Spectroscopic and computational studies of Ni3+ complexes with mixed S/N ligation: implications for the active site of nickel superoxide dismutase

Inorg Chem. 2007 Oct 15;46(21):8511-23. doi: 10.1021/ic061237k. Epub 2007 Feb 17.

Abstract

Both Ni-containing superoxide dismutase (NiSOD) and NiFe hydrogenases feature thiolate-rich active sites that are capable of stabilizing the Ni3+ oxidation state in catalytically relevant species. In an effort to better understand the role of Ni(3+)-S bonding interactions in these metalloenzymes, we have employed various spectroscopic and computational methods to probe the geometric and electronic structures of three Ni(3+) complexes with mixed S/N ligation: [Ni(3+)(pdtc)(2)]- (1), [Ni(3+)(emb)]- (2), and [Ni(3+)(ema)]- (3) [where pdtc is pyridine-2,6-bis(monothiocarboxylate) and emb and ema are the tetraanions of N,N'-ethylenebis(o-mercaptobenzamide) and N,N'-ethylenebis(2-mercaptoacetamide), respectively]. Each complex has been examined with electronic absorption, magnetic circular dichroism, electron paramagnetic resonance, and resonance Raman (rR) spectroscopies. Detailed assignments of the features observed in the corresponding spectra have been established within the framework of density functional theory calculations that provide remarkably accurate reproductions of the absorption spectra, g values, and vibrational frequencies. Collectively, our spectroscopic and computational studies have yielded experimentally validated electronic-structure descriptions for 1-3 that provide significant insights into the nature of the Ni(3+)-S bonding interactions. Additionally, the results obtained in these studies reveal that the thermochromism observed for 2 is due to the formation of a dimeric species at reduced temperatures, the structure of which has been determined through computational analysis of viable dimer models. Finally, we have employed the framework established in our spectroscopic and computational studies of the Ni(3+) models to carry out a detailed analysis of our rR data of NiSOD obtained previously. Our results indicate that the Ni(3+)-S bonds in oxidized NiSOD are significantly stronger than those in 1-3 due to the unique mixed amine/amide ligation that is present at the enzyme active site.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Binding Sites
  • Catalysis
  • Chemistry / methods*
  • Dimerization
  • Electron Spin Resonance Spectroscopy
  • Models, Chemical
  • Molecular Conformation
  • Nickel / analysis*
  • Nickel / chemistry
  • Oxidation-Reduction
  • Software
  • Spectrophotometry / methods*
  • Spectrum Analysis, Raman / methods
  • Superoxide Dismutase / chemistry*
  • Temperature

Substances

  • Nickel
  • Superoxide Dismutase