Isolation and Crystal Structure of a Peroxo-Bridged Heme–Copper Complex

The reaction of dioxygen with transition metal complexes is important from the standpoint of O₂ binding and activation in biological systems.1 Cytochrome c oxidase (CcO), which a catalyzes four electron reduction of O₂ to water, has a unique heme/nonheme copper dinuclear core in its active site.2 A number of heme-based iron–copper dinuclear complexes have been synthesized to elucidate the mechanism of O₂ reduction in CcO.3–6 We reported the reaction of O₂ with tetraphenylporphyrin (TPP)-Fe^II-linked tris(2-pyridylmethyl)amine (TPA)–Cu^I dinuclear complexes and the formation of peroxo-bridged dinuclear species Fe–O₂–Cu with a moderate stability in CH₃CN at room temperature.4 Karlin et al. also reported a similar dioxygen reaction with both the analogous dinuclear complexes5d and the 1:1 mixture of the heme and the Cu complex.5e, 6 Although these peroxo-bridged dinuclear species were characterized by various spectroscopic methods, the detailed structure of Fe^III–O₂–Cu^II moiety has not been clarified. Moreover, to the best of our knowlege, the isolation and structure of such a heterodimetallic peroxo-bridged complex has never been reported. Herein, we describe the first report of the isolation and crystal structure of a peroxo-bridged heme–copper dinuclear complex.

We prepared a dinuclear complex, [(TMP)Fe^II-(5MeTPA)Cu^I]BPh₄ (1, TMP-5MeTPA=10,15,20-tris(2,4,6-trimethylphenyl)-5-(2′-bis((5′′-methyl-2′′-pyridylmethyl)aminomethyl)pyridine-5′-carboxyamidophenyl)-porphyrin). The UV/Vis spectrum of 1 in CH₃CN showed absorption maxima at 428 and 534 nm. When 1 was exposed to O₂ in CH₃CN at −30 °C (Scheme 1), the 428 and 534 nm bands disappeared and bands at 420, 557 and 612 nm appeared (Figure 1), thus indicating the formation of a peroxo-bridged Fe–O₂–Cu species, as we described previously.4 This peroxo species exhibited much higher stability in the CH₃CN solution than the previously reported analogues,7 on account of the steric hindrance by the multiple methyl groups. The solution of the peroxo complex could be kept at −30 °C for several days without decomposition finally yielding dark-purple crystals. The formula of the crystals was determined as [(TMP)Fe^III-(O₂)-(5MeTPA)Cu^II]BPh₄ (2) from the elemental analysis and ESI-mass spectrum. The UV/Vis spectrum of the redissolved solution of 2 in CH₃CN (λ_max (ε, M⁻¹ cm⁻¹)=420 (126 000), 557 (8500), 612 (3500) nm) was in good agreement with that of the peroxo complex before the isolation. The resonance Raman spectrum of 2 in CH₃CN exhibited an isotope sensitive band at 790 (¹⁶O₂)/746 (¹⁸O₂) cm⁻¹ (Figure 1, inset), which was assigned to peroxy ν(OO) as were the analogues reported previously.4 These results clearly indicate the successful isolation of the peroxo complex 2. The decomposition of 2 was not observed for a sample that was left for several months in the solid state, even at room temperature.

Figure 1. UV/Vis absorption spectra of 1 (- - - -) and 2 (—) in CH₃CN at −30 °C; inset. resonance Raman spectra of 2 (in CH₃CN, room temperature, λ_ex=413.1 nm), A: ¹⁶O₂, B: ¹⁸O₂, C: A-B.

Scheme 1. Formation of [(TMP)Fe^III-(O₂)-(5MeTPA)Cu^II)]BPh₄ (2) from [(TMP)Fe^II-(5MeTPA)Cu^I]BPh₄ (1) and dioxygen.

The crystal structure of 2 was determined by single-crystal X-ray analysis (Figure 2).8 The Fe–O₂–Cu moiety has a μ-η²:η¹ coordination mode; both oxygen atoms (O(2) and O(3)) of the peroxo ligand bind to Fe(1) while only O(2) binds to Cu(1). The observed OO bond length (1.460(6) Å) is reasonable for a peroxo ligand,9 although this value is larger than those of other side-on peroxometalloporphyrins.10–12 The Fe(1)O(2)Cu(1) unit is almost linear with the angle 166.0(3)°, being similar to that of the heme–copper μ-oxo species (Fe-O-Cu=171.1(3)°).5c The μ-η²:η¹ coordination mode in metal-peroxo species has been reported for the rhodium(III), vanadium(V) and palladium(II) homodinuclear complexes.13 However, in those cases, the M-O-M units are bent with an angle 103≤M-O-M≤133°.

Figure 2. ORTEP view of [(TMP)Fe^III-(O₂)-(5MeTPA)Cu^II)]⁺ in crystals of 2 drawn with the thermal elliposids at the 30 % probability level. All hydrogen atoms are omitted for clarity. Selected bond length [Å] and angles [°]: Cu(1)-O(2) 1.915(5), Cu(1)⋅⋅⋅O(3) 2.657(7), Fe(1)-O(2) 2.031(4), Fe(1)-O(3) 1.890(6), O(2)-O(3) 1.460(6), Cu(1)-N(1) 2.054(8), Cu(1)-N(2) 2.15(1), Cu(1)-N(3) 2.035(6), Cu(1)-N(4) 2.061(6), Fe(1)-N(5) 2.15(1), Fe(1)-N(6) 2.08(1), Fe(1)-N(7) 2.18(1), Fe(1)-N(8) 2.03(2), Cu(1)-O(2)-Fe(1) 166.0(3), Cu(1)-O(2)-O(3) 103.0(4).

