Bis-Fe(IV): nature's sniper for long-range oxidation

J Biol Inorg Chem. 2014 Oct;19(7):1057-67. doi: 10.1007/s00775-014-1123-8. Epub 2014 Apr 11.

Abstract

Iron-dependent enzymes are prevalent in nature and participate in a wide range of biological redox activities. Frequently, high-valence iron intermediates are involved in the catalytic events of iron-dependent enzymes, especially when the activation of peroxide or molecular oxygen is involved. Building on the fundamental framework of iron-oxygen chemistry, these reactive intermediates constantly attract significant attention from the enzymology community. During the past few decades, tremendous efforts from a number of laboratories have been dedicated to the capture and characterization of these intermediates to improve mechanistic understandings. In 2008, an unprecedented bis-Fe(IV) intermediate was reported in a c-type diheme enzyme, MauG, which is involved in the maturation of a tryptophan tryptophylquinone cofactor of methylamine dehydrogenase. This intermediate, although chemically equivalent to well-characterized high-valence iron intermediates, such as compound I, compound ES, and intermediate Q in methane monooxygenase, as well as the hypothetical Fe(V) species in Rieske non-heme oxygenases, is orders of magnitude more stable than these other high-valence species in the absence of its primary substrate. It has recently been discovered that the bis-Fe(IV) intermediate exhibits a unique near-IR absorption feature which has been attributed to a novel charge-resonance phenomenon. This review compares the properties of MauG with structurally related enzymes, summarizes the current knowledge of this new high-valence iron intermediate, including its chemical origin and structural basis, explores the formation and consequences of charge resonance, and recounts the long-range catalytic mechanism in which bis-Fe(IV) participates. Biological strategies for storing oxidizing equivalents with iron ions are also discussed.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.
  • Review

MeSH terms

  • Indolequinones / chemistry
  • Indolequinones / metabolism*
  • Iron Compounds / chemistry
  • Iron Compounds / metabolism
  • Models, Molecular
  • Oxidation-Reduction
  • Oxidoreductases Acting on CH-NH Group Donors / chemistry*
  • Oxidoreductases Acting on CH-NH Group Donors / metabolism*
  • Paracoccus / chemistry
  • Paracoccus / enzymology*
  • Paracoccus / metabolism
  • Tryptophan / analogs & derivatives*
  • Tryptophan / chemistry
  • Tryptophan / metabolism

Substances

  • Indolequinones
  • Iron Compounds
  • tryptophan tryptophylquinone
  • Tryptophan
  • methylamine dehydrogenase
  • Oxidoreductases Acting on CH-NH Group Donors