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Electron and Hydride Transfer in a RedoxActive NiFe Hydride Complex: A DFT Study Miho Isegawa, Akhilesh K. Sharma, Seiji Ogo, and Keiji Morokuma ACS Catal., Just Accepted Manuscript • DOI: 10.1021/acscatal.8b02368 • Publication Date (Web): 28 Sep 2018 Downloaded from http://pubs.acs.org on September 28, 2018

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ACS Catalysis

Electron and Hydride Transfer in a Redox-Active NiFe Hydride Complex: A DFT Study Miho Isegawa,*† § Akhilesh K. Sharma,§ Seiji Ogo,*† Keiji Morokuma § †

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International Institute for Carbon-Neutral Energy Research (WPI-I CNER), Kyushu University, 744 Moto-oka, Nishi-ku, Fukuoka 819-0395, Japan

§

Fukui Institute for Fundamental Chemistry, Kyoto University, Kyoto 606-8103, Japan

ABSTRACT: We present mechanistic details of the formation of a NiFe hydride complex and provide information on its electron- and hydride- transfer processes based on density functional theory calculations and artificial-force-inducedreaction studies. The NiFe hydride complex conducts three transfer reactions, namely, electron transfer, hydride transfer, and proton transfer (Ogo et al. Science, 2013, 339, 682-684). In a NiFe hydride complex, the hydride binds to Fe, which is different from the Ni-R state in hydrogenase where the hydride locates between Ni and Fe. According to our calculations, in reaction with the ferrocenium ion, electron transfer occurs from the NiFe hydride complex to the ferrocenium ion, followed by a hydrogen-atom transfer (HAT) to the second ferrocenium ion. The oxidation state of Fe varies during the redox process, different from the case of NiFe hydrogenase where the oxidation state of Ni varies. A single-step hydride transfer occurs in the presence of a 10-methylacridinium ion (AcrH+), which is more kinetically feasible than the HAT process. In contrast to the HAT and hydride-transfer process, the proton transfer occurs barrierlessly from a protonated diethyl ether. The revealed reaction mechanism guides the interpretation of the catalytic cycle of NiFe hydrogenase and leads to the development of efficient biomimetic catalysts for H2 generation and an electron/hydride transfer. Keywords: H2 activation, redox reaction, hydride complex, electron transfer, hydride transfer, metal oxidation state, sustainable energy respectively corresponds to the Ni-SIa (NiIIFeII) and Ni-R 1. INTRODUCTION (NiIIμ(H)FeII) states in hydrogenase.7,8 The proposed Molecular hydrogen is a promising candidate for the catalytic cycle is given in Figure 1. First, H–H bond next generation of clean energy resource serving as an cleavage occurs with the help of a strong base (MeO–) alternative to fossil fuels that are finite and emit and the hydride complex (E1) is generated as a product. undesirable chemical compounds, such as CO2, NOx, The obtained hydride complex accomplishes electron and SOx into the environment. The development of transfer (ET), hydride transfer and proton transfer (PT) catalyst that can efficiently and selectively activate and as seen in hydrogenase. 9 ,10 generate hydrogen molecule is in great demand. Furthermore, the use of nonprecious metals such as Ni, Fe, and Mn and designing ligands for the metal complexes that are catalytically active in nontoxic solvents is crucial for industrial applications. It is known that the biological enzyme hydrogenase,1-3 which is found in cyanobacteria can catalyze the activation/generation of H2. Therefore, a great deal of effort has been devoted to synthesizing complexes mimicking the function and/or structure of the catalytic center of hydrogenase. These synthetic models have been well summarized in the recent reviews.4,5 A careful analysis by theoretical calculations of biomimetic models can give insights into the catalytic mechanism of hydrogenase and guide the development of efficient and robust biomimetic catalysts. Recently, Ogo et al.6,7,8 synthesized a biomimetic NiFe complex that performs the heterolytic H−H bond cleavage in a presence of a strong base, such as MeO– (Figure 1). The triethylphosphite ligand in the NiFe complex reduces the electron density of Fe and such an electron-deficient state is crucial for H2 binding as the hydrogen molecule weakly donates sigma electron(s) to the metal site. Two NiFe complexes have been trapped and experimentally characterized, namely the solventcoordinated complex (A1, [NiII(L)FeII(MeCN)[P(OEt)3]3], L = N,N'-diethyl-3,7-diazanonane-1,9-dithiolato) and hydride complex (E1, [NiII(L)(μ-H)FeII[P(OEt)3]3]), which

Figure 1. The proposed catalytic cycle for H2 activation and electron/hydride/proton transfer seen in the NiFe complex. Gastel and coworkers11 performed Mössbauer and computational studies on the present NiFe complex to elucidate the reaction mechanism of H2 activation and formation. They showed that both H2 activation and H2 formation occur barrierlessly, but the redox process due to electron and hydride transfers has not been investigated yet.

