X-ray spectroscopic studies of nickel complexes, with application to the structure of nickel sites in hydrogenases

Abstract

X-ray absorption near-edge spectra (XANES) are reported for 44 Ni(I1) and Ni(II1) complexes with Nand/or S-donor ligands.The spectra reveal features associated with 1s -3d and 1s -4p, electronic transitions, whose presence or absence and intensity provide information that allows the coordination number/geometry of the complex to be determined in most cases. The complexes in this study were selected in order to examine the reliability of coordination number/geometry assignments in complexes with low symmetry and to examine the effects on the spectra of a change in formal oxidation state from +I1 to +HI. The effects on the spectra due to changes in the ligand environment are examined, and the edge energy and the breadth of the edge are found to correlate with the average hardness of the ligand environment. The effects on the spectra due to oxidation state changes are examined by using several pairs of Ni(II/III) isoleptic complexes. These compounds reveal that the effects of changes in the formal oxidation state of the Ni center are strongly dependent on the nature of the ligands present, with S-donor ligands giving rise to smaller shifts in edge energy than N,O-donor ligands. These trends are indicative of the increasing role of ligand oxidation in Ni(lI1) thiolate complexes. These trends are corroborated by X-ray photoelectron spectroscopic (XPS) studies that show a similar trend in both ligand and metal electron binding energies. The information obtained from the model studies is used to examine the Ni K-edge XANES spectrum obtained from a sample of Thiocapsa roseopersicina hydrogenase poised in form C. This spectrum is shown to be consistent with a distorted trigonal-bipyramidal geometry and a mixed 0,N-and S-donor ligand environment for this biological Ni site. ' (3) (a) Cammack, R.; Fernandez, V. M.; Schneider, K. In The Bioinorganic Chemistry of Nickel; Lancaster, J. R., Ed.; VCH: Deerfield Beach, FL, 1988; Chapter 8. (b) Moura, J. J. G.; Tiexera, M.; Moura, I.; LeGall. J. Ibid., Chapter 9. (c) Bastian, N. R.; Wink, D. A.; Wackett, L. P.; Livingston, D. J.; Jordan, L. M.; Fox, J.; Orme-Johnson, W. H.; Walsh, C. T. Ibid., Chapter 10. (4) Ragsdale, S . W.; Wood, H. G.; Morton, T. A.; Ljungdahl, L. G.; DerVartanian, D. Hasnain, S. S.; Piggott, B.; Williams, D. J. Biochem. J. 1984, 220, 591. (9) Fauque, G.; Peck, H. D., Jr.; Moura, J. J. G.; Huynh. B. H.; Berlier, Y.; DerVartanian, D. V.; Teixeira, M.; Przybyla, A. E.; Lespinat, P. A.; Moura, I.; LeGall, J. FEMS Microbiol. Rev. 1988, 54, 299. (IO) (a) Lindahl, P. A.; Kojima, N.; Hausinger, R. P.; Fox, J. A,; Tco, B. K.; Walsh, C. T.; Orme-Johnson, W. H. J. Am. Chem. Soc. 1984,106, 3062. (b) Scott, R. A.; Wallin, S . A.; Czechowski, M.; Dervartanian, D. V.; LeGall, J.; Peck, H. D., Jr.; Moura, I. J. Am. Chem. Soc. 1984, 106, 6864. (c) Scott, R. A.; Czechowski, M.; DerVartanian, D. V.; LeGall, J.; Peck, H. D., Jr.; Moura, I. Rev. Port. Quim. 1985, 27,67. (d) Albracht, S . P. J.; Kroger, A,; van der Zwaan, J. W.; Unden, G.; Bikher, R.; Mell, H.; Fontijn, R. D. Bioc...

Nickel Ions Inhibit Histone Demethylase JMJD1A and DNA Repair Enzyme ABH2 by Replacing the Ferrous Iron in the Catalytic Centers

“…This technique yields information about the coordination number, ligand environment, and metric details regarding the metal-binding site(s). In XAS, comparison of shifts in metal K-edge energies may reveal redox-active metal sites; the analysis of extended x-ray absorption fine structure (EXAFS) provides information regarding the types and number of ligands bound to a metal ion and metric details for the metal ion site; and the analysis of x-ray absorption near edge structure (XANES) provides information about the coordination number of a metal ion and the geometry of the metal site (44,45). Because XAS analysis requires a large amount of purified protein that can only be obtained by using a bacterial expression system and because we had no success in expressing JMJD1A in bacteria due to its large molecular weight, ABH2 was chosen for this analysis.…”

“…The peak areas will depend on the coordination number and geometry of the metal site. From comparison of the peak areas of the observed 1s 3 3d transitions ( Table 1) with samples of known coordination numbers and geometries (44,45), both iron and nickel (in presence and absence of 2-oxoglutarate) have a coordination number of five, which is in agreement with the previous work with Fe(II)-AlkB (46). In the case of the nickel samples, small shoulders associated with peaks involving 1-s 3 4-p z transitions are observed and consistent with a geometry that is closer to square pyramidal than trigonal bipyramidal (44).…”

[NiFe] and [FeS] Cofactors in the Membrane-Bound Hydrogenase of Ralstonia eutropha Investigated by X-ray Absorption Spectroscopy: Insights into O2-Tolerant H2 Cleavage

“…3). In the oxidized MBH at pH 8.0, a pronounced increase of the primary edge maximum at ~8350 eV suggested additional terminal oxygen ligands at the Ni(II) (23,58,82,85) in the Ni ia -S state and therefore a substantially different site structure compared to Ni-B.…”

Reduction of Unusual Iron-Sulfur Clusters in the H2-sensing Regulatory Ni-Fe Hydrogenase from Ralstonia eutropha H16

“…The maxima of the XANES spectra of the RH WT were larger, and the pre-edge peak magnitudes and areas were smaller than in the RH stop , pointing to an average coordination of iron in the RH WT by less sulfur and more O/N ligands (32). For one-electron reduction of single-Fe(III) compounds with mixed O/N/S ligation of iron, a shift of the K-edge by about Ϫ2.5 eV may be expected (29,31,33).…”