Electronic structure of iron(II)-porphyrin nitroxyl complexes: molecular mechanism of fungal nitric oxide reductase (P450nor)

J Comput Chem. 2006 Sep;27(12):1338-51. doi: 10.1002/jcc.20400.

Abstract

Density functional calculations are employed to investigate key intermediates of the catalytic cycle of fungal nitric oxide reductase (P450nor). The formal Fe(II)-nitroxyl species Fe(II)--NO/(-) can principally exist in the two spin-states S = 0 and S = 1. In the S = 0 case, a very covalent Fe--NO sigma bond is present, which leads to an electronic structure description that is actually intermediate between Fe(I)--NO and Fe(II)--NO(-). In contrast, the S = 1 case shows a ferrous Fe(II)--NO complex with the extra electron being stored in the pi system of the porphyrin ligand. Importantly, the Fe(II)--NO/(-) species are very basic. The electronic structures and spectroscopic properties of the corresponding N- and O-protonated forms are very different, and unequivocally show that the Mb-HNO adduct (Mb-Myoglobin) prepared by farmer and coworkers is in fact N-protonated. The presence of an axial thiolate ligand enables a second protonation leading to the corresponding Fe(IV)--NHOH- species, which is identified with the catalytically active intermediate I of P450nor. This species reacts with a second molecule of NO by initial electron transfer from NO to Fe(IV) followed by addition of NO+ forming an N--N bond. This is accompanied by an energetically very favorable intramolecular proton transfer leading to the generation of a quite stable Fe(III)--N(OH)(NOH) complex. This way, the enzyme is able to produce dimerized HNO under very controlled conditions and to prevent loss of this ligand from Fe(III). The energetically disfavoured tautomer Fe(III)--N(OH2)(NO) is the catalytically productive species that spontaneously cleaves the N--OH2 bond forming N2O and H2O in a highly exergonic reaction.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Fungi / enzymology
  • Iron / chemistry*
  • Iron / metabolism
  • Models, Molecular
  • Molecular Structure
  • Nitrogen Oxides / chemistry*
  • Nitrogen Oxides / metabolism
  • Oxidoreductases / chemistry
  • Oxidoreductases / metabolism*
  • Porphyrins / chemistry*
  • Porphyrins / metabolism

Substances

  • Nitrogen Oxides
  • Porphyrins
  • Iron
  • Oxidoreductases
  • nitric-oxide reductase
  • nitroxyl