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In several mechanistic studies of NiFe hydrogenase, different redox states, arising from the transport of electrons via proximal iron–sulfur clusters, have been determined using spectroscopic techniques.12, 13, 14, 15-16 The next step of the study is to elucidate the transformation path among these different redox states.15 However, it is difficult to model this system, which includes both a NiFe catalytic center and proximal iron-sulfur clusters in a computational study. Thus, it is adequate to obtain mechanistic insights from a biomimetic model as an initial step. To understand the complicated redox process in hydrogenases,14,17 the experimentalists have synthesized a variety of biomimetic models including both catalytic center and cofactor which relate to the redox process in NiFe, Fe-Fe, Fe-only hydrogenases.18,19-20,21,22,23 Furthermore, theoretical calculations have been conducted to obtain the mechanistic insight for the redox processes.24, 25 In this study, we focus on the mechanistic details of electron/hydride transfer from a NiFe complex and the corresponding changes in the redox states. Furthermore, we examine the correspondence of redox states in the biomimetic NiFe complex and those in NiFe hydrogenase with a clarification of the oxidation states of Ni and Fe. We also review the mechanism of H2 activation/evolution in a NiFe model complex. The plausible reaction paths are determined based on both thermodynamics and kinetics, where the artificialforce-induced-reaction (AFIR) technique26 is applied to determine the transition states (TSs). The method has been applied to a variety of chemical processes to know the reaction mechanisms in our previous studies.27,28-29, 30,

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Vibrational frequency calculations were performed at the same level of theory to confirm all stationary points; minima (i.e. no imaginary frequencies) and TSs (i.e. one imaginary frequency), and to obtain zero-point vibrational energy (ZPE) corrections. Thermal corrections were computed at the reaction conditions, that is, 298.15 K (room temperature) and 1 atm pressure. Connectivity of the stationary points was confirmed by the “pseudo” intrinsic reaction coordinate (IRC) approach,43 where IRC calculations were performed for 20 steps from the TS (both in the forward and backward directions), and subsequent structures were fully optimized to obtain the minima. Initial approximations of the TSs were obtained by the conventional AFIR methodology,26 where the two-layer our own N-layered integrated molecular orbital and molecular mechanics (ONIOM) method was applied.44 The ONIOM partitioning of the molecular system is shown in Figure 2a. The BP86 functional was applied for the high-level, using the SDD40 basis set for Ni and Fe, and the 3-21G basis sets45 for the remaining atoms. The parametrization method 6 (PM6)46 was applied for the low-level. An artificial force parameter of 47.8 kcal/mol was used to explore the approximate reaction paths and TSs (Figure 2b). The approximate TSs obtained by AFIR method were finally optimized at the level of SMD/BP86-D3/BS1.

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2. COMPUTATIONAL DETAILS Geometry optimization and potential energy calculations were performed using the Gaussian 09 program.32 All the structures were fully optimized without any constraints using the Becke–Perdew 1986 (BP86)33,34 functional with Grimme’s (D3) dispersion correction,35 where the BP86 functional has been used before to model biomimetic NiFe complexes.36,37,38,39 The Stuttgart–Dresden (SDD)40 basis set and the associated effective core potential were used for Ni and Fe, and the def2-SVP(split valence polarization) basis sets41 were applied for other atoms (BS1). The potential energies were calculated at the level of BP86-D3/BS2, (BS2 = SDD for Ni and Fe, and def2-TZVP for the other toms). Solvation effects were considered using the solvent model density (SMD) implicit solvation model42 with acetonitrile as the solvent (ε = 35.688) in both geometry optimizations and potential energy calculations. Integrals were evaluated using the pruned grid consisting of 99 radial shells and 590 angular points per shell. The wavefunction stability was checked for all metal complexes.

Figure 2. (a) Partitioning of the molecule into ONIOM high (black) and low (blue) levels. (b) An artificial force was added between the highlighted atoms (red).

3. RESULTS AND DISCUSSION 3-1. Analysis of complexes A1 and E1 Complex A1: The experimentally determined oxidation states of complex A1 on the Ni and Fe species are both 2+, indicating that the orbital occupancies are d8 (Ni) and d6 (Fe), respectively. Therefore, we considered four spin multiplicities (S = 0, 1, 2, and 3). The ground state of complex A1 is singlet and the three higher spin states (S =1, 2, and 3) are more than 26.7 kcal/mol higher in energy than the singlet state (Table 1). Furthermore, the singlet state of geometry (Figure 3a) gave the lowest mean unsigned error for the selected bond lengths (MUE, 0.04 ) from the X-ray structure (Table S1) with the deviations being less than 0.1 Å. Thus, the energy values and geometry suggest that the ground state of complex A1 is the singlet state.

