Interactions of Cu<inf>B</inf> with Carbon Monoxide in Cytochrome c Oxidase

Origin of the Anomalous Correlation between the Fe-CO and C-O Stretching Frequencies

Tsuyoshi Egawa, Jonah Haber, James A. Fee, Syun-Ru Yeh, Denis L. Rousseau

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4 Citations (Scopus)

Abstract

In heme-copper oxidases, the correlation curve between the iron-CO and C-O stretching vibrational modes (ν<inf>Fe-CO</inf> and ν<inf>C-O</inf>, respectively) is anomalous as compared to the correlation in other heme proteins. To extend the correlation curve, the resonance Raman (RR) and infrared (IR) spectra of the CO adducts of cytochrome ba<inf>3</inf> (ba<inf>3</inf>) from Thermus thermophilus were measured. The RR spectrum has two strong ν<inf>Fe-CO</inf> lines (508 and 515 cm<sup>-1</sup>) and a very weak line at 526 cm<sup>-1</sup>, and the IR spectrum has three ν<inf>C-O</inf> lines (1966, 1973, and 1981 cm<sup>-1</sup>), indicating the presence of multiple conformers. Employing photodissociation methods, the ν<inf>Fe-CO</inf> RR and ν<inf>C-O</inf> IR lines were assigned to each conformer, enabling the establishment of a reliable inverse correlation curve for the ν<inf>Fe-CO</inf> versus the ν<inf>C-O</inf> stretching frequencies. To determine the molecular basis of the correlation, a series of DFT calculations on 6-coordinate porphyrin-CO compounds and a model of the binuclear center of the heme-copper oxidases were carried out. The calculations demonstrated that the copper unit model caused significant mixing among porphyrin-CO molecular orbitals (MOs) that contribute to the Fe-C and C-O bonding interactions, and also indicated the presence of mixing between the d<inf>z</inf><sup>2</sup> orbital of the copper and MOs that are responsible for the ν<inf>Fe-CO</inf> vs ν<inf>C-O</inf> inverse correlation. Together, the spectroscopic and DFT results clarify the origin of the anomaly of ν<inf>Fe-CO</inf> and ν<inf>C-O</inf> frequencies in the heme-copper oxidases, a long-standing issue. (Graph Presented).

Original languageEnglish (US)
Pages (from-to)8509-8520
Number of pages12
JournalJournal of Physical Chemistry B
Volume119
Issue number27
DOIs
StatePublished - Jul 9 2015

Fingerprint

oxidase
cytochromes
Electron Transport Complex IV
Carbon Monoxide
Carbon monoxide
carbon monoxide
Stretching
Copper
copper
Porphyrins
Molecular orbitals
Infrared radiation
Discrete Fourier transforms
interactions
porphyrins
Heme
molecular orbitals
Photodissociation
curves
infrared spectra

ASJC Scopus subject areas

  • Physical and Theoretical Chemistry
  • Materials Chemistry
  • Surfaces, Coatings and Films

Cite this

@article{913ed723cd814213938c215957cfbadd,
title = "Interactions of CuB with Carbon Monoxide in Cytochrome c Oxidase: Origin of the Anomalous Correlation between the Fe-CO and C-O Stretching Frequencies",
abstract = "In heme-copper oxidases, the correlation curve between the iron-CO and C-O stretching vibrational modes (νFe-CO and νC-O, respectively) is anomalous as compared to the correlation in other heme proteins. To extend the correlation curve, the resonance Raman (RR) and infrared (IR) spectra of the CO adducts of cytochrome ba3 (ba3) from Thermus thermophilus were measured. The RR spectrum has two strong νFe-CO lines (508 and 515 cm-1) and a very weak line at 526 cm-1, and the IR spectrum has three νC-O lines (1966, 1973, and 1981 cm-1), indicating the presence of multiple conformers. Employing photodissociation methods, the νFe-CO RR and νC-O IR lines were assigned to each conformer, enabling the establishment of a reliable inverse correlation curve for the νFe-CO versus the νC-O stretching frequencies. To determine the molecular basis of the correlation, a series of DFT calculations on 6-coordinate porphyrin-CO compounds and a model of the binuclear center of the heme-copper oxidases were carried out. The calculations demonstrated that the copper unit model caused significant mixing among porphyrin-CO molecular orbitals (MOs) that contribute to the Fe-C and C-O bonding interactions, and also indicated the presence of mixing between the dz2 orbital of the copper and MOs that are responsible for the νFe-CO vs νC-O inverse correlation. Together, the spectroscopic and DFT results clarify the origin of the anomaly of νFe-CO and νC-O frequencies in the heme-copper oxidases, a long-standing issue. (Graph Presented).",
author = "Tsuyoshi Egawa and Jonah Haber and Fee, {James A.} and Syun-Ru Yeh and Rousseau, {Denis L.}",
year = "2015",
month = "7",
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doi = "10.1021/acs.jpcb.5b04444",
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TY - JOUR

