Structure and coordination of CuB in the Acidianus ambivalens aa3 quinol oxidase heme-copper center

Tiago M. Bandeiras, Manuel M. Pereira, Miguel Teixeira, Pierre Moenne-Loccoz, Ninian Blackburn

Research output: Contribution to journalArticle

3 Citations (Scopus)

Abstract

The coordination environment of the CuB center of the quinol oxidase from Acidianus ambivalens, a type B heme-copper oxygen reductase, was investigated by Fourier transform (FT) IR and extended X-ray absorption fine structure (EXAFS) spectroscopy. The comparative structural chemistry of dinuclear Fe-Cu sites of the different types of oxygen reductases is of great interest. Fully reduced A. ambivalens quinol oxidase binds CO at the heme a 3 center, with ν(CO)=1,973 cm-1. On photolysis, the CO migrated to the CuB center, forming a Cu B I -CO complex with ν(CO)=2,047 cm-1. Raising the temperature of the samples to 25°C did not result in a total loss of signal in the FTIR difference spectrum although the intensity of these signals was reduced sevenfold. This observation is consistent with a large energy barrier against the geminate rebinding of CO to the heme iron from CuB, a restricted limited access at the active-site pocket for a second binding, and a kinetically stable CuB-CO complex in A. ambivalens aa 3. The Cu B center was probed in a number of different states using EXAFS spectroscopy. The oxidized state was best simulated by three histidines and a solvent O scatterer. On reduction, the site became three-coordinate, but in contrast to the bo 3 enzyme, there was no evidence for heterogeneity of binding of the coordinated histidines. The CuB centers in both the oxidized and the reduced enzymes also appeared to contain substoichiometric amounts (0.2 mol equiv) of nonlabile chloride ion. EXAFS data of the reduced carbonylated enzyme showed no difference between dark and photolyzed forms. The spectra could be well fit by 2.5 imidazoles, 0.5 Cl- and 0.5 CO ligands. This arrangement of scatterers would be consistent with about half the sites remaining as unligated Cu(his)3 and half being converted to Cu(his)2Cl-CO, a 50/50 ratio of Cu(his)2Cl - and Cu(his)3CO, or some combination of these formulations.

Original languageEnglish (US)
Pages (from-to)625-635
Number of pages11
JournalJournal of Biological Inorganic Chemistry
Volume10
Issue number6
DOIs
StatePublished - Oct 2005

Fingerprint

Acidianus
Carbon Monoxide
Heme
Copper
Extended X ray absorption fine structure spectroscopy
X-Rays
Histidine
Spectrum Analysis
Oxidoreductases
Enzymes
Imidazoles
Oxygen
duroquinol oxidase
Photolysis
Energy barriers
X ray absorption
Fourier Analysis
Fourier Transform Infrared Spectroscopy
Chlorides
Catalytic Domain

Keywords

  • Acidianus ambivalens
  • Cytochrome c oxidase
  • Extremophile
  • Heme-copper
  • Quinol oxidase

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Biochemistry

Cite this

Structure and coordination of CuB in the Acidianus ambivalens aa3 quinol oxidase heme-copper center. / Bandeiras, Tiago M.; Pereira, Manuel M.; Teixeira, Miguel; Moenne-Loccoz, Pierre; Blackburn, Ninian.

In: Journal of Biological Inorganic Chemistry, Vol. 10, No. 6, 10.2005, p. 625-635.

Research output: Contribution to journalArticle

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abstract = "The coordination environment of the CuB center of the quinol oxidase from Acidianus ambivalens, a type B heme-copper oxygen reductase, was investigated by Fourier transform (FT) IR and extended X-ray absorption fine structure (EXAFS) spectroscopy. The comparative structural chemistry of dinuclear Fe-Cu sites of the different types of oxygen reductases is of great interest. Fully reduced A. ambivalens quinol oxidase binds CO at the heme a 3 center, with ν(CO)=1,973 cm-1. On photolysis, the CO migrated to the CuB center, forming a Cu B I -CO complex with ν(CO)=2,047 cm-1. Raising the temperature of the samples to 25°C did not result in a total loss of signal in the FTIR difference spectrum although the intensity of these signals was reduced sevenfold. This observation is consistent with a large energy barrier against the geminate rebinding of CO to the heme iron from CuB, a restricted limited access at the active-site pocket for a second binding, and a kinetically stable CuB-CO complex in A. ambivalens aa 3. The Cu B center was probed in a number of different states using EXAFS spectroscopy. The oxidized state was best simulated by three histidines and a solvent O scatterer. On reduction, the site became three-coordinate, but in contrast to the bo 3 enzyme, there was no evidence for heterogeneity of binding of the coordinated histidines. The CuB centers in both the oxidized and the reduced enzymes also appeared to contain substoichiometric amounts (0.2 mol equiv) of nonlabile chloride ion. EXAFS data of the reduced carbonylated enzyme showed no difference between dark and photolyzed forms. The spectra could be well fit by 2.5 imidazoles, 0.5 Cl- and 0.5 CO ligands. This arrangement of scatterers would be consistent with about half the sites remaining as unligated Cu(his)3 and half being converted to Cu(his)2Cl-CO, a 50/50 ratio of Cu(his)2Cl - and Cu(his)3CO, or some combination of these formulations.",
keywords = "Acidianus ambivalens, Cytochrome c oxidase, Extremophile, Heme-copper, Quinol oxidase",
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T1 - Structure and coordination of CuB in the Acidianus ambivalens aa3 quinol oxidase heme-copper center