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ACS Catalysis

Table 1. Mulliken spin densities (ρ), enthalpies (ΔH)a, and free energies (ΔG)a for complex A1 and E1 at four spin states S=0

a

S=1

ρ(Ni) ρ(Fe) ρ(S) ρ(S) ΔH ΔG

0.00 0.00 0.00 0.00 0.0 0.0

S=2 Complex A1 0.00 1.40 2.10 2.26 -0.03 0.10 -0.02 0.13 30.7 50.3 26.7 44.8

ρ(Ni) ρ(Fe) ρ(S) ρ(S) ΔH ΔG

0.00 0.00 0.00 0.00 0.0 0.0

1.33 0.20 0.15 0.15 6.0 5.9

S=3 1.46 3.61 0.29 0.27 62.6 57.1

Complex E1 1.23 2.33 0.27 0.10 34.8 30.7

1.37 3.40 0.31 0.31 55.9 48.5

Energies are in kcal/mol. (b) Complex 1E1

(a) Complex 1A1

P2 N2 S2

N Fe

P3 N2 H S2 N1 Fe P1

P3 P2

N1 S1

P1

Ni

Ni

Ni–Fe Ni–N1 Ni–S1 Fe–S1 Fe–P1 Fe–P2 Fe–P3 Fe–NCMe

calc. 3.28 0.04 2.08 0.04 2.18 0.02 2.36 0.02 2.18 0.03 2.16 0.00 2.16 0.02 1.90 0.06

/ / / / / / / / /

X-ray 3.32 2.05 2.16 2.34 2.18 2.18 2.19 1.96

Ni–Fe Ni–N1 Ni–S1 Ni–H Fe–S1 Fe–P1 Fe–P2 Fe–P3 Fe–H

S1

calc. 2.69 0.10 2.01 0.00 2.22 0.04 1.89 0.26 2.40 0.03 2.19 0.00 2.12 0.00 2.13 0.01 1.57 0.00

/ / / / / / / / / /

X-ray 2.79 2.01 2.18 2.15 2.37 2.19 2.12 2.14 1.57

Figure 3. Comparison of the selected geometrical parameters of the fully optimized ground state (S = 0) structures of: (a) complex 1A1 and (b) complex 1E1, and their corresponding X-ray crystal structures. Deviations from the X-ray structure are given in parentheses: bond lengths are in . The electronic configurations of Ni and Fe are (Ni3dxy)2(Ni-3dyz)2(Ni-3dxz)2(Ni-3dz2)2(Ni-3dx2-y2)0 and (Fe3dxz)2(Fe-3dyz)2(Fe-3dxy)2(Fe-3dx2-y2)0(Fe-3dz2)0, respectively (Figure S1), so both are low-spin with a 2+ oxidation state, which agrees with the experimental observations. Complex E1: For complex E1, four spin multiplicities (S = 0, 1, 2, and 3) were examined. The lowest MUE was observed for the singlet spin state (MUE, 0.05 , Table S2), as well as the lowest energy. The energy gap between the singlet and triplet states is relatively small (5.9 kcal/mol), whereas the quintet and septet states are

energetically well separated (> 30 kcal/mol, Table 1). Thus, the spin state of complex E1 is the singlet state, which is in agreement with the results of 1H NMR, electron spin resonance6, and Mössbauer spectroscopy experiment. 11 Since the singlet and triplet energies are relatively close in complex E1, we checked the DFT dependency on the energies for two local density functionals, that is, BLYP47,48-D3 (D3-corrected Becke–Lee–Yang–Parr) and PBE49-D3 (D3–corrected Perdew–Burk–Ernzerhof), and two hybrid functionals, B3LYP50,33-D3 (D3-corrected Becke three–parameter Lee–Yang–Parr functional) and TPSSh (Tao–perduew–Staroverov–Scuseria),51 for the optimized structure obtained by BP86-D3. The BLYP-D3 and PBE-D3 showed a performance similar to that of BP86-D3 (Table S3), whereas the hybrid functionals suggested that the triplet state was the ground state in complex E1, which disagrees with the experimental observations. The hybrid functionals also failed to predict the ground state in the NiFe–O2 adduct in our previous study.31 According to a recent report evaluating the energy gaps of the singlet and triplet states in an active site model of NiFe hydrogenase, local density functionals such as TPSS lead to smaller deviations from the coupled-cluster (CCSD(T)) level of theory compared to the hybrid functionals, TPSSh and B3LYP.39 Swart52 compared spin state splitting of iron complexes with complete active space perturbation theory (CASPT2), and showed that the B3LYP gave the smaller deviation than BP86. Reiher and co-workers53 showed that the use of B3LYP functional with 15% Hartree-Fock exchange correctly describes energy order of the experimentally observed high and low spin in Fe complexes. Thus, the optimal density functional is different depending on the system. Significant deviation of Ni–H distance was found from the X-ray structure in the optimized structure. In order to explore the origin of this error, we have considered effect of basis set, empirical dispersion correction, and the solvent. First, the effect of diffuse function in the basis set was examined by employing SDD(Ni, Fe) and 6-31++G(d,p) for the reset of atoms (Table S6). The calculated Ni-H distance (R(Ni–H) = 1.90 Å) only slightly changes from BS1 basis set (R(Ni–H) = 1.89 Å) as well as the other bond distances. The solvent effect was also minor for the geometry as can be seen from the comparison of calc. 2 and calc. 4 in Table S6. Next, the effect of dispersion correction was examined. The bond distance without dispersion correction was 2.09 Å, which is the obvious change from the use of dispersion correction(R(Ni–H) = 1.89 Å) and is closer to the experiment. However, according to the previous DFT study, the Ni-H distance was calculated as 2.30 Å at the RI-BP86/def2-TZVP level without dispersion correction.11 Thus, it is difficult to ascertain the origin of the large deviation in Ni–H distance. The bond lengths which largely deviate from X-ray structure are not

