The varied roles of pilA-N, omcE, omcS, omcT, and omcZ in extracellular electron transfer by Geobacter sulfurreducens

Geobacter sulfurreducens mediates extracellular electron transfer (EET) reactions with different substrates, such as solid-phase Fe(III)-containing minerals, anodes and the cells of Geobacter metallireducens. To compare their roles in EET, the pilA-N, omcE, omcS, omcT and omcZ genes of G. sulfurredu...

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Main Authors: Jie Jiang, Pengchen He, Ying Luo, Zhaofeng Peng, Yongguang Jiang, Yidan Hu, Lei Qi, Xiuzhu Dong, Yiran Dong, Liang Shi
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-10-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1251346/full
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author Jie Jiang
Pengchen He
Ying Luo
Zhaofeng Peng
Yongguang Jiang
Yidan Hu
Lei Qi
Xiuzhu Dong
Yiran Dong
Yiran Dong
Yiran Dong
Yiran Dong
Liang Shi
Liang Shi
Liang Shi
Liang Shi
author_facet Jie Jiang
Pengchen He
Ying Luo
Zhaofeng Peng
Yongguang Jiang
Yidan Hu
Lei Qi
Xiuzhu Dong
Yiran Dong
Yiran Dong
Yiran Dong
Yiran Dong
Liang Shi
Liang Shi
Liang Shi
Liang Shi
author_sort Jie Jiang
collection DOAJ
description Geobacter sulfurreducens mediates extracellular electron transfer (EET) reactions with different substrates, such as solid-phase Fe(III)-containing minerals, anodes and the cells of Geobacter metallireducens. To compare their roles in EET, the pilA-N, omcE, omcS, omcT and omcZ genes of G. sulfurreducens were systematically deleted. All mutants showed impaired and varied ability to form biofilms on nonconductive surface. Deletion of omcE also impaired bacterial ability to reduce ferrihydrite, but its impacts on the ability for anode reduction and the co-culture of G. metallireducens-G. sulfurreducens were minimal. The mutant without omcS showed diminished ability to reduce ferrihydrite and to form the co-culture, but was able to regain its ability to reduce anodes. Deletion of omcT, omcZ or pilA-N alone impaired bacterial ability to reduce ferrihydrite and anodes and to form the co-culture. Deletion of all tested genes abolished bacterial ability to reduce ferrihydrite and anodes. Triple-deletion of all omcS, omcT and omcZ abolished the ability of G. sulfurreducens to co-culture with G. metallireducens. However, deletion of only omcZ or pilA-N or both omcS and omcT abolished the ability of G. sulfurreducens without hydrogenase gene hybL to co-culture with G. metallireducens, which show their indispensable roles in direct electron transfer from G. metallireducens to G. sulfurreducens. Thus, the roles of pilA-N, omcE, omcS, omcT and omcZ for G. sulfurreducens in EET vary substantially, which also suggest that possession of PilA-N and multiple cytochromes of different structures enables G. sulfurreducens to mediate EET reactions efficiently with substrates of different properties.