AU - Bandeiras, Tiago M.

AU - Pereira, Manuel M.

AU - Teixeira, Miguel

AU - Moenne-Loccoz, Pierre

AU - Blackburn, Ninian

PY - 2005/10

Y1 - 2005/10

N2 - The coordination environment of the CuB center of the quinol oxidase from Acidianus ambivalens, a type B heme-copper oxygen reductase, was investigated by Fourier transform (FT) IR and extended X-ray absorption fine structure (EXAFS) spectroscopy. The comparative structural chemistry of dinuclear Fe-Cu sites of the different types of oxygen reductases is of great interest. Fully reduced A. ambivalens quinol oxidase binds CO at the heme a 3 center, with ν(CO)=1,973 cm-1. On photolysis, the CO migrated to the CuB center, forming a Cu B I -CO complex with ν(CO)=2,047 cm-1. Raising the temperature of the samples to 25°C did not result in a total loss of signal in the FTIR difference spectrum although the intensity of these signals was reduced sevenfold. This observation is consistent with a large energy barrier against the geminate rebinding of CO to the heme iron from CuB, a restricted limited access at the active-site pocket for a second binding, and a kinetically stable CuB-CO complex in A. ambivalens aa 3. The Cu B center was probed in a number of different states using EXAFS spectroscopy. The oxidized state was best simulated by three histidines and a solvent O scatterer. On reduction, the site became three-coordinate, but in contrast to the bo 3 enzyme, there was no evidence for heterogeneity of binding of the coordinated histidines. The CuB centers in both the oxidized and the reduced enzymes also appeared to contain substoichiometric amounts (0.2 mol equiv) of nonlabile chloride ion. EXAFS data of the reduced carbonylated enzyme showed no difference between dark and photolyzed forms. The spectra could be well fit by 2.5 imidazoles, 0.5 Cl- and 0.5 CO ligands. This arrangement of scatterers would be consistent with about half the sites remaining as unligated Cu(his)3 and half being converted to Cu(his)2Cl-CO, a 50/50 ratio of Cu(his)2Cl - and Cu(his)3CO, or some combination of these formulations.

AB - The coordination environment of the CuB center of the quinol oxidase from Acidianus ambivalens, a type B heme-copper oxygen reductase, was investigated by Fourier transform (FT) IR and extended X-ray absorption fine structure (EXAFS) spectroscopy. The comparative structural chemistry of dinuclear Fe-Cu sites of the different types of oxygen reductases is of great interest. Fully reduced A. ambivalens quinol oxidase binds CO at the heme a 3 center, with ν(CO)=1,973 cm-1. On photolysis, the CO migrated to the CuB center, forming a Cu B I -CO complex with ν(CO)=2,047 cm-1. Raising the temperature of the samples to 25°C did not result in a total loss of signal in the FTIR difference spectrum although the intensity of these signals was reduced sevenfold. This observation is consistent with a large energy barrier against the geminate rebinding of CO to the heme iron from CuB, a restricted limited access at the active-site pocket for a second binding, and a kinetically stable CuB-CO complex in A. ambivalens aa 3. The Cu B center was probed in a number of different states using EXAFS spectroscopy. The oxidized state was best simulated by three histidines and a solvent O scatterer. On reduction, the site became three-coordinate, but in contrast to the bo 3 enzyme, there was no evidence for heterogeneity of binding of the coordinated histidines. The CuB centers in both the oxidized and the reduced enzymes also appeared to contain substoichiometric amounts (0.2 mol equiv) of nonlabile chloride ion. EXAFS data of the reduced carbonylated enzyme showed no difference between dark and photolyzed forms. The spectra could be well fit by 2.5 imidazoles, 0.5 Cl- and 0.5 CO ligands. This arrangement of scatterers would be consistent with about half the sites remaining as unligated Cu(his)3 and half being converted to Cu(his)2Cl-CO, a 50/50 ratio of Cu(his)2Cl - and Cu(his)3CO, or some combination of these formulations.

KW - Acidianus ambivalens

KW - Cytochrome c oxidase

KW - Extremophile

KW - Heme-copper

KW - Quinol oxidase

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