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ACS Catalysis covalently bonded 11 and the reproduction of chemically binding distance is more critical. In the end, we determined to use dispersion correction which is expected to provide more accurate thermodynamics54 and is important to discuss the reaction mechanism. The X-ray structure indicates that the hydride binds to the Fe rather than Ni, and the DFT calculation also supports that the complex 1E1 is a terminal hydride. The calculated Ni–H and Fe–H distances are 1.89 and 1.57 , respectively, whereas those determined distances by Xray measurements are 2.15 and 1.57 , respectively (Figure 3b). This geometric feature differs from the Ni-R model in Desulfovibrio vulgaris Miyazaki F hydrogenase, where the hydride is found to be almost middle between Ni and Fe sites. The Ni–H and Fe–H distances are 1.58 and 1.78 ,16 respectively. Such a shorter distance of metal–H distance has been commonly seen in the synthetic NiX (X = Fe/Mn/Ru) models55-58, 6, 59-61 except for the recently developed [NiFe] hydrogenase model in which proton reduction occurs on the Ni site.62 Figure 4 depicts the molecular orbital (MO) diagrams of Ni and Fe for complex 1E1. The electronic configuration is (Ni-3dxy)2(Ni-3dxz)2(Ni-3dyz)2(Ni-3dz2)2(Ni-3dx2-y2)0 for Ni and (Fe-3dxz)2(Fe-3dyz)2(Fe-3dxy)2(Fe-3dx2-y2)0(Fe-3dz2)0 for Fe. Thus, the oxidation states of Ni and Fe are both 2+, which agrees with the experimentally determined oxidation states.6 The oxidation states of Ni and Fe are the same as those in the Ni-R state of hydrogenase.

–1.18 Fe-3dz 2 Ni-3dx2-y 2 –1.94

Fe-3dx 2-y2 –2.82 Ni-3dz2 Orbital energy (eV)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

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–3.87 Fe-3dxy Ni-3dyz –4.51 –4.64 –5.02 –5.21

–4.91 Fe-3dyz

Ni-3dxz –5.63

Ni-3dxy

Fe-3dxz

Figure 4. Molecular orbital diagrams (isovalue = 0.02) of Ni and Fe for complex 1E1. The orbital energy is given in eV. 3-2 Reaction mechanism 3-2-1 Removal of solvent and H2 coordination Starting from complex 1A1, the removal of solvent from the NiFe complex takes place by overcoming an energy barrier of 14.0 kcal/mol (Figure 5 and Figure S7). The transition state (1TS-A1A2) and the intermediate (1A2) are the geometrically very close and the almost same energy, indicating 1TS-A1A2 is the late TS. The generated intermediate 1B is energetically higher than complex 1A1 by 3.8 kcal/mol. Then, dihydrogen approaches to the Fe in a side-on fashion (1TS-C1C2; R (Fe…H1) = 2.39 Å, R(Fe…H2) = 2.49 Å, Figure 6b), and binds to the vacant coordination site, with the H2 and Fe interacting very weakly. The H2 molecule coordinates only to Fe and not to Ni. This is because the lowest unoccupied orbital (LUMO) dz2 (Figure S2) to which the σelectrons of hydrogen are partially donated is on Fe. Furthermore, no vacant orbital exists in the axial direction on the Ni site. This suggests that a modification of the Ni ligand is key to developing the catalyst for Ni-centered H2 coordination. 3-2-2. H− −H bond cleavage and formation of the hydride complex Upon coordination of a H2 molecule into the iron site (complex 1C2), the H−H bond length increases from 0.77 to 0.84 Å (Figure 6c). This complex (1C2) can be

