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Electron Flow From the Inner Membrane Towards the Cell Exterior in Geobacter sulfurreducens: Biochemical Characterization of Cytochrome CbcL

Exoelectrogenic microorganisms are in the spotlight due to their unique respiratory mechanisms and potential applications in distinct biotechnological fields, including bioremediation, bioenergy production and microbial electrosynthesis. These applications rely on the capability of these microorgani...

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Autores principales: Antunes, Jorge M. A., Silva, Marta A., Salgueiro, Carlos A., Morgado, Leonor
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9129911/
https://www.ncbi.nlm.nih.gov/pubmed/35620088
http://dx.doi.org/10.3389/fmicb.2022.898015
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author Antunes, Jorge M. A.
Silva, Marta A.
Salgueiro, Carlos A.
Morgado, Leonor
author_facet Antunes, Jorge M. A.
Silva, Marta A.
Salgueiro, Carlos A.
Morgado, Leonor
author_sort Antunes, Jorge M. A.
collection PubMed
description Exoelectrogenic microorganisms are in the spotlight due to their unique respiratory mechanisms and potential applications in distinct biotechnological fields, including bioremediation, bioenergy production and microbial electrosynthesis. These applications rely on the capability of these microorganisms to perform extracellular electron transfer, a mechanism that allows the bacteria to transfer electrons to the cell’s exterior by establishing functional interfaces between different multiheme cytochromes at the inner membrane, periplasmic space, and outer membrane. The multiheme cytochrome CbcL from Geobacter sulfurreducens is associated to the inner membrane and plays an essential role in the transfer of electrons to final electron acceptors with a low redox potential, as Fe(III) oxides and electrodes poised at −100 mV. CbcL has a transmembranar di-heme b-type cytochrome domain with six helices, linked to a periplasmic cytochrome domain with nine c-type heme groups. The complementary usage of ultraviolet-visible, circular dichroism and nuclear magnetic resonance permitted the structural and functional characterization of CbcL’s periplasmic domain. The protein was found to have a high percentage of disordered regions and its nine hemes are low-spin and all coordinated by two histidine residues. The apparent midpoint reduction potential of the CbcL periplasmic domain was determined, suggesting a thermodynamically favorable transfer of electrons to the putative redox partner in the periplasm − the triheme cytochrome PpcA. The establishment of a redox complex between the two proteins was confirmed by probing the electron transfer reaction and the molecular interactions between CbcL and PpcA. The results obtained show for the first time how electrons are injected into the periplasm of Geobacter sulfurreducens for subsequent transfer to the cell’s exterior.
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spelling pubmed-91299112022-05-25 Electron Flow From the Inner Membrane Towards the Cell Exterior in Geobacter sulfurreducens: Biochemical Characterization of Cytochrome CbcL Antunes, Jorge M. A. Silva, Marta A. Salgueiro, Carlos A. Morgado, Leonor Front Microbiol Microbiology Exoelectrogenic microorganisms are in the spotlight due to their unique respiratory mechanisms and potential applications in distinct biotechnological fields, including bioremediation, bioenergy production and microbial electrosynthesis. These applications rely on the capability of these microorganisms to perform extracellular electron transfer, a mechanism that allows the bacteria to transfer electrons to the cell’s exterior by establishing functional interfaces between different multiheme cytochromes at the inner membrane, periplasmic space, and outer membrane. The multiheme cytochrome CbcL from Geobacter sulfurreducens is associated to the inner membrane and plays an essential role in the transfer of electrons to final electron acceptors with a low redox potential, as Fe(III) oxides and electrodes poised at −100 mV. CbcL has a transmembranar di-heme b-type cytochrome domain with six helices, linked to a periplasmic cytochrome domain with nine c-type heme groups. The complementary usage of ultraviolet-visible, circular dichroism and nuclear magnetic resonance permitted the structural and functional characterization of CbcL’s periplasmic domain. The protein was found to have a high percentage of disordered regions and its nine hemes are low-spin and all coordinated by two histidine residues. The apparent midpoint reduction potential of the CbcL periplasmic domain was determined, suggesting a thermodynamically favorable transfer of electrons to the putative redox partner in the periplasm − the triheme cytochrome PpcA. The establishment of a redox complex between the two proteins was confirmed by probing the electron transfer reaction and the molecular interactions between CbcL and PpcA. The results obtained show for the first time how electrons are injected into the periplasm of Geobacter sulfurreducens for subsequent transfer to the cell’s exterior. Frontiers Media S.A. 2022-05-10 /pmc/articles/PMC9129911/ /pubmed/35620088 http://dx.doi.org/10.3389/fmicb.2022.898015 Text en Copyright © 2022 Antunes, Silva, Salgueiro and Morgado. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Antunes, Jorge M. A.
Silva, Marta A.
Salgueiro, Carlos A.
Morgado, Leonor
Electron Flow From the Inner Membrane Towards the Cell Exterior in Geobacter sulfurreducens: Biochemical Characterization of Cytochrome CbcL
title Electron Flow From the Inner Membrane Towards the Cell Exterior in Geobacter sulfurreducens: Biochemical Characterization of Cytochrome CbcL
title_full Electron Flow From the Inner Membrane Towards the Cell Exterior in Geobacter sulfurreducens: Biochemical Characterization of Cytochrome CbcL
title_fullStr Electron Flow From the Inner Membrane Towards the Cell Exterior in Geobacter sulfurreducens: Biochemical Characterization of Cytochrome CbcL
title_full_unstemmed Electron Flow From the Inner Membrane Towards the Cell Exterior in Geobacter sulfurreducens: Biochemical Characterization of Cytochrome CbcL
title_short Electron Flow From the Inner Membrane Towards the Cell Exterior in Geobacter sulfurreducens: Biochemical Characterization of Cytochrome CbcL
title_sort electron flow from the inner membrane towards the cell exterior in geobacter sulfurreducens: biochemical characterization of cytochrome cbcl
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9129911/
https://www.ncbi.nlm.nih.gov/pubmed/35620088
http://dx.doi.org/10.3389/fmicb.2022.898015
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