hydrazine resulting in N–N bond cleavage. A similar reaction leading to N–N bond cleavage and formation of a bridging imide could be envisioned in the FeMoco. Note that these cubane structures were obtained only with sterically hindered thiolates and 1,2-diarylhydrazines; all other substrates gave mixtures of products. In a different set of studies, iron-imide-sulfide heterocubanes were also structurally and spectroscopically characterized [118, 119].

3.4 N _x H _y Complexes with Thiolate and Cp Ligands

Several complexes incorporating thiolate and Cp donors are also known to catalyze the N–N bond cleavage of hydrazines. Qu and coworkers reported that alkylthiolate-bridged iron complexes react with hydrazines to form cis diazene complexes (22) [120, 121]:

$$2\left[{\mathrm{Cp}}^{\ast }{\mathrm{Fe}}^{\mathrm{I}}{\left(\mathrm{\mu }-{\mathrm{R}}^1\mathrm{SEt}\right)}_3{\mathrm{Fe}}^{\mathrm{II}}{\mathrm{Cp}}^{\ast }\right]+3{\mathrm{R}}^2\mathrm{NH}-{\mathrm{NH}}_2➔2\left[{\mathrm{Cp}}^{\ast }{\mathrm{Fe}}^{\mathrm{II}}{\left(\mathrm{\mu }-{\mathrm{R}}^1\mathrm{SEt}\right)}_2\left(\mathrm{\mu }-{\mathrm{N}}_2{\mathrm{R}}^2\mathrm{H}\right){\mathrm{Fe}}^{\mathrm{II}}{\mathrm{Cp}}^{\ast }\right]\left(\mathbf{22}\right)+{\mathrm{R}}^2{\mathrm{NH}}_2+{\mathrm{NH}}_3+2{\mathrm{HSR}}^1$$

In the presence of reductant and acid, these compounds catalytically cleave the N–N bond of various alkyl- and aryl-substituted hydrazines. No intermediates could be detected in this reaction, but DFT calculations suggested that protonation and reduction of diazene involves isomerization to a (μ-NH)-NH₂ species [122]. The strong donation of the thiolates and their ability to shift coordination mode are thought to be important in allowing this isomerization to occur. Nishibayashi and coworkers reported a similar system containing an ortho-substituted aryl thiolate in which a methyldiazene (CH₃–N=NH) or methyldiazenido (N=NCH₃ ⁻) moiety is bound side-on between two iron centers (23–24) [123] (Fig. 10). In this case, the bridging structure was important for promoting selective hydrazine cleavage; a corresponding monomeric complex promoted H₂ formation rather than NH₃ production. Again, however, the mechanism of N–N bond cleavage was not clear and the key hydrazido (R₂N-NR⁻) intermediate could not be detected.

Fig. 10

Structures of Cp-supported thiolate-bridged diazene complexes reported by Qu and Nishibayashi

In another system, Qu and coworkers studied the generation of ammonia from treatment of a benzenedithiolate-bridged diiron complex with hydrazine [124]. Several intermediates along the pathway to NH₃ release were accessible via stepwise protonation and/or reduction. Starting from a diferrous complex with cis-diazene bound μ-η¹:η¹ between the iron centers (25), protonation led to electron transfer from the iron centers to the diazene ligand and rearrangement to afford a diferric complex in which a hydrazido (N₂H₃ ⁻) ligand is bound asymmetrically in a μ-η¹:η² fashion (26). The bridging benzenedithiolate ligand also rearranged to a μ-η¹:η² coordination mode, which resembles the hypothesized rearrangement of sulfides in the FeMoco during turnover. Subsequent two-electron reduction and protonation of 26 resulted in ammonia release and formation of an amido-bridged diferrous complex (27). DFT calculations suggest that the ammonia comes from the non-bridging NH₂ of the hydrazido species via the mechanism shown in Fig. 11. Note that this process involves an NH–NH₃ intermediate that is not part of the traditional distal or alternating pathways but has been proposed for the FeMoco based on computational results [34]. The amido complex 27 also produces NH₃ upon further reduction and protonation, although the yield is low due to competitive proton reduction.

Fig. 11

Proposed mechanism of NH₃ release leading to the formation of 27 upon protonation and reduction of 25 via 26. Of the complexes shown in this figure, only 26 and 27 are structurally characterized, although the structure of 25 (which is an isolable species) can be inferred based on the structure of the analogous one-electron oxidized species. The sequence of protonation and electron transfer steps is proposed based on DFT calculations

4 Conclusions

The results presented above show the variety of synthetic strategies that have yielded N₂ and N _x H _y complexes of iron with sulfur-containing supporting ligands. It is becoming clear that the coordinative flexibility, electron-rich character, and hydrogen-bonding capability of sulfur atoms can influence the behavior of bound N₂ and N _x H _y coligands. Understanding the electronic structure and reactivity of these compounds has begun to provide insight into the possible role(s) of the sulfides in the FeMoco of nitrogenase.