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ACS Catalysis

classified as a “Kubus’s type (normal H2) complex”.63,64 in which the interaction between two hydrogen atoms remains (i.e. the H–H bond distance is less than 1.5 65). Furthermore, it can reversibly dissociate from the metal.63 Bond elongation occurs due to a shift in electron density from hydrogen to Fe, where the Lewis acidity of Fe is enhanced by electron–withdrawing [P(OEt)3]3 ligands. The almost equivalent bond lengths of Fe–H1 and Fe–H2 (1.66 and 1.65 , Figure 6c) indicate that the electron densities on the two hydrogens atoms are the same. In hydrogenase, a side-on H2–binding complex is formed which is also a Kubus–type complex, according to computational results.15 However, the H2binding site is Ni in hydrogenase.37 Next, MeO– approaches the NiFe-H2 complex and abstracts a proton, where this is a barrierless process (see the IRC path, Figure S10) and the TS (1TS-D1D2) has a fairly low imaginary frequency (43.5 cm–1, Table S7). The slightly higher energy of precursor (1D1) than the TS (1TS-D1D2) originates from the thermal correction of enthalpy (Table S10). This heterolytic splitting of the H−H bond accompanies the formation of MeOH, and the system is significantly stabilized (~40 kcal/mol) due to the disappearance of the highly unstable methoxy species (MeO–). This remarkable exergonic process was also predicted in a previous computational study.11 The H2-activation process in the present NiFe model and in NiFe hydrogenase are analogous with the heterolytic activation being achieved through a Lewis acid-base pair that does not directly react with each other.4, 66 Such a conceptual mechanism is denoted as “frustrated Lewis pair” and is found in both metal and metal-free systems.67,68,69,70,71 In [NiFe] hydrogenase, it has been accepted that the Ni acts as the Lewis acid. However, multiple candidates have been suggested for the Lewis base, forexample, arginine,66,72 glutamate73, 74 and cysteine,1,75 so it is still under debate which substance acts as the Lewis base in the catalytic cycle. We have checked the possibility of contribution from the triplet spin state as the energy difference between S = 0 and S = 1 in complex E1 is relatively small (5.9 kcal/mol , Table 1). The calculated free energies of the triplet complexes, 3B (14.9 kcal/mol) and 3C2 (23.4 kcal/mol) are higher than those of singlet TSs: 1TS-C1C2 and 1TS-D1D2. Thus, one can exclude the possibility of multistate reactivity.76,77 As a summary of “STEP1”, the rate determining step is acetonitrile removal rather than H–H bond cleavage. The calculated activation enthalpy (ΔΔH) is 15.4 kcal/mol, which underestimates the experimentally determined activation barrier; (ΔΔH = 18.0 ).78

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Figure 5. Free energy profiles of (a) acetonitrile removal, (b) H2 binding, and (c) H–H bond cleavage in the presence of MeO–. ΔG and ΔH (in parentheses) are given in kcal/mol. (a)

(b)

1TS-A1A2

(c)

H2

1TS-C1C2

(d)

H1

1C2

1TS-D1D2

Figure 6. Optimized key geometries: (a) TS of acetonitrile removal, (b) TS of H2 binding, (c)NiFe dihydrogen complex, and (d) TS of H–H bond cleavage with the help of MeO–.

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(a)

(b) 0

+

PT1

N N NiI

P(OEt)3 I S Fe P(OEt)3 S P(OEt) 3

C H

1E1

3B3

+[Fe(III)L2]+ + [Fe(III)L2]+ +[Fe(III)L2]+

+ [Fe(III)L2H]2+ + [Fe(III)L2]+ + [Fe(III)L2]+

–39.0 (–34.7)

35.1 (39.1)

Fe1

∆G [kcal/mol]

H N N NiII II P(OEt)3 S Fe P(OEt)3 S P(OEt)3

Ni

ET3

ET1

1TS-E2B1

2+ H N N NiII III P(OEt)3 S Fe P(OEt)3 S P(OEt)3

–26.8 (–37.6)

+ N N NiII

PT2

2E2

2B2

+ [Fe(II)L2H]+ + [Fe(III)L2]+ + [Fe(III)L2]+

–52.1 (–48.3)

–36.2 (–31.4)

–52.1 (–48.3)

3+

H N P(OEt)3 N NiII FeIII S P(OEt)3 S P(OEt)3

+

+

2+

N N NiII

2E2

2+

S S

FeII

P(OEt)3 P(OEt)3

P(OEt)3

1B1

+

+

PT3

N N NiII

P(OEt)3 S P(OEt)3 S P(OEt) 3 FeII

1E3

[Fe(II)L2]0 [Fe(III)L2]+

–57.7 (–51.8)

2+

ET4

ET2

[Fe(II)L2]0 +

ρ (Ni) = 0.20 ρ (Fe1) = 0.47 ρ (Fe2) = –0.82

P(OEt)3 I S Fe P(OEt)3 S P(OEt) 3

+ [Fe(II)L2]0 + [Fe(III)L2]+ + [Fe(III)L2]+

H N N NiII IV P(OEt)3 S Fe P(OEt)3 S P(OEt)3

R1(Fe1–H) = 1.72 R2(C–H) = 1.50

Fe2

+

FeII

1B1

+

+

FeIII H

H

[Fe(II)L2]0 + +

–37.4 (–33.7)

[Fe(II)L2H]+ [Fe(III)L2]+

(c)

–57.7 (–51.8)

N N NiII

II P(OEt)3 S Fe P(OEt)3 S P(OEt) 3 1B1

+ [Fe(II)L2]0 + [Fe(II)L2]0 + [Fe(III)L2H]2+

–30.9 (–25.7)

