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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Main Authors:	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.
Format:	Article
Language:	English English
Published:	American Society for Biochemistry and Molecular Biology 2018
Online Access:	http://eprints.nottingham.ac.uk/51122/ http://eprints.nottingham.ac.uk/51122/ http://eprints.nottingham.ac.uk/51122/ http://eprints.nottingham.ac.uk/51122/1/J.%20Biol.%20Chem.-2018-Edwards-jbc.RA118.001850.pdf http://eprints.nottingham.ac.uk/51122/8/J.%20Biol.%20Chem.-2018-Edwards-8103-12.pdf

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recordtype	eprints
spelling	nottingham-511222018-06-14T16:31:07Z http://eprints.nottingham.ac.uk/51122/ 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. 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 transfers 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 ~105×60×35ÅforMtrABand~170×60×45Å 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 Article PeerReviewed application/pdf en http://eprints.nottingham.ac.uk/51122/1/J.%20Biol.%20Chem.-2018-Edwards-jbc.RA118.001850.pdf application/pdf en cc_by http://eprints.nottingham.ac.uk/51122/8/J.%20Biol.%20Chem.-2018-Edwards-8103-12.pdf Edwards, Marcus J. and White, Gaye F. and Lockwood, Colin W. and Lawes, Matthew C. and Martel, Anne and Harris, Gemma and Scott, David J. and Richardson, David J. and Butt, Julea N. and Clarke, Thomas A. (2018) Structural modeling of an outer membrane electron conduit from a metal-reducing bacterium suggests electron transfer via periplasmic redox partners. Journal of Biological Chemistry, 293 (21). pp. 8103-8112. ISSN 1083-351X http://www.jbc.org/content/early/2018/04/10/jbc.RA118.001850 doi:10.1074/jbc.RA118.001850 doi:10.1074/jbc.RA118.001850
repository_type	Digital Repository
institution_category	Local University
institution	University of Nottingham Malaysia Campus
building	Nottingham Research Data Repository
collection	Online Access
language	English English
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 transfers 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 ~105×60×35ÅforMtrABand~170×60×45Å 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.
format	Article
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.
spellingShingle	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
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.
title	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_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_sort	structural modeling of an outer membrane electron conduit from a metal-reducing bacterium suggests electron transfer via periplasmic redox partners
publisher	American Society for Biochemistry and Molecular Biology
publishDate	2018
url	http://eprints.nottingham.ac.uk/51122/ http://eprints.nottingham.ac.uk/51122/ http://eprints.nottingham.ac.uk/51122/ http://eprints.nottingham.ac.uk/51122/1/J.%20Biol.%20Chem.-2018-Edwards-jbc.RA118.001850.pdf http://eprints.nottingham.ac.uk/51122/8/J.%20Biol.%20Chem.-2018-Edwards-8103-12.pdf
first_indexed	2018-09-06T14:18:33Z
last_indexed	2018-09-06T14:18:33Z
_version_	1610868078586888192

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

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