<italic toggle="yes">Geobacter</italic> Strains Expressing Poorly Conductive Pili Reveal Constraints on Direct Interspecies Electron Transfer Mechanisms

ABSTRACT Cytochrome-to-cytochrome electron transfer and electron transfer along conduits of multiple extracellular magnetite grains are often proposed as strategies for direct interspecies electron transfer (DIET) that do not require electrically conductive pili (e-pili). However, physical evidence...

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Autores principales:	Toshiyuki Ueki, Kelly P. Nevin, Amelia-Elena Rotaru, Li-Ying Wang, Joy E. Ward, Trevor L. Woodard, Derek R. Lovley
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	DIET coculture extracellular electron transfer syntrophy Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/dc02b0b3b8a1419e9817f448612d8d16
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spelling	oai:doaj.org-article:dc02b0b3b8a1419e9817f448612d8d162021-11-15T16:00:15Z<italic toggle="yes">Geobacter</italic> Strains Expressing Poorly Conductive Pili Reveal Constraints on Direct Interspecies Electron Transfer Mechanisms10.1128/mBio.01273-182150-7511https://doaj.org/article/dc02b0b3b8a1419e9817f448612d8d162018-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01273-18https://doaj.org/toc/2150-7511ABSTRACT Cytochrome-to-cytochrome electron transfer and electron transfer along conduits of multiple extracellular magnetite grains are often proposed as strategies for direct interspecies electron transfer (DIET) that do not require electrically conductive pili (e-pili). However, physical evidence for these proposed DIET mechanisms has been lacking. To investigate these possibilities further, we constructed Geobacter metallireducens strain Aro-5, in which the wild-type pilin gene was replaced with the aro-5 pilin gene that was previously shown to yield poorly conductive pili in Geobacter sulfurreducens strain Aro-5. G. metallireducens strain Aro-5 did not reduce Fe(III) oxide and produced only low current densities, phenotypes consistent with expression of poorly conductive pili. Like G. sulfurreducens strain Aro-5, G. metallireducens strain Aro-5 displayed abundant outer surface cytochromes. Cocultures initiated with wild-type G. metallireducens as the electron-donating strain and G. sulfurreducens strain Aro-5 as the electron-accepting strain grew via DIET. However, G. metallireducens Aro-5/G. sulfurreducens wild-type cocultures did not. Cocultures initiated with the Aro-5 strains of both species grew only when amended with granular activated carbon (GAC), a conductive material known to be a conduit for DIET. Magnetite could not substitute for GAC. The inability of the two Aro-5 strains to adapt for DIET in the absence of GAC suggests that there are physical constraints on establishing DIET solely through cytochrome-to-cytochrome electron transfer or along chains of magnetite. The finding that DIET is possible with electron-accepting partners that lack highly conductive pili greatly expands the range of potential electron-accepting partners that might participate in DIET. IMPORTANCE DIET is thought to be an important mechanism for interspecies electron exchange in natural anaerobic soils and sediments in which methane is either produced or consumed, as well as in some photosynthetic mats and anaerobic digesters converting organic wastes to methane. Understanding the potential mechanisms for DIET will not only aid in modeling carbon and electron flow in these geochemically significant environments but will also be helpful for interpreting meta-omic data from as-yet-uncultured microbes in DIET-based communities and for designing strategies to promote DIET in anaerobic digesters. The results demonstrate the need to develop a better understanding of the diversity of types of e-pili in the microbial world to identify potential electron-donating partners for DIET. Novel methods for recovering as-yet-uncultivated microorganisms capable of DIET in culture will be needed to further evaluate whether DIET is possible without e-pili in the absence of conductive materials such as GAC.Toshiyuki UekiKelly P. NevinAmelia-Elena RotaruLi-Ying WangJoy E. WardTrevor L. WoodardDerek R. LovleyAmerican Society for MicrobiologyarticleDIETcocultureextracellular electron transfersyntrophyMicrobiologyQR1-502ENmBio, Vol 9, Iss 4 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	DIET coculture extracellular electron transfer syntrophy Microbiology QR1-502
