Tactic Response of <named-content content-type="genus-species">Shewanella oneidensis</named-content> MR-1 toward Insoluble Electron Acceptors

ABSTRACT Exoelectrogenic bacteria are defined by their ability to respire on extracellular and insoluble electron acceptors and have applications in bioremediation and microbial electrochemical systems (MESs), while playing important roles in biogeochemical cycling. Shewanella oneidensis MR-1, which...

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Autores principales:	Joseph Oram, Lars J. C. Jeuken
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Shewanella oneidensis extracellular electron transfer flavin insoluble electron acceptors microbe-mineral interactions motility Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/1d0fe56ed19f44b082cc34f9a84bdc1a
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spelling	oai:doaj.org-article:1d0fe56ed19f44b082cc34f9a84bdc1a2021-11-15T15:55:14ZTactic Response of <named-content content-type="genus-species">Shewanella oneidensis</named-content> MR-1 toward Insoluble Electron Acceptors10.1128/mBio.02490-182150-7511https://doaj.org/article/1d0fe56ed19f44b082cc34f9a84bdc1a2019-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02490-18https://doaj.org/toc/2150-7511ABSTRACT Exoelectrogenic bacteria are defined by their ability to respire on extracellular and insoluble electron acceptors and have applications in bioremediation and microbial electrochemical systems (MESs), while playing important roles in biogeochemical cycling. Shewanella oneidensis MR-1, which has become a model organism for the study of extracellular respiration, is known to display taxis toward insoluble electron acceptors, including electrodes. Multiple mechanisms have been proposed for MR-1’s tactic behavior, and, here, we report on the role of electrochemical potential by video microscopy cell tracking experiments in three-electrode electrochemical cells. MR-1 trajectories were determined using a particle tracking algorithm and validated with Shannon’s entropy method. Tactic response by MR-1 in the electrochemical cell was observed to depend on the applied potential, as indicated by the average velocity and density of motile (>4 µm/s) MR-1 close to the electrode (<50 µm). Tactic behavior was observed at oxidative potentials, with a strong switch between the potentials −0.15 to −0.25 V versus the standard hydrogen electrode (SHE), which coincides with the reduction potential of flavins. The average velocity and density of motile MR-1 close to the electrode increased when riboflavin was added (2 µM), but were completely absent in a ΔmtrC/ΔomcA mutant of MR-1. Besides flavin’s function as an electron mediator to support anaerobic respiration on insoluble electron acceptors, we propose that riboflavin is excreted by MR-1 to sense redox gradients in its environment, aiding taxis toward insoluble electron acceptors, including electrodes in MESs. IMPORTANCE Previous hypotheses of tactic behavior of exoelectrogenic bacteria are based on techniques that do not accurately control the electrochemical potential, such as chemical-in-plug assays or microscopy tracking experiments in two-electrode cells. Here, we have revisited previous experiments and, for the first time, performed microscopy cell-tracking experiments in three-electrode electrochemical cells, with defined electrode potentials. Based on these experiments, taxis toward electrodes is observed to switch at about −0.2 V versus standard hydrogen electrode (SHE), coinciding with the reduction potential of flavins.Joseph OramLars J. C. JeukenAmerican Society for MicrobiologyarticleShewanella oneidensisextracellular electron transferflavininsoluble electron acceptorsmicrobe-mineral interactionsmotilityMicrobiologyQR1-502ENmBio, Vol 10, Iss 1 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Shewanella oneidensis extracellular electron transfer flavin insoluble electron acceptors microbe-mineral interactions motility Microbiology QR1-502
spellingShingle	Shewanella oneidensis extracellular electron transfer flavin insoluble electron acceptors microbe-mineral interactions motility Microbiology QR1-502 Joseph Oram Lars J. C. Jeuken Tactic Response of <named-content content-type="genus-species">Shewanella oneidensis</named-content> MR-1 toward Insoluble Electron Acceptors
description	ABSTRACT Exoelectrogenic bacteria are defined by their ability to respire on extracellular and insoluble electron acceptors and have applications in bioremediation and microbial electrochemical systems (MESs), while playing important roles in biogeochemical cycling. Shewanella oneidensis MR-1, which has become a model organism for the study of extracellular respiration, is known to display taxis toward insoluble electron acceptors, including electrodes. Multiple mechanisms have been proposed for MR-1’s tactic behavior, and, here, we report on the role of electrochemical potential by video microscopy cell tracking experiments in three-electrode electrochemical cells. MR-1 trajectories were determined using a particle tracking algorithm and validated with Shannon’s entropy method. Tactic response by MR-1 in the electrochemical cell was observed to depend on the applied potential, as indicated by the average velocity and density of motile (>4 µm/s) MR-1 close to the electrode (<50 µm). Tactic behavior was observed at oxidative potentials, with a strong switch between the potentials −0.15 to −0.25 V versus the standard hydrogen electrode (SHE), which coincides with the reduction potential of flavins. The average velocity and density of motile MR-1 close to the electrode increased when riboflavin was added (2 µM), but were completely absent in a ΔmtrC/ΔomcA mutant of MR-1. Besides flavin’s function as an electron mediator to support anaerobic respiration on insoluble electron acceptors, we propose that riboflavin is excreted by MR-1 to sense redox gradients in its environment, aiding taxis toward insoluble electron acceptors, including electrodes in MESs. IMPORTANCE Previous hypotheses of tactic behavior of exoelectrogenic bacteria are based on techniques that do not accurately control the electrochemical potential, such as chemical-in-plug assays or microscopy tracking experiments in two-electrode cells. Here, we have revisited previous experiments and, for the first time, performed microscopy cell-tracking experiments in three-electrode electrochemical cells, with defined electrode potentials. Based on these experiments, taxis toward electrodes is observed to switch at about −0.2 V versus standard hydrogen electrode (SHE), coinciding with the reduction potential of flavins.
format	article
author	Joseph Oram Lars J. C. Jeuken
author_facet	Joseph Oram Lars J. C. Jeuken
author_sort	Joseph Oram
title	Tactic Response of <named-content content-type="genus-species">Shewanella oneidensis</named-content> MR-1 toward Insoluble Electron Acceptors
title_short	Tactic Response of <named-content content-type="genus-species">Shewanella oneidensis</named-content> MR-1 toward Insoluble Electron Acceptors
title_full	Tactic Response of <named-content content-type="genus-species">Shewanella oneidensis</named-content> MR-1 toward Insoluble Electron Acceptors
title_fullStr	Tactic Response of <named-content content-type="genus-species">Shewanella oneidensis</named-content> MR-1 toward Insoluble Electron Acceptors
title_full_unstemmed	Tactic Response of <named-content content-type="genus-species">Shewanella oneidensis</named-content> MR-1 toward Insoluble Electron Acceptors
title_sort	tactic response of <named-content content-type="genus-species">shewanella oneidensis</named-content> mr-1 toward insoluble electron acceptors
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/1d0fe56ed19f44b082cc34f9a84bdc1a
work_keys_str_mv	AT josephoram tacticresponseofnamedcontentcontenttypegenusspeciesshewanellaoneidensisnamedcontentmr1towardinsolubleelectronacceptors AT larsjcjeuken tacticresponseofnamedcontentcontenttypegenusspeciesshewanellaoneidensisnamedcontentmr1towardinsolubleelectronacceptors
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Tactic Response of <named-content content-type="genus-species">Shewanella oneidensis</named-content> MR-1 toward Insoluble Electron Acceptors

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