Current production by non-methanotrophic bacteria enriched from an anaerobic methane-oxidizing microbial community

In recent years, the externalization of electrons as part of respiratory metabolic processes has been discovered in many different bacteria and some archaea. Microbial extracellular electron transfer (EET) plays an important role in many anoxic natural or engineered ecosystems. In this study, an ana...

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Main Authors: S. Berger, D.R. Shaw, T. Berben, H.T. Ouboter, M.H. in ’t Zandt, J. Frank, J. Reimann, M.S.M. Jetten, C.U. Welte
Format: Article
Language:English
Published: Elsevier 2021-12-01
Series:Biofilm
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2590207521000125
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author S. Berger
D.R. Shaw
T. Berben
H.T. Ouboter
M.H. in ’t Zandt
J. Frank
J. Reimann
M.S.M. Jetten
C.U. Welte
spellingShingle S. Berger
D.R. Shaw
T. Berben
H.T. Ouboter
M.H. in ’t Zandt
J. Frank
J. Reimann
M.S.M. Jetten
C.U. Welte
Current production by non-methanotrophic bacteria enriched from an anaerobic methane-oxidizing microbial community
Biofilm
Extracellular electron transfer
Microbial community
Acetate
Cytochromes
Zoogloea
ANME-2d
author_facet S. Berger
D.R. Shaw
T. Berben
H.T. Ouboter
M.H. in ’t Zandt
J. Frank
J. Reimann
M.S.M. Jetten
C.U. Welte
author_sort S. Berger
title Current production by non-methanotrophic bacteria enriched from an anaerobic methane-oxidizing microbial community
title_short Current production by non-methanotrophic bacteria enriched from an anaerobic methane-oxidizing microbial community
title_full Current production by non-methanotrophic bacteria enriched from an anaerobic methane-oxidizing microbial community
title_fullStr Current production by non-methanotrophic bacteria enriched from an anaerobic methane-oxidizing microbial community
title_full_unstemmed Current production by non-methanotrophic bacteria enriched from an anaerobic methane-oxidizing microbial community
title_sort current production by non-methanotrophic bacteria enriched from an anaerobic methane-oxidizing microbial community
publisher Elsevier
series Biofilm
issn 2590-2075
publishDate 2021-12-01
description In recent years, the externalization of electrons as part of respiratory metabolic processes has been discovered in many different bacteria and some archaea. Microbial extracellular electron transfer (EET) plays an important role in many anoxic natural or engineered ecosystems. In this study, an anaerobic methane-converting microbial community was investigated with regard to its potential to perform EET. At this point, it is not well-known if or how EET confers a competitive advantage to certain species in methane-converting communities. EET was investigated in a two-chamber electrochemical system, sparged with methane and with an applied potential of +400 mV versus standard hydrogen electrode. A biofilm developed on the working electrode and stable low-density current was produced, confirming that EET indeed did occur. The appearance and presence of redox centers at −140 to −160 mV and at −230 mV in the biofilm was confirmed by cyclic voltammetry scans. Metagenomic analysis and fluorescence in situ hybridization of the biofilm showed that the anaerobic methanotroph ‘Candidatus Methanoperedens BLZ2’ was a significant member of the biofilm community, but its relative abundance did not increase compared to the inoculum. On the contrary, the relative abundance of other members of the microbial community significantly increased (up to 720-fold, 7.2% of mapped reads), placing these microorganisms among the dominant species in the bioanode community. This group included Zoogloea sp., Dechloromonas sp., two members of the Bacteroidetes phylum, and the spirochete Leptonema sp. Genes encoding proteins putatively involved in EET were identified in Zoogloea sp., Dechloromonas sp. and one member of the Bacteroidetes phylum. We suggest that instead of methane, alternative carbon sources such as acetate were the substrate for EET. Hence, EET in a methane-driven chemolithoautotrophic microbial community seems a complex process in which interactions within the microbial community are driving extracellular electron transfer to the electrode.