0.9

0.4

2+

Spin density (ρ)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

ACS Catalysis

-0.1

Fe1

1TS-E2B1

Fe2 -0.6

-1.1 1.40

1.60

1.80

2.00

2.20

R1(Fe1–H) ( )

Figure 7. (a) Schematic representation of the redox states and ET, HAT, and PT processes. The most plausible pathway is represented by the stick arrows. The free energies (kcal/mol) are calculated relative to complex 1A1, and the enthalpies are given in parentheses. (b) The free- energy profile of HAT with optimized TS structure (1TS-E2B1). ΔG and ΔH (in parentheses) are given in kcal/mol. The selected bond lengths in TS are given in angstrom. (c) Plots of spin densities of two irons, Fe1 and Fe2, along the reaction coordinate. 3-2-3 Electron/hydride/proton transfer in the NiFe– hydride complex

transfer (PT) from a strong acid, such as HBF4.6 We have theoretically examined the mechanistic details of these processes (Figure 1).

Experimental studies have demonstrated that the hydride complex 1E1 accomplishes: (a) electron transfer to the ferrocenium ion ([Fe(III)L2]+, L = C5H5), (b) hydride transfer to 10-methylacridinium, and (c) proton

a. Electron transfer from the NiFe hydride complex to the ferrocenium ion: One proton and two electrons are transferred from the hydride complex 1E1 to reduce the ferrocenium ion and generate complex B1. The

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possible pathway can be represented by a double square diagram (Figure 7a). All the complexes in Figure 7a are optimized starting from X-ray structure of 1E1. The free energies of all possible intermediates were calculated for four spin multiplicities (S = 1,2, 3, and 4, or S =1/2, 3/2, 5/2, and 7/2) (Tables S8), and the ground state of each complex was shown in Figure 7a. It is known that ferrocene and ferrocenium ions act as a proton79,80,81 and an electron acceptor,82 respectively. Protonated ferrocene, [Fe(II)L2H]+, has two isomers depending on the position of the protonation, that is, metal- and ring-protonated ferrocene.79,81 Therefore, we have checked the thermodynamic stability of these isomers in [Fe(II)L2H]+ and [Fe(III)L2H]2+. The two isomers are energetically close in [Fe(II)L2H]+, with the energy difference being 0.8 kcal/mol (which qualitatively agrees with a previous computational study),79whereas they are energetically separated in [Fe(III)L2H]2+. The ring-protonated isomer is about 6.9 kcal/mol lower in energy than the metal-protonated one. In Figure 7a, the lower energy isomers were used for the thermodynamic calculations. The oxidation states of Ni and Fe were determined based on the electron occupancies of the 3d orbitals (Figure 4 and Figures S2-S6). The electronic configurations of Ni and Fe are (d8, d5) for 2E2, (d8, d4) for 1E3, (d9, d7) for 1B3, and (d8, d7) for 2B2, then the oxidation states were determined as depicted in Figure 7a. In the possible redox processes, the oxidation state of Fe changes, whereas the oxidation state of Ni does not vary except for the two electron reduced form of 1B1. This differs from the NiFe hydrogenase redox process where the oxidation state of Ni varies. The change in the oxidation state of Fe is proportional to the number of electrons transferred to the ferrocenium ion, indicating that both the Ni and Fe ligands are redox-innocent. The key geometrical parameters and the spin densities on Ni and Fe are listed in Table 2 for all the complexes in the double square diagram (Figure 7a). The Ni–Fe distance in complex 1E1 is shortened by 0.11 Å during the first one-electron oxidation (1E1 (2.69 Å) 2E2 (2.58Å )), implying that a metal–metal bond is formed.83,84 On the other hand, the change in Ni–H and Fe–H distances are ~0.05 Å. Interestingly, Ni–H and Fe–H bond lengths of complex 2E2 are closer than 1E1 to the Ni–R state, which has been detected in NiFe hydrogenase by X-ray crystallographic techniques.16 An additional one-electron oxidation (2E2 1E3) increases the Ni–Fe distance, accompanied by a shortening of the Ni–H distance, where Ni–H and Fe–H are almost equivalent. Complexes 1 B1, 2B2, and 3B3 have consistently large distance than 1E1, 2 E2, and 1E3, implying the interactions between H and metals. Overall, the structural features are fairly sensitive to the oxidation state. For the two S = 1/2 species, 2E2 and 2B2, the spin density distribution differs; the spin density is

Page 8 of 14

almost equally shared between Ni and Fe in complex 2E2, whereas it is localized on Fe in complex 2B2. Complex 1E3 has opposite spins on Ni and Fe, then this is the open shell singlet system.

