Thermodynamic and kinetic properties of the outer membrane cytochrome OmcF, a key protein for extracellular electron transfer in Geobacter sulfurreducens

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Abstract

Gene knock-out studies on Geobacter sulfurreducens have shown that the monoheme c-type cytochrome OmcF is essential for the extracellular electron transfer pathways involved in the reduction of iron and uranium oxy-hydroxides, as well as, on electricity production in microbial fuel cells. A detailed electrochemical characterization of OmcF was performed for the first time, allowing attaining kinetics and thermodynamic data. The heterogeneous electron transfer rate constant was determined at pH 7 (0.16 ± 0.01 cm s−1) indicating that the protein displays high electron transfer efficiency compared to other monoheme cytochromes. The pH dependence of the redox potential indicates that the protein has an important redox-Bohr effect in the physiological pH range for G. sulfurreducens growth. The analysis of the structures of OmcF allowed us to assign the redox-Bohr centre to the side chain of His47 residue and its pKa values in the reduced and oxidized states were determined (pKox = 6.73; pKred = 7.55). The enthalpy, entropy and Gibbs free energy associated with the redox transaction were calculated, pointing the reduced form of the cytochrome as the most favourable. The data obtained indicate that G. sulfurreducens cells evolved to warrant a down-hill electron transfer from the periplasm to the outer-membrane associated cytochrome OmcF.

Original languageEnglish
Pages (from-to)1132-1137
Number of pages6
JournalBiochimica et Biophysica Acta - Bioenergetics
Volume1859
Issue number10
DOIs
Publication statusPublished - 1 Oct 2018

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Geobacter
Cytochromes
Thermodynamics
Oxidation-Reduction
Electrons
Membranes
Kinetics
Proteins
Hydroxides
Bioelectric Energy Sources
Cytochrome c Group
Microbial fuel cells
Periplasm
Electricity
Gastrin-Secreting Cells
Gene Knockout Techniques
Uranium
Entropy
Gibbs free energy
Enthalpy

Keywords

  • Bioelectrochemistry
  • Cytochrome
  • Electron transfer
  • Geobacter
  • Redox potential

Cite this

@article{4b3d4a3fc5b64e81bc98b6d2138ed8c9,
title = "Thermodynamic and kinetic properties of the outer membrane cytochrome OmcF, a key protein for extracellular electron transfer in Geobacter sulfurreducens",
abstract = "Gene knock-out studies on Geobacter sulfurreducens have shown that the monoheme c-type cytochrome OmcF is essential for the extracellular electron transfer pathways involved in the reduction of iron and uranium oxy-hydroxides, as well as, on electricity production in microbial fuel cells. A detailed electrochemical characterization of OmcF was performed for the first time, allowing attaining kinetics and thermodynamic data. The heterogeneous electron transfer rate constant was determined at pH 7 (0.16 ± 0.01 cm s−1) indicating that the protein displays high electron transfer efficiency compared to other monoheme cytochromes. The pH dependence of the redox potential indicates that the protein has an important redox-Bohr effect in the physiological pH range for G. sulfurreducens growth. The analysis of the structures of OmcF allowed us to assign the redox-Bohr centre to the side chain of His47 residue and its pKa values in the reduced and oxidized states were determined (pKox = 6.73; pKred = 7.55). The enthalpy, entropy and Gibbs free energy associated with the redox transaction were calculated, pointing the reduced form of the cytochrome as the most favourable. The data obtained indicate that G. sulfurreducens cells evolved to warrant a down-hill electron transfer from the periplasm to the outer-membrane associated cytochrome OmcF.",
keywords = "Bioelectrochemistry, Cytochrome, Electron transfer, Geobacter, Redox potential",
author = "Teixeira, {Liliana R.} and Dantas, {Joana M.} and Salgueiro, {Carlos A.} and Cordas, {Cristina M.}",
note = "Sem PDF conforme despacho. info:eu-repo/grantAgreement/FCT/5876/147412/PT# info:eu-repo/grantAgreement/FCT/5876/147258/PT# We are grateful to Prof. M. Schiffer, Dr. P.R. Pokkuluri and Dr. Y. Y. Londer (Argonne National Laboratory, USA) for the kind gift of the OmcF plasmid. This work was supported by Fundacao para a Ciencia e a Tecnologia (FCT-MCTES) through Radiation Biology and Biophysics Doctoral Training Programme (RaBBiT), PD/00193/2012, UID/FIS/00068/2013 (CEFITEC); PTDC/BBB-BQB/3554/2014 (to CAS), and scholarship grant number PD/BD/114445/2016 (to LRT). This work was also supported by Unidade de Ciencias Biomoleculares Aplicadas-UCIBIO which is financed by national funds from FCT/MEC (UID/Multi/04378/2013) and co-financed by the ERDF under the PT2020 Partnership Agreement (POCI-01-0145-FEDER-007728).",
year = "2018",
month = "10",
day = "1",
doi = "10.1016/j.bbabio.2018.07.007",
language = "English",
volume = "1859",
pages = "1132--1137",
journal = "Biochimica Et Biophysica Acta-Bioenergetics",
issn = "0005-2728",
publisher = "Elsevier Science B.V., Inc",
number = "10",

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TY - JOUR

T1 - Thermodynamic and kinetic properties of the outer membrane cytochrome OmcF, a key protein for extracellular electron transfer in Geobacter sulfurreducens

AU - Teixeira, Liliana R.