T1 - Interactions of CuB with Carbon Monoxide in Cytochrome c Oxidase

T2 - Origin of the Anomalous Correlation between the Fe-CO and C-O Stretching Frequencies

AU - Egawa, Tsuyoshi

AU - Haber, Jonah

AU - Fee, James A.

AU - Yeh, Syun-Ru

AU - Rousseau, Denis L.

PY - 2015/7/9

Y1 - 2015/7/9

N2 - In heme-copper oxidases, the correlation curve between the iron-CO and C-O stretching vibrational modes (νFe-CO and νC-O, respectively) is anomalous as compared to the correlation in other heme proteins. To extend the correlation curve, the resonance Raman (RR) and infrared (IR) spectra of the CO adducts of cytochrome ba3 (ba3) from Thermus thermophilus were measured. The RR spectrum has two strong νFe-CO lines (508 and 515 cm-1) and a very weak line at 526 cm-1, and the IR spectrum has three νC-O lines (1966, 1973, and 1981 cm-1), indicating the presence of multiple conformers. Employing photodissociation methods, the νFe-CO RR and νC-O IR lines were assigned to each conformer, enabling the establishment of a reliable inverse correlation curve for the νFe-CO versus the νC-O stretching frequencies. To determine the molecular basis of the correlation, a series of DFT calculations on 6-coordinate porphyrin-CO compounds and a model of the binuclear center of the heme-copper oxidases were carried out. The calculations demonstrated that the copper unit model caused significant mixing among porphyrin-CO molecular orbitals (MOs) that contribute to the Fe-C and C-O bonding interactions, and also indicated the presence of mixing between the dz2 orbital of the copper and MOs that are responsible for the νFe-CO vs νC-O inverse correlation. Together, the spectroscopic and DFT results clarify the origin of the anomaly of νFe-CO and νC-O frequencies in the heme-copper oxidases, a long-standing issue. (Graph Presented).

AB - In heme-copper oxidases, the correlation curve between the iron-CO and C-O stretching vibrational modes (νFe-CO and νC-O, respectively) is anomalous as compared to the correlation in other heme proteins. To extend the correlation curve, the resonance Raman (RR) and infrared (IR) spectra of the CO adducts of cytochrome ba3 (ba3) from Thermus thermophilus were measured. The RR spectrum has two strong νFe-CO lines (508 and 515 cm-1) and a very weak line at 526 cm-1, and the IR spectrum has three νC-O lines (1966, 1973, and 1981 cm-1), indicating the presence of multiple conformers. Employing photodissociation methods, the νFe-CO RR and νC-O IR lines were assigned to each conformer, enabling the establishment of a reliable inverse correlation curve for the νFe-CO versus the νC-O stretching frequencies. To determine the molecular basis of the correlation, a series of DFT calculations on 6-coordinate porphyrin-CO compounds and a model of the binuclear center of the heme-copper oxidases were carried out. The calculations demonstrated that the copper unit model caused significant mixing among porphyrin-CO molecular orbitals (MOs) that contribute to the Fe-C and C-O bonding interactions, and also indicated the presence of mixing between the dz2 orbital of the copper and MOs that are responsible for the νFe-CO vs νC-O inverse correlation. Together, the spectroscopic and DFT results clarify the origin of the anomaly of νFe-CO and νC-O frequencies in the heme-copper oxidases, a long-standing issue. (Graph Presented).

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SN - 1520-6106

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