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Structural modeling of an outer membrane electron conduit from a metal-reducing bacterium suggests electron transfer via periplasmic redox partners

Many subsurface microorganisms couple their metabolism to the reduction or oxidation of extracellular substrates. For example, anaerobic mineral-respiring bacteria can use external metal oxides as terminal electron acceptors during respiration. Porin–cytochrome complexes facilitate the movement of e...

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Autores principales: Edwards, Marcus J., White, Gaye F., Lockwood, Colin W., Lawes, Matthew C., Martel, Anne, Harris, Gemma, Scott, David J., Richardson, David J., Butt, Julea N., Clarke, Thomas A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Biochemistry and Molecular Biology 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5971433/
https://www.ncbi.nlm.nih.gov/pubmed/29636412
http://dx.doi.org/10.1074/jbc.RA118.001850
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author Edwards, Marcus J.
White, Gaye F.
Lockwood, Colin W.
Lawes, Matthew C.
Martel, Anne
Harris, Gemma
Scott, David J.
Richardson, David J.
Butt, Julea N.
Clarke, Thomas A.
author_facet Edwards, Marcus J.
White, Gaye F.
Lockwood, Colin W.
Lawes, Matthew C.
Martel, Anne
Harris, Gemma
Scott, David J.
Richardson, David J.
Butt, Julea N.
Clarke, Thomas A.
author_sort Edwards, Marcus J.
collection PubMed
description Many subsurface microorganisms couple their metabolism to the reduction or oxidation of extracellular substrates. For example, anaerobic mineral-respiring bacteria can use external metal oxides as terminal electron acceptors during respiration. Porin–cytochrome complexes facilitate the movement of electrons generated through intracellular catabolic processes across the bacterial outer membrane to these terminal electron acceptors. In the mineral-reducing model bacterium Shewanella oneidensis MR-1, this complex is composed of two decaheme cytochromes (MtrA and MtrC) and an outer-membrane β-barrel (MtrB). However, the structures and mechanisms by which porin–cytochrome complexes transfer electrons are unknown. Here, we used small-angle neutron scattering (SANS) to study the molecular structure of the transmembrane complexes MtrAB and MtrCAB. Ab initio modeling of the scattering data yielded a molecular envelope with dimensions of ∼105 × 60 × 35 Å for MtrAB and ∼170 × 60 × 45 Å for MtrCAB. The shapes of these molecular envelopes suggested that MtrC interacts with the surface of MtrAB, extending ∼70 Å from the membrane surface and allowing the terminal hemes to interact with both MtrAB and an extracellular acceptor. The data also reveal that MtrA fully extends through the length of MtrB, with ∼30 Å being exposed into the periplasm. Proteoliposome models containing membrane-associated MtrCAB and internalized small tetraheme cytochrome (STC) indicate that MtrCAB could reduce Fe(III) citrate with STC as an electron donor, disclosing a direct interaction between MtrCAB and STC. Taken together, both structural and proteoliposome experiments support porin–cytochrome–mediated electron transfer via periplasmic cytochromes such as STC.
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spelling pubmed-59714332018-05-29 Structural modeling of an outer membrane electron conduit from a metal-reducing bacterium suggests electron transfer via periplasmic redox partners Edwards, Marcus J. White, Gaye F. Lockwood, Colin W. Lawes, Matthew C. Martel, Anne Harris, Gemma Scott, David J. Richardson, David J. Butt, Julea N. Clarke, Thomas A. J Biol Chem Molecular Biophysics Many subsurface microorganisms couple their metabolism to the reduction or oxidation of extracellular substrates. For example, anaerobic mineral-respiring bacteria can use external metal oxides as terminal electron acceptors during respiration. Porin–cytochrome complexes facilitate the movement of electrons generated through intracellular catabolic processes across the bacterial outer membrane to these terminal electron acceptors. In the mineral-reducing model bacterium Shewanella oneidensis MR-1, this complex is composed of two decaheme cytochromes (MtrA and MtrC) and an outer-membrane β-barrel (MtrB). However, the structures and mechanisms by which porin–cytochrome complexes transfer electrons are unknown. Here, we used small-angle neutron scattering (SANS) to study the molecular structure of the transmembrane complexes MtrAB and MtrCAB. Ab initio modeling of the scattering data yielded a molecular envelope with dimensions of ∼105 × 60 × 35 Å for MtrAB and ∼170 × 60 × 45 Å for MtrCAB. The shapes of these molecular envelopes suggested that MtrC interacts with the surface of MtrAB, extending ∼70 Å from the membrane surface and allowing the terminal hemes to interact with both MtrAB and an extracellular acceptor. The data also reveal that MtrA fully extends through the length of MtrB, with ∼30 Å being exposed into the periplasm. Proteoliposome models containing membrane-associated MtrCAB and internalized small tetraheme cytochrome (STC) indicate that MtrCAB could reduce Fe(III) citrate with STC as an electron donor, disclosing a direct interaction between MtrCAB and STC. Taken together, both structural and proteoliposome experiments support porin–cytochrome–mediated electron transfer via periplasmic cytochromes such as STC. American Society for Biochemistry and Molecular Biology 2018-05-25 2018-04-10 /pmc/articles/PMC5971433/ /pubmed/29636412 http://dx.doi.org/10.1074/jbc.RA118.001850 Text en © 2018 Edwards et al. Published under exclusive license by The American Society for Biochemistry and Molecular Biology, Inc. Author's Choice—Final version free via Creative Commons CC-BY license (http://creativecommons.org/licenses/by/4.0) .
spellingShingle Molecular Biophysics
Edwards, Marcus J.
White, Gaye F.
Lockwood, Colin W.
Lawes, Matthew C.
Martel, Anne
Harris, Gemma
Scott, David J.
Richardson, David J.
Butt, Julea N.
Clarke, Thomas A.
Structural modeling of an outer membrane electron conduit from a metal-reducing bacterium suggests electron transfer via periplasmic redox partners
title Structural modeling of an outer membrane electron conduit from a metal-reducing bacterium suggests electron transfer via periplasmic redox partners
title_full Structural modeling of an outer membrane electron conduit from a metal-reducing bacterium suggests electron transfer via periplasmic redox partners
title_fullStr Structural modeling of an outer membrane electron conduit from a metal-reducing bacterium suggests electron transfer via periplasmic redox partners
title_full_unstemmed Structural modeling of an outer membrane electron conduit from a metal-reducing bacterium suggests electron transfer via periplasmic redox partners
title_short Structural modeling of an outer membrane electron conduit from a metal-reducing bacterium suggests electron transfer via periplasmic redox partners
title_sort structural modeling of an outer membrane electron conduit from a metal-reducing bacterium suggests electron transfer via periplasmic redox partners
topic Molecular Biophysics
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5971433/
https://www.ncbi.nlm.nih.gov/pubmed/29636412
http://dx.doi.org/10.1074/jbc.RA118.001850
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