Metatranscriptomics Supports the Mechanism for Biocathode Electroautotrophy by “<italic toggle="yes">Candidatus</italic> Tenderia electrophaga”

ABSTRACT Biocathodes provide a stable electron source to drive reduction reactions in electrotrophic microbial electrochemical systems. Electroautotrophic biocathode communities may be more robust than monocultures in environmentally relevant settings, but some members are not easily cultivated outs...

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Autores principales:	Brian J. Eddie, Zheng Wang, W. Judson Hervey, Dagmar H. Leary, Anthony P. Malanoski, Leonard M. Tender, Baochuan Lin, Sarah M. Strycharz-Glaven
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	biocathode electroautotroph metatranscriptomics microbial electrochemical system Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/1c3cce73cc7f45658cad2834a8e2de5f
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spelling	oai:doaj.org-article:1c3cce73cc7f45658cad2834a8e2de5f2021-12-02T18:39:34ZMetatranscriptomics Supports the Mechanism for Biocathode Electroautotrophy by “<italic toggle="yes">Candidatus</italic> Tenderia electrophaga”10.1128/mSystems.00002-172379-5077https://doaj.org/article/1c3cce73cc7f45658cad2834a8e2de5f2017-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00002-17https://doaj.org/toc/2379-5077ABSTRACT Biocathodes provide a stable electron source to drive reduction reactions in electrotrophic microbial electrochemical systems. Electroautotrophic biocathode communities may be more robust than monocultures in environmentally relevant settings, but some members are not easily cultivated outside the electrode environment. We previously used metagenomics and metaproteomics to propose a pathway for coupling extracellular electron transfer (EET) to carbon fixation in “Candidatus Tenderia electrophaga,” an uncultivated but dominant member of an electroautotrophic biocathode community. Here we validate and refine this proposed pathway using metatranscriptomics of replicate aerobic biocathodes poised at the growth potential level of 310 mV and the suboptimal 470 mV (versus the standard hydrogen electrode). At both potentials, transcripts were more abundant from “Ca. Tenderia electrophaga” than from any other constituent, and its relative activity was positively correlated with current. Several genes encoding key components of the proposed “Ca. Tenderia electrophaga” EET pathway were more highly expressed at 470 mV, consistent with a need for cells to acquire more electrons to obtain the same amount of energy as at 310 mV. These included cyc2, encoding a homolog of a protein known to be involved in iron oxidation. Mean expression of all CO2 fixation-related genes is 0.27 log2-fold higher at 310 mV, indicating that reduced energy availability at 470 mV decreased CO2 fixation. Our results substantiate the claim that “Ca. Tenderia electrophaga” is the key electroautotroph, which will help guide further development of this community for microbial electrosynthesis. IMPORTANCE Bacteria that directly use electrodes as metabolic electron donors (biocathodes) have been proposed for applications ranging from microbial electrosynthesis to advanced bioelectronics for cellular communication with machines. However, just as we understand very little about oxidation of analogous natural insoluble electron donors, such as iron oxide, the organisms and extracellular electron transfer (EET) pathways underlying the electrode-cell direct electron transfer processes are almost completely unknown. Biocathodes are a stable biofilm cultivation platform to interrogate both the rate and mechanism of EET using electrochemistry and to study the electroautotrophic organisms that catalyze these reactions. Here we provide new evidence supporting the hypothesis that the uncultured bacterium “Candidatus Tenderia electrophaga” directly couples extracellular electron transfer to CO2 fixation. Our results provide insight into developing biocathode technology, such as microbial electrosynthesis, as well as advancing our understanding of chemolithoautotrophy.Brian J. EddieZheng WangW. Judson HerveyDagmar H. LearyAnthony P. MalanoskiLeonard M. TenderBaochuan LinSarah M. Strycharz-GlavenAmerican Society for Microbiologyarticlebiocathodeelectroautotrophmetatranscriptomicsmicrobial electrochemical systemMicrobiologyQR1-502ENmSystems, Vol 2, Iss 2 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	biocathode electroautotroph metatranscriptomics microbial electrochemical system Microbiology QR1-502