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spelling doaj.art-abaa8df82bfc4206a84f5255f0ddfde82023-10-10T07:05:56ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-10-011410.3389/fmicb.2023.12513461251346The varied roles of pilA-N, omcE, omcS, omcT, and omcZ in extracellular electron transfer by Geobacter sulfurreducensJie Jiang0Pengchen He1Ying Luo2Zhaofeng Peng3Yongguang Jiang4Yidan Hu5Lei Qi6Xiuzhu Dong7Yiran Dong8Yiran Dong9Yiran Dong10Yiran Dong11Liang Shi12Liang Shi13Liang Shi14Liang Shi15School of Environmental Studies, China University of Geosciences-Wuhan, Wuhan, ChinaSchool of Environmental Studies, China University of Geosciences-Wuhan, Wuhan, ChinaSchool of Environmental Studies, China University of Geosciences-Wuhan, Wuhan, ChinaSchool of Environmental Studies, China University of Geosciences-Wuhan, Wuhan, ChinaSchool of Environmental Studies, China University of Geosciences-Wuhan, Wuhan, ChinaSchool of Environmental Studies, China University of Geosciences-Wuhan, Wuhan, ChinaState Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, Beijing, ChinaSchool of Environmental Studies, China University of Geosciences-Wuhan, Wuhan, ChinaState Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences-Wuhan, Wuhan, ChinaState Environmental Protection Key Laboratory of Source Apportionment and Control of Aquatic Pollution, Ministry of Ecology and Environment, China University of Geosciences-Wuhan, Wuhan, ChinaHubei Key Laboratory of Yangtze Catchment Environmental Aquatic Science, China University of Geosciences-Wuhan, Wuhan, ChinaSchool of Environmental Studies, China University of Geosciences-Wuhan, Wuhan, ChinaState Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences-Wuhan, Wuhan, ChinaState Environmental Protection Key Laboratory of Source Apportionment and Control of Aquatic Pollution, Ministry of Ecology and Environment, China University of Geosciences-Wuhan, Wuhan, ChinaHubei Key Laboratory of Yangtze Catchment Environmental Aquatic Science, China University of Geosciences-Wuhan, Wuhan, ChinaGeobacter sulfurreducens mediates extracellular electron transfer (EET) reactions with different substrates, such as solid-phase Fe(III)-containing minerals, anodes and the cells of Geobacter metallireducens. To compare their roles in EET, the pilA-N, omcE, omcS, omcT and omcZ genes of G. sulfurreducens were systematically deleted. All mutants showed impaired and varied ability to form biofilms on nonconductive surface. Deletion of omcE also impaired bacterial ability to reduce ferrihydrite, but its impacts on the ability for anode reduction and the co-culture of G. metallireducens-G. sulfurreducens were minimal. The mutant without omcS showed diminished ability to reduce ferrihydrite and to form the co-culture, but was able to regain its ability to reduce anodes. Deletion of omcT, omcZ or pilA-N alone impaired bacterial ability to reduce ferrihydrite and anodes and to form the co-culture. Deletion of all tested genes abolished bacterial ability to reduce ferrihydrite and anodes. Triple-deletion of all omcS, omcT and omcZ abolished the ability of G. sulfurreducens to co-culture with G. metallireducens. However, deletion of only omcZ or pilA-N or both omcS and omcT abolished the ability of G. sulfurreducens without hydrogenase gene hybL to co-culture with G. metallireducens, which show their indispensable roles in direct electron transfer from G. metallireducens to G. sulfurreducens. Thus, the roles of pilA-N, omcE, omcS, omcT and omcZ for G. sulfurreducens in EET vary substantially, which also suggest that possession of PilA-N and multiple cytochromes of different structures enables G. sulfurreducens to mediate EET reactions efficiently with substrates of different properties.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1251346/fullpilA-Nmultiheme c-type cytochromesextracellular electron transferbiofilmsGeobacter metallireducensGeobacter sulfurreducens
spellingShingle Jie Jiang
Pengchen He
Ying Luo
Zhaofeng Peng
Yongguang Jiang
Yidan Hu
Lei Qi
Xiuzhu Dong
Yiran Dong
Yiran Dong
Yiran Dong
Yiran Dong
Liang Shi
Liang Shi
Liang Shi
Liang Shi
The varied roles of pilA-N, omcE, omcS, omcT, and omcZ in extracellular electron transfer by Geobacter sulfurreducens
Frontiers in Microbiology
pilA-N
multiheme c-type cytochromes
extracellular electron transfer
biofilms
Geobacter metallireducens
Geobacter sulfurreducens
title The varied roles of pilA-N, omcE, omcS, omcT, and omcZ in extracellular electron transfer by Geobacter sulfurreducens
title_full The varied roles of pilA-N, omcE, omcS, omcT, and omcZ in extracellular electron transfer by Geobacter sulfurreducens
title_fullStr The varied roles of pilA-N, omcE, omcS, omcT, and omcZ in extracellular electron transfer by Geobacter sulfurreducens
title_full_unstemmed The varied roles of pilA-N, omcE, omcS, omcT, and omcZ in extracellular electron transfer by Geobacter sulfurreducens
title_short The varied roles of pilA-N, omcE, omcS, omcT, and omcZ in extracellular electron transfer by Geobacter sulfurreducens
title_sort varied roles of pila n omce omcs omct and omcz in extracellular electron transfer by geobacter sulfurreducens
topic pilA-N
multiheme c-type cytochromes
extracellular electron transfer
biofilms
Geobacter metallireducens
Geobacter sulfurreducens
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1251346/full
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