A map of dielectric heterogeneity in a membrane protein: the hetero-oligomeric cytochrome b6f complex.

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TitleA map of dielectric heterogeneity in a membrane protein: the hetero-oligomeric cytochrome b6f complex.
Publication TypeJournal Article
Year of Publication2014
AuthorsS Hasan, S, Zakharov, SD, Chauvet, A, Stadnytskyi, V, Savikhin, S, Cramer, WA
JournalJ Phys Chem B
Volume118
Issue24
Pagination6614-25
Date Published2014 Jun 19
ISSN1520-5207
KeywordsCircular Dichroism, Cytochrome b6f Complex, Dithionite, Electron Transport, Heme, Membrane Proteins, Oxidation-Reduction, Plant Leaves, Protein Structure, Tertiary, Quinones, Spinacia oleracea, Static Electricity, Temperature
Abstract

The cytochrome b6f complex, a member of the cytochrome bc family that mediates energy transduction in photosynthetic and respiratory membranes, is a hetero-oligomeric complex that utilizes two pairs of b-hemes in a symmetric dimer to accomplish trans-membrane electron transfer, quinone oxidation-reduction, and generation of a proton electrochemical potential. Analysis of electron storage in this pathway, utilizing simultaneous measurement of heme reduction, and of circular dichroism (CD) spectra, to assay heme-heme interactions, implies a heterogeneous distribution of the dielectric constants that mediate electrostatic interactions between the four hemes in the complex. Crystallographic information was used to determine the identity of the interacting hemes. The Soret band CD signal is dominated by excitonic interaction between the intramonomer b-hemes, bn and bp, on the electrochemically negative and positive sides of the complex. Kinetic data imply that the most probable pathway for transfer of the two electrons needed for quinone oxidation-reduction utilizes this intramonomer heme pair, contradicting the expectation based on heme redox potentials and thermodynamics, that the two higher potential hemes bn on different monomers would be preferentially reduced. Energetically preferred intramonomer electron storage of electrons on the intramonomer b-hemes is found to require heterogeneity of interheme dielectric constants. Relative to the medium separating the two higher potential hemes bn, a relatively large dielectric constant must exist between the intramonomer b-hemes, allowing a smaller electrostatic repulsion between the reduced hemes. Heterogeneity of dielectric constants is an additional structure-function parameter of membrane protein complexes.

DOI10.1021/jp501165k
Alternate JournalJ Phys Chem B
PubMed ID24867491
PubMed Central IDPMC4067154
Grant ListR01 GM038323 / GM / NIGMS NIH HHS / United States
R56 GM038323 / GM / NIGMS NIH HHS / United States
GM-038323 / GM / NIGMS NIH HHS / United States