Table 2. Key geometrical parameters (Å) and Mulliken spin densities on Ni and Fe for three redox states of NiFe hydride complexes (1E1, 2E2 and 1E3) and NiFe complexes (1B1, 2B2, and 3B3)

1

E1

R (Ni–Fe)

R (Ni–H)

R (Fe–H)

ρ (Ni)

ρ (Fe)

2.69

1.89

1.57

0.00

0.00

2

E2

2.58

1.84

1.59

0.50

0.45

1

E3

2.65

1.70

1.63

–0.25

0.28

1

B1

2.81

–

–

0.00

0.00

2

B2

2.88

–

–

0.03

0.95

3

B3

2.77

–

–

0.91

0.76

Starting from complex 1E1, a single electron transfer from 1 E1 to the ferrocenium ion (with generation of complex 2 E2) is the most plausible pathway. The HAT pathway has a barrier of 15.7 kcal/mol (1TS-E1B2) and the PT route leads to a species with a significantly high energy (3B3). Hence, these pathways are unlikely. In the next step, HAT or PT is the possible pathway because the ET product (1E3) is higher in energy than the 2 E2 (by 14.7 kcal/mol). The two TSs for HAT/PT from 2E2 to the ring and to the Fe species of the ferrocenium ion were optimized. The TS for HAT/PT to the Fe of ferrocenium ion (ΔG = –8.7 kcal/mol) is much higher in energy than that to the ring carbon( Δ G = –26.8 kcal/mol). This is presumably due to large repulsive interactions between the ferrocene ring and the ligands of the NiFe complexes (Figure S14). The energy barrier for HAT/PT was 25.3 kcal/mol, indicating that it is a relatively slower process in comparison to “STEP1”. Further, the barrier height of the triplet state was higher than the singlet (28.7 kcal/mol in Table S9). At the TS of HAT (1TS-E2B1), the spin densities are mainly located on the Ni and two irons (Figure 7b), where the signs of the spin density of Fe1 in the NiFe complex and Fe2 in the ferrocenium ion are opposite (ρ (Fe1) = 0.47 and ρ(Fe2) = –0.82). To confirm whether TS is HAT or PT, the spin densities on Fe1 in the NiFe complex and Fe2 in the ferrocenium ion were plotted along the reaction coordinate (Fe1–H distance) (Figure 7c). It was found that as the Fe1–H distance increases, the spin densities of Fe1 and Fe2 gradually become zero, where the spin densities on the ligands of the NiFe

8


Page 9 of 14

complex and the ferrocenium ion are negligible. Hence, the obtained TS is for HAT. During the ET HAT process, the oxidation state of Fe in the NiFe complex changes Fe(II)(1E1) Fe(III)(2E2) Fe(II)(1B1), whereas that of Ni is conserved. 1

C H Ni

N N NiII

2

The complexes E1 and E2 can be thought to correspond to the Ni-R and Ni-C states in hydrogenase, respectively. On the other hand, the state corresponding to 1E3 is thermodynamically unstable and so the corresponding sate will expectedly not to be observed in NiFe hydrogenase. Instead, the Ni-SIa state which corresponds to 1B1 has been detected. Although the Ni– C state has a bridging hydride,85 the corresponding 2E2 state is a terminal hydride as well as complex 1E1 (Table 2). b. Hydride transfer to the 10-methylacridinium ion: A hydride transfer from complex 1E1 to the 10methylacridinium ion (AcrH+) has been experimentally observed.6 Although AcrH+ has not been broadly used to investigation hydride transfer in metal complexes, it has been utilized by Fukuzumi and co-workers86,87,88-90 to study nicotinamide adenine dinucleotide model complexes. It is of great interest that whether experimentally observed hydride transfer reaction proceeds in a single step (H–) or in multiple steps (H + e– or H+ + 2e–).87 Figure 8 shows the free energy profile of the hydride transfer process and the optimized TS. It is noted that the binding site of hydride is not nitrogen but a carbon in the central ring of AcrH+.91 The calculated activation barrier for this process is 21.3 kcal/mol. We have checked spin density and Mulliken charges along the reaction coordinate. In the TS (1TS-E1B1) and along the IRC, no spin density was present on any atom. In addition, the sum of Mulliken charges for the AcrH2 species in the product (NiFe⋅⋅⋅AcrH2 complex) was zero, suggesting that the process is a hydride transfer, and not HAT and proton transfer reactions. It has been reported that the hydride transfer is triggered by N5,N10-methenyltetrahydromethanopterin in mono-iron hydrogenase. In that system, the barrier height was estimated to be 20.3 kcal/mol at the TPSS/6-31++G(d,p) level,10 which is close to the barrier height for the hydride transfer in the present NiFe complex. A hydride transfer to AcrH+ is a more feasible process (barrier height: 21.3 kcal/mol) than a HAT to the ferrocenium ion [Fe(III)L2]+ (barrier height: 25.3 kcal/mol).

