An Inner Membrane Cytochrome Required Only for Reduction of High Redox Potential Extracellular Electron Acceptors

ABSTRACT Dissimilatory metal-reducing bacteria, such as Geobacter sulfurreducens, transfer electrons beyond their outer membranes to Fe(III) and Mn(IV) oxides, heavy metals, and electrodes in electrochemical devices. In the environment, metal acceptors exist in multiple chelated and insoluble forms...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Caleb E. Levar, Chi Ho Chan, Misha G. Mehta-Kolte, Daniel R. Bond
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2014
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/2c24456f2c46460db4648dfacf3c164a
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:2c24456f2c46460db4648dfacf3c164a
record_format	dspace
spelling	oai:doaj.org-article:2c24456f2c46460db4648dfacf3c164a2021-11-15T15:47:03ZAn Inner Membrane Cytochrome Required Only for Reduction of High Redox Potential Extracellular Electron Acceptors10.1128/mBio.02034-142150-7511https://doaj.org/article/2c24456f2c46460db4648dfacf3c164a2014-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02034-14https://doaj.org/toc/2150-7511ABSTRACT Dissimilatory metal-reducing bacteria, such as Geobacter sulfurreducens, transfer electrons beyond their outer membranes to Fe(III) and Mn(IV) oxides, heavy metals, and electrodes in electrochemical devices. In the environment, metal acceptors exist in multiple chelated and insoluble forms that span a range of redox potentials and offer different amounts of available energy. Despite this, metal-reducing bacteria have not been shown to alter their electron transfer strategies to take advantage of these energy differences. Disruption of imcH, encoding an inner membrane c-type cytochrome, eliminated the ability of G. sulfurreducens to reduce Fe(III) citrate, Fe(III)-EDTA, and insoluble Mn(IV) oxides, electron acceptors with potentials greater than 0.1 V versus the standard hydrogen electrode (SHE), but the imcH mutant retained the ability to reduce Fe(III) oxides with potentials of ≤−0.1 V versus SHE. The imcH mutant failed to grow on electrodes poised at +0.24 V versus SHE, but switching electrodes to −0.1 V versus SHE triggered exponential growth. At potentials of ≤−0.1 V versus SHE, both the wild type and the imcH mutant doubled 60% slower than at higher potentials. Electrodes poised even 100 mV higher (0.0 V versus SHE) could not trigger imcH mutant growth. These results demonstrate that G. sulfurreducens possesses multiple respiratory pathways, that some of these pathways are in operation only after exposure to low redox potentials, and that electron flow can be coupled to generation of different amounts of energy for growth. The redox potentials that trigger these behaviors mirror those of metal acceptors common in subsurface environments where Geobacter is found. IMPORTANCE Insoluble metal oxides in the environment represent a common and vast reservoir of energy for respiratory microbes capable of transferring electrons across their insulating membranes to external acceptors, a process termed extracellular electron transfer. Despite the global biogeochemical importance of metal cycling and the ability of such organisms to produce electricity at electrodes, fundamental gaps in the understanding of extracellular electron transfer biochemistry exist. Here, we describe a conserved inner membrane redox protein in Geobacter sulfurreducens which is required only for electron transfer to high-potential compounds, and we show that G. sulfurreducens has the ability to utilize different electron transfer pathways in response to the amount of energy available in a metal or electrode distant from the cell.Caleb E. LevarChi Ho ChanMisha G. Mehta-KolteDaniel R. BondAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 6 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Caleb E. Levar Chi Ho Chan Misha G. Mehta-Kolte Daniel R. Bond An Inner Membrane Cytochrome Required Only for Reduction of High Redox Potential Extracellular Electron Acceptors