The iron ion is coordinated by the four pyrrole nitrogen atoms and the two oxygen atoms of the peroxo ligand. The peroxo ligand is bound to Fe(1) in a side-on mode eclipsing the two FeN bonds (Fe(1)N(5) and Fe(1)N(7)). The two FeO bond lengths are 2.031(4) (Fe(1)-O(2)) and 1.890(6) (Fe(1)-O(3)) Å. In mononuclear side-on peroxo–M–porphyrin complexes (M=Ti^III,10 Mo^VI,11 or Mn^III12) the MO bond lengths are almost identical. On the other hand, the Fe(1)O(2) bond length in complex 2 is considerably longer than that of Fe(1)O(3), probably as a result of the coordination of Cu(1) to O(2). The iron ion lies 0.595(10) Å above the least-square plane based on the pyrrole nitrogen atoms towards the peroxo ligand. This displacement is also found in peroxo–M–porphyrin complexes (M=Ti^III,10 or Mn^III12) and is consistent with the EXAFS structure of peroxo–iron(III) porphyrin.14b

The structure of the TPA-Cu-O-O unit is similar with that of the trans-(μ-1,2-peroxo)dicopper(II) complex derived from [(TMPA)Cu^I(CH₃CN)]⁺ (TMPA=tris(2-pyridylmethyl)amine) and dioxygen.15 The copper ion is pentacoordinated with a distorted trigonal-bipyramidal geometry by the three pyridine nitrogen atoms, the one tertiary nitrogen atom and the one oxygen atom of the peroxo ligand. Cu(1) is displaced 0.319(2) Å out of the N(1), N(2), N(3) trigonal plane away from the tertiary nitrogen N(4) toward O(2) of the peroxo ligand. The Cu(1)-O(2) bond length (1.915(5) Å) and the Cu(1)-O(2)-O(3) angle (103.0(4)°) are close to those of the trans-(μ-1,2-peroxo)dicopper(II) complex.15

Evidence that the peroxo ligand bridges the iron and the copper ions is also obvious from magnetic studies. The peroxo complex 2 is ESR inactive at 4 K. The magnetic susceptibility of 2 was measured from 10 to 300 K. The determined effective magnetic moment is 4.65 μ_B and temperature independent within this temperature range. This magnetic moment is consistent with a spin-only value of S=2 (μ_eff=4.90 μ_B), therefore, 2 is assigned as a paramagnetic species with an overall S=2 spin state. The Mössbauer spectrum of 2 (77 K, zero field) showed a sharp quadrupole doublet with parameters (ΔE_q=1.17 mm s⁻¹, δ=0.56 mm s⁻¹) typical for high-spin Fe^III compound (see Supporting Information), and is in good agreement with those of peroxo-bound iron(III)-porphyrin complexes.5e, 14c Based on these results, the iron ion has a high-spin d⁵ configuration (S=5/2), and is strongly coupled with the copper(II) ion (S=1/2) in an antiferromagnetic fashion. This strong interaction between the metal ions is mediated by the bridging peroxo ligand.

In conclusion, we synthesized and characterized a peroxo-bridged iron-copper complex 2. The successful isolation of 2 was confirmed by the elemental analysis and various spectroscopic methods. The X-ray structure analysis of 2 revealed that the Fe–O₂–Cu moiety has a μ-η²:η¹ coordination mode. To the best our knowlege, this is the first example of the structure determination of a peroxo-bridged heterodinuclear complex. Further, this is the first X-ray structure of an “iron”-porphyrin complex with a side-on peroxo ligand.14 Complex 2 is a paramagnetic species with a spin state of S=2, as the bridging peroxo ligand mediates the strong antiferromagnetic coupling between the high-spin iron(III) and the copper(II) ions. Further studies of 2 are in progress in our laboratory.

Experimental Section

[(TMP)Fe^II-(5MeTPA)] was prepared by the similar procedure reported in reference 4.

Synthesis of complex 2: [(TMP)Fe^II-(5MeTPA)] (48 mg, 42 mmol), [Cu(CH₃CN)₄]OTf (18 mg, 42 mmol) and NaBPh₄ (16 mg, 42 mmol) were dissolved in CH₃CN (20 mL) and cooled to −30 °C. The resulting solution was exposed to dry O₂ gas for 30 min, and then stored at −30 °C for 5 days, to give 2 (32 mg, 25 mmol, 60 %) as dark purple crystals. Elemental analysis (%) calcd for C₉₈H₈₇N₉O₃Cu₁Fe₁B₁: C 75.02, H 5.59, N 8.03; found: C 74.64, H 5.59, N 7.87, ESI-MS: m/z: [(TMP)Fe^III-(¹⁶O₂)-(5MeTPA)Cu^II]⁺, 1248.

The ¹⁸O-labeled peroxo complex for Raman experiment was synthesized and isolated by the same procedure. ESI-MS: m/z: [(TMP)Fe^III-(¹⁸O₂)-(5MeTPA)Cu^II]⁺, 1252.