M{\\"o}ssbauer characterization of an unusual high-spin side-on\n peroxo-Fe3+ species in the active site of superoxide reductase from\n Desulfoarculus Baarsii. Density functional calculations on related models (2014)

Superoxide reductase (SOR) is an Fe protein that catalyzes the reduction of\nsuperoxide to give H(2)O(2). Recently, the mutation of the Glu47 residue into\nalanine (E47A) in the active site of SOR from Desulfoarculus baarsii has\nallowed the stabilization of an iron-peroxo species when quickly reacted with\nH(2)O(2) [Math{\\'e} et al. (2002) J. Am. Chem. Soc. 124, 4966-4967]. To further\ninvestigate this non-heme peroxo-iron species, we have carried out a\nM{\\"o}ssbauer study of the (57)Fe-enriched E47A SOR from D. baarsii reacted\nquickly with H(2)O(2). Considering the M{\\"o}ssbauer data, we conclude, in\nconjunction with the other spectroscopic data available and with the results of\ndensity functional calculations on related models, that this species\ncorresponds to a high-spin side-on peroxo-Fe(3+) complex. This is one of the\nfirst examples of such a species in a biological system for which M{\\"o}ssbauer\nparameters are now available: delta(/Fe) = 0.54 (1) mm/s, DeltaE(Q) = -0.80 (5)\nmm/s, and the asymmetry parameter eta = 0.60 (5) mm/s. The M{\\"o}ssbauer and\nspin Hamiltonian parameters have been evaluated on a model from the side-on\nperoxo complex (model 2) issued from the oxidized iron center in SOR from\nPyrococcus furiosus, for which structural data are available in the literature\n[Yeh et al. (2000) Biochemistry 39, 2499-2508]. For comparison, similar\ncalculations have been carried out on a model derived from 2 (model 3), where\nthe [CH(3)-S](1)(-) group has been replaced by the neutral [NH(3)](0) group\n[Neese and Solomon (1998) J. Am. Chem. Soc. 120, 12829-12848]. Both models 2\nand 3 contain a formally high-spin Fe(3+) ion (i.e., with empty minority spin\norbitals). We found, however, a significant fraction (approximately 0.6 for 2,\napproximately 0.8 for 3) of spin (equivalently charge) spread over two occupied\n(minority spin) orbitals. The quadrupole splitting value for 2 is found to be\nnegative and matches quite well the experimental value. The computed quadrupole\ntensors are rhombic in the case of 2 and axial in the case of 3. This\ndifference originates directly from the presence of the thiolate ligand in 2. A\ncorrelation between experimental isomer shifts for Fe(3+) mononuclear complexes\nwith computed electron densities at the iron nucleus has been built and used to\nevaluate the isomer shift values for 2 and 3 (0.56 and 0.63 mm/s,\nrespectively). A significant increase of isomer shift value is found upon going\nfrom a methylthiolate to a nitrogen ligand for the Fe(3+) ion, consistent with\ncovalency effects due to the presence of the axial thiolate ligand. Considering\nthat the isomer shift value for 3 is likely to be in the 0.61-0.65 mm/s range\n[Horner et al. (2002) Eur. J. Inorg. Chem., 3278-3283], the isomer shift value\nfor a high-spin eta(2)-O(2) Fe(3+) complex with an axial thiolate group can be\nestimated to be in the 0.54-0.58 mm/s range. The occurrence of a side-on peroxo\nintermediate in SOR is discussed in relation to the recent data published for a\nside-on peroxo-Fe(3+) species in another biological system [Karlsson et al.\n(2003) Science 299, 1039-1042].\n