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Conjugative plasmids inhibit extracellular electron transfer in Geobacter sulfurreducens

Geobacter sulfurreducens is part of a specialized group of microbes with the unique ability to exchange electrons with insoluble materials, such as iron oxides and electrodes. Therefore, G. sulfurreducens plays an essential role in the biogeochemical iron cycle and microbial electrochemical systems....

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Autores principales: Fessler, Mathias, Madsen, Jonas Stenløkke, Zhang, Yifeng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10063792/
https://www.ncbi.nlm.nih.gov/pubmed/37007462
http://dx.doi.org/10.3389/fmicb.2023.1150091
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author Fessler, Mathias
Madsen, Jonas Stenløkke
Zhang, Yifeng
author_facet Fessler, Mathias
Madsen, Jonas Stenløkke
Zhang, Yifeng
author_sort Fessler, Mathias
collection PubMed
description Geobacter sulfurreducens is part of a specialized group of microbes with the unique ability to exchange electrons with insoluble materials, such as iron oxides and electrodes. Therefore, G. sulfurreducens plays an essential role in the biogeochemical iron cycle and microbial electrochemical systems. In G. sulfurreducens this ability is primarily dependent on electrically conductive nanowires that link internal electron flow from metabolism to solid electron acceptors in the extracellular environment. Here we show that when carrying conjugative plasmids, which are self-transmissible plasmids that are ubiquitous in environmental bacteria, G. sulfurreducens reduces insoluble iron oxides at much slower rates. This was the case for all three conjugative plasmids tested (pKJK5, RP4 and pB10). Growth with electron acceptors that do not require expression of nanowires was, on the other hand, unaffected. Furthermore, iron oxide reduction was also inhibited in Geobacter chapellei, but not in Shewanella oneidensis where electron export is nanowire-independent. As determined by transcriptomics, presence of pKJK5 reduces transcription of several genes that have been shown to be implicated in extracellular electron transfer in G. sulfurreducens, including pilA and omcE. These results suggest that conjugative plasmids can in fact be very disadvantageous for the bacterial host by imposing specific phenotypic changes, and that these plasmids may contribute to shaping the microbial composition in electrode-respiring biofilms in microbial electrochemical reactors.
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spelling pubmed-100637922023-04-01 Conjugative plasmids inhibit extracellular electron transfer in Geobacter sulfurreducens Fessler, Mathias Madsen, Jonas Stenløkke Zhang, Yifeng Front Microbiol Microbiology Geobacter sulfurreducens is part of a specialized group of microbes with the unique ability to exchange electrons with insoluble materials, such as iron oxides and electrodes. Therefore, G. sulfurreducens plays an essential role in the biogeochemical iron cycle and microbial electrochemical systems. In G. sulfurreducens this ability is primarily dependent on electrically conductive nanowires that link internal electron flow from metabolism to solid electron acceptors in the extracellular environment. Here we show that when carrying conjugative plasmids, which are self-transmissible plasmids that are ubiquitous in environmental bacteria, G. sulfurreducens reduces insoluble iron oxides at much slower rates. This was the case for all three conjugative plasmids tested (pKJK5, RP4 and pB10). Growth with electron acceptors that do not require expression of nanowires was, on the other hand, unaffected. Furthermore, iron oxide reduction was also inhibited in Geobacter chapellei, but not in Shewanella oneidensis where electron export is nanowire-independent. As determined by transcriptomics, presence of pKJK5 reduces transcription of several genes that have been shown to be implicated in extracellular electron transfer in G. sulfurreducens, including pilA and omcE. These results suggest that conjugative plasmids can in fact be very disadvantageous for the bacterial host by imposing specific phenotypic changes, and that these plasmids may contribute to shaping the microbial composition in electrode-respiring biofilms in microbial electrochemical reactors. Frontiers Media S.A. 2023-03-17 /pmc/articles/PMC10063792/ /pubmed/37007462 http://dx.doi.org/10.3389/fmicb.2023.1150091 Text en Copyright © 2023 Fessler, Madsen and Zhang. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Fessler, Mathias
Madsen, Jonas Stenløkke
Zhang, Yifeng
Conjugative plasmids inhibit extracellular electron transfer in Geobacter sulfurreducens
title Conjugative plasmids inhibit extracellular electron transfer in Geobacter sulfurreducens
title_full Conjugative plasmids inhibit extracellular electron transfer in Geobacter sulfurreducens
title_fullStr Conjugative plasmids inhibit extracellular electron transfer in Geobacter sulfurreducens
title_full_unstemmed Conjugative plasmids inhibit extracellular electron transfer in Geobacter sulfurreducens
title_short Conjugative plasmids inhibit extracellular electron transfer in Geobacter sulfurreducens
title_sort conjugative plasmids inhibit extracellular electron transfer in geobacter sulfurreducens
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10063792/
https://www.ncbi.nlm.nih.gov/pubmed/37007462
http://dx.doi.org/10.3389/fmicb.2023.1150091
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