Spectroscopic studies of 1-aminocyclopropane-1-carboxylic acid oxidase: molecular mechanism and CO(2) activation in the biosynthesis of ethylene

J Am Chem Soc. 2002 May 1;124(17):4602-9. doi: 10.1021/ja017250f.

Abstract

1-Aminocyclopropane-1-carboxylic acid (ACC) oxidase (ACCO) catalyzes the last step in the biosynthesis of the gaseous plant hormone ethylene, which is involved in development, including germination, fruit ripening, and senescence. ACCO is a mononuclear non-heme ferrous enzyme that couples the oxidation of the cosubstrate ascorbate to the oxidation of substrate ACC by dioxygen. In addition to substrate and cosubstrate, ACCO requires the activator CO(2) for continuous turnover. NIR circular dichroism and magnetic circular dichroism spectroscopies have been used to probe the geometric and electronic structure of the ferrous active site in ACCO to obtain molecular-level insight into its catalytic mechanism. Resting ACCO/Fe(II) is coordinatively saturated (six-coordinate). In the presence of CO(2), one ferrous ligand is displaced to yield a five-coordinate site only when both the substrate ACC and cosubstrate ascorbate are bound to the enzyme. The open coordination position allows rapid O(2) activation for the oxidation of both substrates. In the absence of CO(2), ACC binding alone converts the site to five-coordinate, which would react with O(2) in the absence of ascorbate and quickly deactivate the enzyme. These studies show that ACCO employs a general strategy similar to other non-heme iron enzymes in terms of opening iron coordination sites at the appropriate time in the reaction cycle and define the role of CO(2) as stabilizing the six-coordinate ACCO/Fe(II)/ACC complex, thus preventing the uncoupled reaction that inactivates the enzyme.

Publication types

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

MeSH terms

  • Amino Acid Oxidoreductases / biosynthesis
  • Amino Acid Oxidoreductases / chemistry*
  • Amino Acid Oxidoreductases / genetics
  • Amino Acid Oxidoreductases / metabolism
  • Ascorbic Acid / chemistry
  • Ascorbic Acid / metabolism
  • Binding Sites
  • Carbon Dioxide / chemistry
  • Carbon Dioxide / metabolism*
  • Catalysis
  • Circular Dichroism
  • Escherichia coli / enzymology
  • Escherichia coli / genetics
  • Ethylenes / metabolism*
  • Ferrous Compounds / chemistry
  • Ferrous Compounds / metabolism
  • Ketoglutaric Acids / chemistry
  • Ketoglutaric Acids / metabolism
  • Spectroscopy, Near-Infrared

Substances

  • Ethylenes
  • Ferrous Compounds
  • Ketoglutaric Acids
  • Carbon Dioxide
  • ethylene
  • Amino Acid Oxidoreductases
  • 1-aminocyclopropane-1-carboxylic acid oxidase
  • Ascorbic Acid