Characterization of the inner membrane cytochrome ImcH from Geobacter reveals its importance for extracellular electron transfer and energy conservation

Andreia I. Pimenta; Catarina M. Paquete; Leonor Morgado; Marcus J. Edwards; THOMAS A. CLARKE; Carlos A. Salgueiro; Inês A. C. Pereira; Américo G. Duarte

doi:10.1002/pro.4796

journal article Oct 26, 2023

Characterization of the inner membrane cytochrome ImcH from Geobacter reveals its importance for extracellular electron transfer and energy conservation

Andreia I. Pimenta

Catarina M. Paquete

Leonor Morgado Marcus J. Edwards

THOMAS A. CLARKE

Carlos A. Salgueiro Inês A. C. Pereira

Américo G. Duarte

Protein Science Vol. 32 No. 11 · Wiley

View at Publisher Save 10.1002/pro.4796

Abstract

AbstractElectroactive bacteria combine the oxidation of carbon substrates with an extracellular electron transfer (EET) process that discharges electrons to an electron acceptor outside the cell. This process involves electron transfer through consecutive redox proteins that efficiently connect the inner membrane to the cell exterior. In this study, we isolated and characterized the quinone‐interacting membrane cytochrome c ImcH from Geobacter sulfurreducens, which is involved in the EET process to high redox potential acceptors. Spectroscopic and electrochemical studies show that ImcH hemes have low midpoint redox potentials, ranging from −150 to −358 mV, and connect the oxidation of the quinol‐pool to EET, transferring electrons to the highly abundant periplasmic cytochrome PpcA with higher affinity than to its homologues. Despite the larger number of hemes and transmembrane helices, the ImcH structural model has similarities with the NapC/NirT/NrfH superfamily, namely the presence of a quinone‐binding site on the P‐side of the membrane. In addition, the first heme, likely involved on the quinol oxidation, has apparently an unusual His/Gln coordination. Our work suggests that ImcH is electroneutral and transfers electrons and protons to the same side of the membrane, contributing to the maintenance of a proton motive force and playing a central role in recycling the menaquinone pool.

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Details

Published: Oct 26, 2023
Vol/Issue: 32(11)
License: View

Authors

A

Andreia I. Pimenta

Instituto de Tecnologia Química e Biológica António Xavier Universidade Nova de Lisboa Oeiras Portugal

C

Catarina M. Paquete

Instituto de Tecnologia Química e Biológica António Xavier Universidade Nova de Lisboa Oeiras Portugal

L

Leonor Morgado

Associate Laboratory i4HB—Institute for Health and Bioeconomy, NOVA School of Science and Technology Universidade NOVA de Lisboa Caparica Portugal; UCIBIO—Applied Molecular Biosciences Unit, Department of Chemistry, NOVA School of Science and Technology Universidade NOVA de Lisboa Caparica Portugal

M

Marcus J. Edwards

School of Life Sciences University of Essex Colchester UK

T

THOMAS A. CLARKE

Centre for Molecular and Structural Biochemistry, School of Biological Sciences University of East Anglia Norwich UK

C

Carlos A. Salgueiro

Associate Laboratory i4HB—Institute for Health and Bioeconomy, NOVA School of Science and Technology Universidade NOVA de Lisboa Caparica Portugal; UCIBIO—Applied Molecular Biosciences Unit, Department of Chemistry, NOVA School of Science and Technology Universidade NOVA de Lisboa Caparica Portugal

I

Inês A. C. Pereira

Instituto de Tecnologia Química e Biológica António Xavier Universidade Nova de Lisboa Oeiras Portugal

A

Américo G. Duarte

Instituto de Tecnologia Química e Biológica António Xavier Universidade Nova de Lisboa Oeiras Portugal

Funding

Applied Molecular Biosciences Unit Award: UIDB/04378/2020

Cite This Article

Andreia I. Pimenta, Catarina M. Paquete, Leonor Morgado, et al. (2023). Characterization of the inner membrane cytochrome ImcH from Geobacter reveals its importance for extracellular electron transfer and energy conservation. Protein Science, 32(11). https://doi.org/10.1002/pro.4796

Characterization of the inner membrane cytochrome ImcH from Geobacter reveals its importance for extracellular electron transfer and energy conservation

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