description	ABSTRACT Dissimilatory metal-reducing bacteria, such as Geobacter sulfurreducens, transfer electrons beyond their outer membranes to Fe(III) and Mn(IV) oxides, heavy metals, and electrodes in electrochemical devices. In the environment, metal acceptors exist in multiple chelated and insoluble forms that span a range of redox potentials and offer different amounts of available energy. Despite this, metal-reducing bacteria have not been shown to alter their electron transfer strategies to take advantage of these energy differences. Disruption of imcH, encoding an inner membrane c-type cytochrome, eliminated the ability of G. sulfurreducens to reduce Fe(III) citrate, Fe(III)-EDTA, and insoluble Mn(IV) oxides, electron acceptors with potentials greater than 0.1 V versus the standard hydrogen electrode (SHE), but the imcH mutant retained the ability to reduce Fe(III) oxides with potentials of ≤−0.1 V versus SHE. The imcH mutant failed to grow on electrodes poised at +0.24 V versus SHE, but switching electrodes to −0.1 V versus SHE triggered exponential growth. At potentials of ≤−0.1 V versus SHE, both the wild type and the imcH mutant doubled 60% slower than at higher potentials. Electrodes poised even 100 mV higher (0.0 V versus SHE) could not trigger imcH mutant growth. These results demonstrate that G. sulfurreducens possesses multiple respiratory pathways, that some of these pathways are in operation only after exposure to low redox potentials, and that electron flow can be coupled to generation of different amounts of energy for growth. The redox potentials that trigger these behaviors mirror those of metal acceptors common in subsurface environments where Geobacter is found. IMPORTANCE Insoluble metal oxides in the environment represent a common and vast reservoir of energy for respiratory microbes capable of transferring electrons across their insulating membranes to external acceptors, a process termed extracellular electron transfer. Despite the global biogeochemical importance of metal cycling and the ability of such organisms to produce electricity at electrodes, fundamental gaps in the understanding of extracellular electron transfer biochemistry exist. Here, we describe a conserved inner membrane redox protein in Geobacter sulfurreducens which is required only for electron transfer to high-potential compounds, and we show that G. sulfurreducens has the ability to utilize different electron transfer pathways in response to the amount of energy available in a metal or electrode distant from the cell.
format	article
author	Caleb E. Levar Chi Ho Chan Misha G. Mehta-Kolte Daniel R. Bond
author_facet	Caleb E. Levar Chi Ho Chan Misha G. Mehta-Kolte Daniel R. Bond
author_sort	Caleb E. Levar
title	An Inner Membrane Cytochrome Required Only for Reduction of High Redox Potential Extracellular Electron Acceptors
title_short	An Inner Membrane Cytochrome Required Only for Reduction of High Redox Potential Extracellular Electron Acceptors
title_full	An Inner Membrane Cytochrome Required Only for Reduction of High Redox Potential Extracellular Electron Acceptors
title_fullStr	An Inner Membrane Cytochrome Required Only for Reduction of High Redox Potential Extracellular Electron Acceptors
title_full_unstemmed	An Inner Membrane Cytochrome Required Only for Reduction of High Redox Potential Extracellular Electron Acceptors
title_sort	inner membrane cytochrome required only for reduction of high redox potential extracellular electron acceptors
publisher	American Society for Microbiology
publishDate	2014
url	https://doaj.org/article/2c24456f2c46460db4648dfacf3c164a
work_keys_str_mv	AT calebelevar aninnermembranecytochromerequiredonlyforreductionofhighredoxpotentialextracellularelectronacceptors AT chihochan aninnermembranecytochromerequiredonlyforreductionofhighredoxpotentialextracellularelectronacceptors AT mishagmehtakolte aninnermembranecytochromerequiredonlyforreductionofhighredoxpotentialextracellularelectronacceptors AT danielrbond aninnermembranecytochromerequiredonlyforreductionofhighredoxpotentialextracellularelectronacceptors AT calebelevar innermembranecytochromerequiredonlyforreductionofhighredoxpotentialextracellularelectronacceptors AT chihochan innermembranecytochromerequiredonlyforreductionofhighredoxpotentialextracellularelectronacceptors AT mishagmehtakolte innermembranecytochromerequiredonlyforreductionofhighredoxpotentialextracellularelectronacceptors AT danielrbond innermembranecytochromerequiredonlyforreductionofhighredoxpotentialextracellularelectronacceptors
_version_	1718427506640420864

An Inner Membrane Cytochrome Required Only for Reduction of High Redox Potential Extracellular Electron Acceptors

Ejemplares similares