topic Extracellular electron transfer
Microbial community
Acetate
Cytochromes
Zoogloea
ANME-2d
url http://www.sciencedirect.com/science/article/pii/S2590207521000125
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spelling doaj-6b1996db546f42179ff8e42e35d357992021-07-01T04:35:26ZengElsevierBiofilm2590-20752021-12-013100054Current production by non-methanotrophic bacteria enriched from an anaerobic methane-oxidizing microbial communityS. Berger0D.R. Shaw1T. Berben2H.T. Ouboter3M.H. in ’t Zandt4J. Frank5J. Reimann6M.S.M. Jetten7C.U. Welte8Institute for Water and Wetland Research, Department of Microbiology, Radboud University, Nijmegen, the NetherlandsBiological and Environmental Science and Engineering Division, Water Desalination and Reuse Research Center, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia; Soehngen Institute of Anaerobic Microbiology, Radboud University, Nijmegen, the NetherlandsInstitute for Water and Wetland Research, Department of Microbiology, Radboud University, Nijmegen, the NetherlandsInstitute for Water and Wetland Research, Department of Microbiology, Radboud University, Nijmegen, the Netherlands; Soehngen Institute of Anaerobic Microbiology, Radboud University, Nijmegen, the NetherlandsInstitute for Water and Wetland Research, Department of Microbiology, Radboud University, Nijmegen, the Netherlands; Netherlands Earth System Science Center, Utrecht University, Utrecht, the NetherlandsInstitute for Water and Wetland Research, Department of Microbiology, Radboud University, Nijmegen, the Netherlands; Soehngen Institute of Anaerobic Microbiology, Radboud University, Nijmegen, the NetherlandsInstitute for Water and Wetland Research, Department of Microbiology, Radboud University, Nijmegen, the NetherlandsInstitute for Water and Wetland Research, Department of Microbiology, Radboud University, Nijmegen, the Netherlands; Netherlands Earth System Science Center, Utrecht University, Utrecht, the Netherlands; Soehngen Institute of Anaerobic Microbiology, Radboud University, Nijmegen, the NetherlandsInstitute for Water and Wetland Research, Department of Microbiology, Radboud University, Nijmegen, the Netherlands; Soehngen Institute of Anaerobic Microbiology, Radboud University, Nijmegen, the Netherlands; Corresponding author. Radboud University, Institute for Water and Wetland Research, Department of Microbiology, Heyendaalseweg 135, 6525AJ, Nijmegen, the Netherlands.In recent years, the externalization of electrons as part of respiratory metabolic processes has been discovered in many different bacteria and some archaea. Microbial extracellular electron transfer (EET) plays an important role in many anoxic natural or engineered ecosystems. In this study, an anaerobic methane-converting microbial community was investigated with regard to its potential to perform EET. At this point, it is not well-known if or how EET confers a competitive advantage to certain species in methane-converting communities. EET was investigated in a two-chamber electrochemical system, sparged with methane and with an applied potential of +400 mV versus standard hydrogen electrode. A biofilm developed on the working electrode and stable low-density current was produced, confirming that EET indeed did occur. The appearance and presence of redox centers at −140 to −160 mV and at −230 mV in the biofilm was confirmed by cyclic voltammetry scans. Metagenomic analysis and fluorescence in situ hybridization of the biofilm showed that the anaerobic methanotroph ‘Candidatus Methanoperedens BLZ2’ was a significant member of the biofilm community, but its relative abundance did not increase compared to the inoculum. On the contrary, the relative abundance of other members of the microbial community significantly increased (up to 720-fold, 7.2% of mapped reads), placing these microorganisms among the dominant species in the bioanode community. This group included Zoogloea sp., Dechloromonas sp., two members of the Bacteroidetes phylum, and the spirochete Leptonema sp. Genes encoding proteins putatively involved in EET were identified in Zoogloea sp., Dechloromonas sp. and one member of the Bacteroidetes phylum. We suggest that instead of methane, alternative carbon sources such as acetate were the substrate for EET. Hence, EET in a methane-driven chemolithoautotrophic microbial community seems a complex process in which interactions within the microbial community are driving extracellular electron transfer to the electrode.http://www.sciencedirect.com/science/article/pii/S2590207521000125Extracellular electron transferMicrobial communityAcetateCytochromesZoogloeaANME-2d