Spin coupling models for cytochrome oxidase

Abstract Spin coupling between high-spin ferric heme a 3 and cupric Cu B is the most popular explanation for the EPR silent active site of resting state cytochrome oxidase [1]. In this paper we examine how synthetic model compounds with spin coupling between S = 5 2 ferric porphyrins and adjacents S = 1 2 centers support this hypothesis. Communications from a number of different laboratories chronicle the progress which is being made in the synthesis of cytochrome oxidase models having iron(III) porphyrins which are chemically linked to adjacent copper(II) centers [2–6]. While we await the evolution of this model compound approach and the full structural and magnetic characterization of these materials it is instructive to consider the properties of two magnetically interesting iron(III) porphyrins which might appear at first glance not to be particularly relevant to the ironcopper spin coupling problem. The π-radical cations of iron(III) porphyrins are, however, the best characterized of the very few known examples of S = 5 2 heme groups which are spin coupled to nearby S = 1 2 centers. The two complexes [FeCl(TPP·)] + and Fe(OClO 3 ) 2 (TPP·) have been characterized unambiguously as high-spin iron(III) complexes of the tetraphenylporphyrin π-cation radical (TPP·) [7–9]. Both are EPR silent. However, they are magnetically quite distinct and represent two extremes of magnetic interaction between the S = 5 2 iron(III) centers and the S = 1 2 ligand. The first complex, [FeCl(TTP·)] + , has a linear 4–300 K Curie magnetic susceptibility plot with values that identify it as an S = 2 system (μ 300K eff = 5.1 BM). To our knowledge this is the only known example of strong antiferromagnetism [|–J¦⪢200 cm −1 ) between S = 5 2 and S = 1 2 centers and as such, it provides a conceptual spin model for the widely accepted, albeit unproven, S = 2 model for the heme a 3 /Cu B site of oxidase. The second complex, Fe(OClO 3 ) 2 (TPP·), also has a linear Curie plot but its magnetic moment (μ 300 K eff = 6.1 BM) requires a higher spin multiplicity. The two possibilities are an S = 3 ferromagnet (+J ⪢ 200 cm −1 ) or an independent S = 5 2 , S = 1 2 spin system. Magnetic measurements and Mossbauer data favor the latter assignment [8]. This is intriguing from many points of view not the least of which is the possibility that this system has no detectable spin coupling in a magnetic susceptibility experiment (4–300 K) and yet is EPR silent under normal spectrometer conditions (10 K). Mossbauer effect measurements on these complexes are also of interest in considering spin-coupling models for oxidase. Both complexes show zero field Mossbauer parameters for the isomer shift (δ) and quadruple splitting (ΔE Q ) which are quite typical of high-spin ferric porphyrins [7–9]. However, Mossbauer spectra run in applied magnetic fields reveal differences ascribable to the effects of spin-coupling in FeCl(TPP·) + [8]. These results provide but one demonstration of a hypothesis which probably has general validity, namely, isomer shift and quadruple splitting parameters are reliably diagnostic of spin state and oxidation state in spite of possible spin coupling to adjacent paramagnetic centers. It is linewidth information and data collected in the presence of applied magnetic fields which give clues to the presence of spin coupling although its nature can be difficult to decipher. These observations support the spin and oxidation state assignments made recently for heme a 3 from Mossbauer effects studies with bacterial oxidase [10] and at the same time lead to some uncertainty in reconciling the low-spin ferric-like Mossbauer parameters of one model complex [5] with its proposed spin state and structure.