spellingShingle	biocathode electroautotroph metatranscriptomics microbial electrochemical system Microbiology QR1-502 Brian J. Eddie Zheng Wang W. Judson Hervey Dagmar H. Leary Anthony P. Malanoski Leonard M. Tender Baochuan Lin Sarah M. Strycharz-Glaven Metatranscriptomics Supports the Mechanism for Biocathode Electroautotrophy by “<italic toggle="yes">Candidatus</italic> Tenderia electrophaga”
description	ABSTRACT Biocathodes provide a stable electron source to drive reduction reactions in electrotrophic microbial electrochemical systems. Electroautotrophic biocathode communities may be more robust than monocultures in environmentally relevant settings, but some members are not easily cultivated outside the electrode environment. We previously used metagenomics and metaproteomics to propose a pathway for coupling extracellular electron transfer (EET) to carbon fixation in “Candidatus Tenderia electrophaga,” an uncultivated but dominant member of an electroautotrophic biocathode community. Here we validate and refine this proposed pathway using metatranscriptomics of replicate aerobic biocathodes poised at the growth potential level of 310 mV and the suboptimal 470 mV (versus the standard hydrogen electrode). At both potentials, transcripts were more abundant from “Ca. Tenderia electrophaga” than from any other constituent, and its relative activity was positively correlated with current. Several genes encoding key components of the proposed “Ca. Tenderia electrophaga” EET pathway were more highly expressed at 470 mV, consistent with a need for cells to acquire more electrons to obtain the same amount of energy as at 310 mV. These included cyc2, encoding a homolog of a protein known to be involved in iron oxidation. Mean expression of all CO2 fixation-related genes is 0.27 log2-fold higher at 310 mV, indicating that reduced energy availability at 470 mV decreased CO2 fixation. Our results substantiate the claim that “Ca. Tenderia electrophaga” is the key electroautotroph, which will help guide further development of this community for microbial electrosynthesis. IMPORTANCE Bacteria that directly use electrodes as metabolic electron donors (biocathodes) have been proposed for applications ranging from microbial electrosynthesis to advanced bioelectronics for cellular communication with machines. However, just as we understand very little about oxidation of analogous natural insoluble electron donors, such as iron oxide, the organisms and extracellular electron transfer (EET) pathways underlying the electrode-cell direct electron transfer processes are almost completely unknown. Biocathodes are a stable biofilm cultivation platform to interrogate both the rate and mechanism of EET using electrochemistry and to study the electroautotrophic organisms that catalyze these reactions. Here we provide new evidence supporting the hypothesis that the uncultured bacterium “Candidatus Tenderia electrophaga” directly couples extracellular electron transfer to CO2 fixation. Our results provide insight into developing biocathode technology, such as microbial electrosynthesis, as well as advancing our understanding of chemolithoautotrophy.
format	article
author	Brian J. Eddie Zheng Wang W. Judson Hervey Dagmar H. Leary Anthony P. Malanoski Leonard M. Tender Baochuan Lin Sarah M. Strycharz-Glaven
author_facet	Brian J. Eddie Zheng Wang W. Judson Hervey Dagmar H. Leary Anthony P. Malanoski Leonard M. Tender Baochuan Lin Sarah M. Strycharz-Glaven
author_sort	Brian J. Eddie
title	Metatranscriptomics Supports the Mechanism for Biocathode Electroautotrophy by “<italic toggle="yes">Candidatus</italic> Tenderia electrophaga”
title_short	Metatranscriptomics Supports the Mechanism for Biocathode Electroautotrophy by “<italic toggle="yes">Candidatus</italic> Tenderia electrophaga”
title_full	Metatranscriptomics Supports the Mechanism for Biocathode Electroautotrophy by “<italic toggle="yes">Candidatus</italic> Tenderia electrophaga”
title_fullStr	Metatranscriptomics Supports the Mechanism for Biocathode Electroautotrophy by “<italic toggle="yes">Candidatus</italic> Tenderia electrophaga”
title_full_unstemmed	Metatranscriptomics Supports the Mechanism for Biocathode Electroautotrophy by “<italic toggle="yes">Candidatus</italic> Tenderia electrophaga”
title_sort	metatranscriptomics supports the mechanism for biocathode electroautotrophy by “<italic toggle="yes">candidatus</italic> tenderia electrophaga”
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/1c3cce73cc7f45658cad2834a8e2de5f
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Metatranscriptomics Supports the Mechanism for Biocathode Electroautotrophy by “<italic toggle="yes">Candidatus</italic> Tenderia electrophaga”

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