AU - Dantas, Joana M.

AU - Salgueiro, Carlos A.

AU - Cordas, Cristina M.

N1 - Sem PDF conforme despacho. info:eu-repo/grantAgreement/FCT/5876/147412/PT# info:eu-repo/grantAgreement/FCT/5876/147258/PT# We are grateful to Prof. M. Schiffer, Dr. P.R. Pokkuluri and Dr. Y. Y. Londer (Argonne National Laboratory, USA) for the kind gift of the OmcF plasmid. This work was supported by Fundacao para a Ciencia e a Tecnologia (FCT-MCTES) through Radiation Biology and Biophysics Doctoral Training Programme (RaBBiT), PD/00193/2012, UID/FIS/00068/2013 (CEFITEC); PTDC/BBB-BQB/3554/2014 (to CAS), and scholarship grant number PD/BD/114445/2016 (to LRT). This work was also supported by Unidade de Ciencias Biomoleculares Aplicadas-UCIBIO which is financed by national funds from FCT/MEC (UID/Multi/04378/2013) and co-financed by the ERDF under the PT2020 Partnership Agreement (POCI-01-0145-FEDER-007728).

PY - 2018/10/1

Y1 - 2018/10/1

N2 - Gene knock-out studies on Geobacter sulfurreducens have shown that the monoheme c-type cytochrome OmcF is essential for the extracellular electron transfer pathways involved in the reduction of iron and uranium oxy-hydroxides, as well as, on electricity production in microbial fuel cells. A detailed electrochemical characterization of OmcF was performed for the first time, allowing attaining kinetics and thermodynamic data. The heterogeneous electron transfer rate constant was determined at pH 7 (0.16 ± 0.01 cm s−1) indicating that the protein displays high electron transfer efficiency compared to other monoheme cytochromes. The pH dependence of the redox potential indicates that the protein has an important redox-Bohr effect in the physiological pH range for G. sulfurreducens growth. The analysis of the structures of OmcF allowed us to assign the redox-Bohr centre to the side chain of His47 residue and its pKa values in the reduced and oxidized states were determined (pKox = 6.73; pKred = 7.55). The enthalpy, entropy and Gibbs free energy associated with the redox transaction were calculated, pointing the reduced form of the cytochrome as the most favourable. The data obtained indicate that G. sulfurreducens cells evolved to warrant a down-hill electron transfer from the periplasm to the outer-membrane associated cytochrome OmcF.

AB - Gene knock-out studies on Geobacter sulfurreducens have shown that the monoheme c-type cytochrome OmcF is essential for the extracellular electron transfer pathways involved in the reduction of iron and uranium oxy-hydroxides, as well as, on electricity production in microbial fuel cells. A detailed electrochemical characterization of OmcF was performed for the first time, allowing attaining kinetics and thermodynamic data. The heterogeneous electron transfer rate constant was determined at pH 7 (0.16 ± 0.01 cm s−1) indicating that the protein displays high electron transfer efficiency compared to other monoheme cytochromes. The pH dependence of the redox potential indicates that the protein has an important redox-Bohr effect in the physiological pH range for G. sulfurreducens growth. The analysis of the structures of OmcF allowed us to assign the redox-Bohr centre to the side chain of His47 residue and its pKa values in the reduced and oxidized states were determined (pKox = 6.73; pKred = 7.55). The enthalpy, entropy and Gibbs free energy associated with the redox transaction were calculated, pointing the reduced form of the cytochrome as the most favourable. The data obtained indicate that G. sulfurreducens cells evolved to warrant a down-hill electron transfer from the periplasm to the outer-membrane associated cytochrome OmcF.

KW - Bioelectrochemistry

KW - Cytochrome

KW - Electron transfer

KW - Geobacter

KW - Redox potential

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U2 - 10.1016/j.bbabio.2018.07.007

DO - 10.1016/j.bbabio.2018.07.007

M3 - Article

VL - 1859

SP - 1132

EP - 1137

JO - Biochimica Et Biophysica Acta-Bioenergetics

JF - Biochimica Et Biophysica Acta-Bioenergetics

SN - 0005-2728

IS - 10

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