spellingShingle	DIET coculture extracellular electron transfer syntrophy Microbiology QR1-502 Toshiyuki Ueki Kelly P. Nevin Amelia-Elena Rotaru Li-Ying Wang Joy E. Ward Trevor L. Woodard Derek R. Lovley <italic toggle="yes">Geobacter</italic> Strains Expressing Poorly Conductive Pili Reveal Constraints on Direct Interspecies Electron Transfer Mechanisms
description	ABSTRACT Cytochrome-to-cytochrome electron transfer and electron transfer along conduits of multiple extracellular magnetite grains are often proposed as strategies for direct interspecies electron transfer (DIET) that do not require electrically conductive pili (e-pili). However, physical evidence for these proposed DIET mechanisms has been lacking. To investigate these possibilities further, we constructed Geobacter metallireducens strain Aro-5, in which the wild-type pilin gene was replaced with the aro-5 pilin gene that was previously shown to yield poorly conductive pili in Geobacter sulfurreducens strain Aro-5. G. metallireducens strain Aro-5 did not reduce Fe(III) oxide and produced only low current densities, phenotypes consistent with expression of poorly conductive pili. Like G. sulfurreducens strain Aro-5, G. metallireducens strain Aro-5 displayed abundant outer surface cytochromes. Cocultures initiated with wild-type G. metallireducens as the electron-donating strain and G. sulfurreducens strain Aro-5 as the electron-accepting strain grew via DIET. However, G. metallireducens Aro-5/G. sulfurreducens wild-type cocultures did not. Cocultures initiated with the Aro-5 strains of both species grew only when amended with granular activated carbon (GAC), a conductive material known to be a conduit for DIET. Magnetite could not substitute for GAC. The inability of the two Aro-5 strains to adapt for DIET in the absence of GAC suggests that there are physical constraints on establishing DIET solely through cytochrome-to-cytochrome electron transfer or along chains of magnetite. The finding that DIET is possible with electron-accepting partners that lack highly conductive pili greatly expands the range of potential electron-accepting partners that might participate in DIET. IMPORTANCE DIET is thought to be an important mechanism for interspecies electron exchange in natural anaerobic soils and sediments in which methane is either produced or consumed, as well as in some photosynthetic mats and anaerobic digesters converting organic wastes to methane. Understanding the potential mechanisms for DIET will not only aid in modeling carbon and electron flow in these geochemically significant environments but will also be helpful for interpreting meta-omic data from as-yet-uncultured microbes in DIET-based communities and for designing strategies to promote DIET in anaerobic digesters. The results demonstrate the need to develop a better understanding of the diversity of types of e-pili in the microbial world to identify potential electron-donating partners for DIET. Novel methods for recovering as-yet-uncultivated microorganisms capable of DIET in culture will be needed to further evaluate whether DIET is possible without e-pili in the absence of conductive materials such as GAC.
format	article
author	Toshiyuki Ueki Kelly P. Nevin Amelia-Elena Rotaru Li-Ying Wang Joy E. Ward Trevor L. Woodard Derek R. Lovley
author_facet	Toshiyuki Ueki Kelly P. Nevin Amelia-Elena Rotaru Li-Ying Wang Joy E. Ward Trevor L. Woodard Derek R. Lovley
author_sort	Toshiyuki Ueki
title	<italic toggle="yes">Geobacter</italic> Strains Expressing Poorly Conductive Pili Reveal Constraints on Direct Interspecies Electron Transfer Mechanisms
title_short	<italic toggle="yes">Geobacter</italic> Strains Expressing Poorly Conductive Pili Reveal Constraints on Direct Interspecies Electron Transfer Mechanisms
title_full	<italic toggle="yes">Geobacter</italic> Strains Expressing Poorly Conductive Pili Reveal Constraints on Direct Interspecies Electron Transfer Mechanisms
title_fullStr	<italic toggle="yes">Geobacter</italic> Strains Expressing Poorly Conductive Pili Reveal Constraints on Direct Interspecies Electron Transfer Mechanisms
title_full_unstemmed	<italic toggle="yes">Geobacter</italic> Strains Expressing Poorly Conductive Pili Reveal Constraints on Direct Interspecies Electron Transfer Mechanisms
title_sort	<italic toggle="yes">geobacter</italic> strains expressing poorly conductive pili reveal constraints on direct interspecies electron transfer mechanisms
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/dc02b0b3b8a1419e9817f448612d8d16
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<italic toggle="yes">Geobacter</italic> Strains Expressing Poorly Conductive Pili Reveal Constraints on Direct Interspecies Electron Transfer Mechanisms

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