Interactions between heme d and heme b595 in quinol oxidase bd from Escherichia coli

A photoselection study using femtosecond spectroscopy

Vitaliy B. Borisov, Ursula Liebl, Fabrice Rappaport, Jean Louis Martin, Jie Zhang, Robert B. Gennis, Alexander A. Konstantinov, Marten H. Vos

Research output: Contribution to journalArticle

52 Citations (Scopus)

Abstract

Femtosecond spectroscopy was performed on CO-liganded (fully reduced and mixed-valence states) and O2-liganded quinol oxidase bd from Escherichia coli. Substantial polarization effects, unprecedented for optical studies of heme proteins, were observed in the CO photodissociation spectra, implying interactions between heme d (the chlorin ligand binding site) and the close-lying heme b595 on the picosecond time scale; this general result is fully consistent with previous work [Vos, M. H., Borisov, V. B., Liebl, U., Martin, J.-L., and Konstantinov, A. A. (2000) Proc. Natl. Acad. Sci. U.S.A. 97, 1554-1559]. Analysis of the data obtained under isotropic and anisotropic polarization conditions and additional flash photolysis nanosecond experiments on a mutant of cytochrome bd mostly lacking heme b595 allow to attribute the features in the well-known but unusual CO dissociation spectrum of cytochrome bd to individual heme d and heme b595 transitions. This renders it possible to compare the spectra of CO dissociation from reduced and mixed-valence cytochrome bd under static conditions and on a picosecond time scale in much more detail than previously possible. CO binding/dissociation from heme d is shown to perturb ferrous heme b595, causing induction/loss of an absorption band centered at ∼435 nm. In addition, the CO photodissociation-induced absorption changes at 50 ps reveal a bathochromic shift of ferrous heme b595 relative to the static spectrum. No evidence for transient binding of CO to heme b595 after dissociation from heme d is found in the picosecond time range. The yield of CO photodissociation from heme d on a time scale of < 15 ps is found to be diminished more than 3-fold when heme b595 is oxidized rather than reduced. In contrast to other known heme proteins, molecular oxygen cannot be photodissociated from the mixed-valence cytochrome bd at all, indicating a unique structural and electronic configuration of the diheme active site in the enzyme.

Original languageEnglish (US)
Pages (from-to)1654-1662
Number of pages9
JournalBiochemistry
Volume41
Issue number5
DOIs
StatePublished - Feb 5 2002
Externally publishedYes

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Carbon Monoxide
Escherichia coli
Spectrum Analysis
Spectroscopy
Cytochromes
Photodissociation
Hemeproteins
Polarization
heme b(595)
duroquinol oxidase
heme d
Molecular oxygen
Photolysis
Absorption spectra
Catalytic Domain
Binding Sites
Oxygen
Ligands
Enzymes

ASJC Scopus subject areas

  • Biochemistry

Cite this

Interactions between heme d and heme b595 in quinol oxidase bd from Escherichia coli : A photoselection study using femtosecond spectroscopy. / Borisov, Vitaliy B.; Liebl, Ursula; Rappaport, Fabrice; Martin, Jean Louis; Zhang, Jie; Gennis, Robert B.; Konstantinov, Alexander A.; Vos, Marten H.

In: Biochemistry, Vol. 41, No. 5, 05.02.2002, p. 1654-1662.

Research output: Contribution to journalArticle

Borisov, VB, Liebl, U, Rappaport, F, Martin, JL, Zhang, J, Gennis, RB, Konstantinov, AA & Vos, MH 2002, 'Interactions between heme d and heme b595 in quinol oxidase bd from Escherichia coli: A photoselection study using femtosecond spectroscopy', Biochemistry, vol. 41, no. 5, pp. 1654-1662. https://doi.org/10.1021/bi0158019
Borisov, Vitaliy B. ; Liebl, Ursula ; Rappaport, Fabrice ; Martin, Jean Louis ; Zhang, Jie ; Gennis, Robert B. ; Konstantinov, Alexander A. ; Vos, Marten H. / Interactions between heme d and heme b595 in quinol oxidase bd from Escherichia coli : A photoselection study using femtosecond spectroscopy. In: Biochemistry. 2002 ; Vol. 41, No. 5. pp. 1654-1662.
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abstract = "Femtosecond spectroscopy was performed on CO-liganded (fully reduced and mixed-valence states) and O2-liganded quinol oxidase bd from Escherichia coli. Substantial polarization effects, unprecedented for optical studies of heme proteins, were observed in the CO photodissociation spectra, implying interactions between heme d (the chlorin ligand binding site) and the close-lying heme b595 on the picosecond time scale; this general result is fully consistent with previous work [Vos, M. H., Borisov, V. B., Liebl, U., Martin, J.-L., and Konstantinov, A. A. (2000) Proc. Natl. Acad. Sci. U.S.A. 97, 1554-1559]. Analysis of the data obtained under isotropic and anisotropic polarization conditions and additional flash photolysis nanosecond experiments on a mutant of cytochrome bd mostly lacking heme b595 allow to attribute the features in the well-known but unusual CO dissociation spectrum of cytochrome bd to individual heme d and heme b595 transitions. This renders it possible to compare the spectra of CO dissociation from reduced and mixed-valence cytochrome bd under static conditions and on a picosecond time scale in much more detail than previously possible. CO binding/dissociation from heme d is shown to perturb ferrous heme b595, causing induction/loss of an absorption band centered at ∼435 nm. In addition, the CO photodissociation-induced absorption changes at 50 ps reveal a bathochromic shift of ferrous heme b595 relative to the static spectrum. No evidence for transient binding of CO to heme b595 after dissociation from heme d is found in the picosecond time range. The yield of CO photodissociation from heme d on a time scale of < 15 ps is found to be diminished more than 3-fold when heme b595 is oxidized rather than reduced. In contrast to other known heme proteins, molecular oxygen cannot be photodissociated from the mixed-valence cytochrome bd at all, indicating a unique structural and electronic configuration of the diheme active site in the enzyme.",
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AU - Gennis, Robert B.

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