Towards electrosynthesis in shewanella: energetics of reversing the mtr pathway for reductive metabolism.

Bioelectrochemical systems rely on microorganisms to link complex oxidation/reduction reactions to electrodes. For example, in Shewanella oneidensis strain MR-1, an electron transfer conduit consisting of cytochromes and structural proteins, known as the Mtr respiratory pathway, catalyzes electron f...

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Autores principales:	Daniel E Ross, Jeffrey M Flynn, Daniel B Baron, Jeffrey A Gralnick, Daniel R Bond
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2011
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/56a2dccfba75418c85dafeac61d9080e
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spelling	oai:doaj.org-article:56a2dccfba75418c85dafeac61d9080e2021-11-18T06:59:19ZTowards electrosynthesis in shewanella: energetics of reversing the mtr pathway for reductive metabolism.1932-620310.1371/journal.pone.0016649https://doaj.org/article/56a2dccfba75418c85dafeac61d9080e2011-02-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/21311751/pdf/?tool=EBIhttps://doaj.org/toc/1932-6203Bioelectrochemical systems rely on microorganisms to link complex oxidation/reduction reactions to electrodes. For example, in Shewanella oneidensis strain MR-1, an electron transfer conduit consisting of cytochromes and structural proteins, known as the Mtr respiratory pathway, catalyzes electron flow from cytoplasmic oxidative reactions to electrodes. Reversing this electron flow to drive microbial reductive metabolism offers a possible route for electrosynthesis of high value fuels and chemicals. We examined electron flow from electrodes into Shewanella to determine the feasibility of this process, the molecular components of reductive electron flow, and what driving forces were required. Addition of fumarate to a film of S. oneidensis adhering to a graphite electrode poised at -0.36 V versus standard hydrogen electrode (SHE) immediately led to electron uptake, while a mutant lacking the periplasmic fumarate reductase FccA was unable to utilize electrodes for fumarate reduction. Deletion of the gene encoding the outer membrane cytochrome-anchoring protein MtrB eliminated 88% of fumarate reduction. A mutant lacking the periplasmic cytochrome MtrA demonstrated more severe defects. Surprisingly, disruption of menC, which prevents menaquinone biosynthesis, eliminated 85% of electron flux. Deletion of the gene encoding the quinone-linked cytochrome CymA had a similar negative effect, which showed that electrons primarily flowed from outer membrane cytochromes into the quinone pool, and back to periplasmic FccA. Soluble redox mediators only partially restored electron transfer in mutants, suggesting that soluble shuttles could not replace periplasmic protein-protein interactions. This work demonstrates that the Mtr pathway can power reductive reactions, shows this conduit is functionally reversible, and provides new evidence for distinct CymA:MtrA and CymA:FccA respiratory units.Daniel E RossJeffrey M FlynnDaniel B BaronJeffrey A GralnickDaniel R BondPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 6, Iss 2, p e16649 (2011)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Daniel E Ross Jeffrey M Flynn Daniel B Baron Jeffrey A Gralnick Daniel R Bond Towards electrosynthesis in shewanella: energetics of reversing the mtr pathway for reductive metabolism.
description	Bioelectrochemical systems rely on microorganisms to link complex oxidation/reduction reactions to electrodes. For example, in Shewanella oneidensis strain MR-1, an electron transfer conduit consisting of cytochromes and structural proteins, known as the Mtr respiratory pathway, catalyzes electron flow from cytoplasmic oxidative reactions to electrodes. Reversing this electron flow to drive microbial reductive metabolism offers a possible route for electrosynthesis of high value fuels and chemicals. We examined electron flow from electrodes into Shewanella to determine the feasibility of this process, the molecular components of reductive electron flow, and what driving forces were required. Addition of fumarate to a film of S. oneidensis adhering to a graphite electrode poised at -0.36 V versus standard hydrogen electrode (SHE) immediately led to electron uptake, while a mutant lacking the periplasmic fumarate reductase FccA was unable to utilize electrodes for fumarate reduction. Deletion of the gene encoding the outer membrane cytochrome-anchoring protein MtrB eliminated 88% of fumarate reduction. A mutant lacking the periplasmic cytochrome MtrA demonstrated more severe defects. Surprisingly, disruption of menC, which prevents menaquinone biosynthesis, eliminated 85% of electron flux. Deletion of the gene encoding the quinone-linked cytochrome CymA had a similar negative effect, which showed that electrons primarily flowed from outer membrane cytochromes into the quinone pool, and back to periplasmic FccA. Soluble redox mediators only partially restored electron transfer in mutants, suggesting that soluble shuttles could not replace periplasmic protein-protein interactions. This work demonstrates that the Mtr pathway can power reductive reactions, shows this conduit is functionally reversible, and provides new evidence for distinct CymA:MtrA and CymA:FccA respiratory units.
format	article
author	Daniel E Ross Jeffrey M Flynn Daniel B Baron Jeffrey A Gralnick Daniel R Bond
author_facet	Daniel E Ross Jeffrey M Flynn Daniel B Baron Jeffrey A Gralnick Daniel R Bond
author_sort	Daniel E Ross
title	Towards electrosynthesis in shewanella: energetics of reversing the mtr pathway for reductive metabolism.
title_short	Towards electrosynthesis in shewanella: energetics of reversing the mtr pathway for reductive metabolism.
title_full	Towards electrosynthesis in shewanella: energetics of reversing the mtr pathway for reductive metabolism.
title_fullStr	Towards electrosynthesis in shewanella: energetics of reversing the mtr pathway for reductive metabolism.
title_full_unstemmed	Towards electrosynthesis in shewanella: energetics of reversing the mtr pathway for reductive metabolism.
title_sort	towards electrosynthesis in shewanella: energetics of reversing the mtr pathway for reductive metabolism.
publisher	Public Library of Science (PLoS)
publishDate	2011
url	https://doaj.org/article/56a2dccfba75418c85dafeac61d9080e
work_keys_str_mv	AT danieleross towardselectrosynthesisinshewanellaenergeticsofreversingthemtrpathwayforreductivemetabolism AT jeffreymflynn towardselectrosynthesisinshewanellaenergeticsofreversingthemtrpathwayforreductivemetabolism AT danielbbaron towardselectrosynthesisinshewanellaenergeticsofreversingthemtrpathwayforreductivemetabolism AT jeffreyagralnick towardselectrosynthesisinshewanellaenergeticsofreversingthemtrpathwayforreductivemetabolism AT danielrbond towardselectrosynthesisinshewanellaenergeticsofreversingthemtrpathwayforreductivemetabolism
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Towards electrosynthesis in shewanella: energetics of reversing the mtr pathway for reductive metabolism.

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