Fe

+

∆G [kcal/mol]

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

ACS Catalysis

H S S

FeII

R1 (Fe–H) = 1.64 R2 (H–C) = 1.76

P(OEt)3 2+

P(OEt)3

P(OEt)3 1E1

1TS-E1B1

+

N N NiII

S S

–17.7 (–29.1)

Me N+

P(OEt)3

II

Fe

P(OEt)3

P(OEt)3 1B1

+

Me N

–39.0 (–34.7) HH

–54.0 (–48.8)

Figure 8. Free energy profile for a hydride transfer to the 10-methylacridinium ion. ΔG and ΔH (in parentheses) are given in kcal/mol. The selected bond lengths are given in angstrom. c. Proton transfer and formation of H2: The addition of a strong acid, namely HBF4, resulted in the formation of H2 in previous experiment.6 Since the proton in HBF4 is dissociative and forms HF and BF3, we have considered the following chemical reactions: BF3

+ HF + Et2O

→ BF4– +

Et2OH+

(1) The reaction is exergonic by 5.3 kcal/mol, and therefore, the proton-addition TS was calculated using protonated diethyl ether (Et2OH+) . The calculated free profile is depicted in Figure 9. In contrast to the HAT and hydride-transfer routes, this process is barrierless, which is presumably due to the use of a strong acid rather than the high nucleophilicity of the complex 1E1. Furthermore, once a proton has been transferred from the acid, complex 1C3 is formed with the liberation of H2 as shown in Figure 5 (1C2 →1TS-C1C2 →1B).

9


ACS Catalysis

O H2 +

H N P(OEt)3 N NiII FeII S P(OEt)3 S P(OEt)3

Ni

details of the reaction processes. Although the catalytic center for H2 activation differs from that in NiFe hydrogenase, the details of the redox processes and the reaction kinetics investigated in this study should be helpful for understanding catalytic processes in NiFe hydrogenase and developing more efficient biomimetic catalysts.

R1 (Fe–H1) = 1.55 R2 (H1–H2) = 1.08 R3 (H2–O) = 1.14

H1 Fe

1E1

+ H

∆G [kcal/mol]

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Et

O+ Et

–39.0 (–34.7)

1TS-E1C3

–35.0 (–43.9)

Page 10 of 14

2+

N N NiII

H H S S

FeII

P(OEt)3 P(OEt)3

P(OEt)3 1C3

+

Et

O Et

–51.0 (–45.3)

Figure 9. Free energy profile for proton transfer from protonated diethyl ether. ΔG and ΔH (in parentheses) are given in kcal/mol. The selected bond lengths are given in angstrom.

IV. CONCLUSIONS We have explored the whole catalytic processes of a bioinspired model complex of NiFe hydrogenase by DFT calculations and AFIR studies (Figure 10). The reaction is initiated by the removal of acetonitrile from Fe. Once H2 binds to Fe, the H2 bond cleavage occurs barrierlessly in the presence of MeO–. The process is remarkably exergonic for the generation of the NiFe hydride complex and methanol. Our calculations showed that H2 binds to the Fe center rather than to Ni. This is because the LUMO (dz2) is located on Fe and no vacant axially oriented orbitals exist on Ni. Our calculated free energy profile showed that the ratedetermining step of “STEP1” (Figure 1) was acetonitrile removal rather than H–H bond cleavage. The redox process involving the hydride complex and a ferrocenium ion was carefully examined. The calculated thermodynamic and kinetic data revealed that first an electron transfer occurs from the NiFe hydride complex to the ferrocenium ion, which is then followed by a hydrogen-atom transfer to the second ferrocenium ion. During the process, the oxidation state of Fe in the NiFe complex varies Fe(II)Fe(III)Fe(II), whereas that of Ni(II) is preserved. This differs from the redox process in hydrogenase where the oxidation state of Ni varies. The barrier heights of the HAT and hydride-transfer processes were estimated to be ~25 and ~21 kcal/mol, respectively, which supports experimental data suggesting that both reactions can take place at the room temperature. In contrast, the proton transfer from a strong acid to the NiFe hydride complex is a barrierless process.

Figure 10. The catalytic cycle of the NiFe complex.

SUPPORTING INFORMATION Tables S1–S10, Figures S1–S16, and Cartesian coordinates of all optimized geometries. This material is available free of charge via the Internet at http://pubs.acs.org.

Corresponding Authors *Email:[email protected], [email protected]

Acknowledgment M.I. acknowledges the Fukui Fellowship, Kyoto University. This work was in support in part by the World Premier International Research Center Initiative (WPI), Grants-in-Aid for Specially Promoted Research (26000008) from the Ministry of Education, Culture, Sports, Science and Technology (MEXT), and Grants-inAid for Scientific Research (KAKENHI 15H00938, 15H02158 and 18K05297). Computer resources at the Academic Center for Computing and Media Studies at Kyoto University, Research Center of Computer Science at the Institute for Molecular Science are also acknowledged.

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Overall, our theoretical calculations corroborated the experimental observations, and rationally explained the

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ACS Catalysis

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ACS Catalysis Ferrocenium ion

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! Reaction with 10-methylacridinium ion: H– transfer (one step) ! Reaction with ferrocenium ion: ET → HAT (two steps)

NiFe

H2

10-methylacridinium ion

H!

H–

H+

e– NiFe–H

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Electron and Hydride Transfer in a Redox-Active ... - ACS Publications

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