Response of the Anaerobic Methanotrophic Archaeon Candidatus “Methanoperedens nitroreducens” to the Long-Term Ferrihydrite Amendment

Anaerobic methanotrophic (ANME) archaea can drive anaerobic oxidation of methane (AOM) using solid iron or manganese oxides as the electron acceptors, hypothetically via direct extracellular electron transfer (EET). This study investigated the response of Candidatus “Methanoperedens nitroreducens TS...

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Main Authors: Chen Cai, Gaofeng Ni, Jun Xia, Xueqin Zhang, Yue Zheng, Bingqing He, Esteban Marcellin, Weiwei Li, Jiaoyang Pu, Zhiguo Yuan, Shihu Hu
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-04-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.799859/full
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author Chen Cai
Chen Cai
Gaofeng Ni
Jun Xia
Xueqin Zhang
Yue Zheng
Bingqing He
Bingqing He
Esteban Marcellin
Weiwei Li
Weiwei Li
Jiaoyang Pu
Zhiguo Yuan
Shihu Hu
author_facet Chen Cai
Chen Cai
Gaofeng Ni
Jun Xia
Xueqin Zhang
Yue Zheng
Bingqing He
Bingqing He
Esteban Marcellin
Weiwei Li
Weiwei Li
Jiaoyang Pu
Zhiguo Yuan
Shihu Hu
author_sort Chen Cai
collection DOAJ
description Anaerobic methanotrophic (ANME) archaea can drive anaerobic oxidation of methane (AOM) using solid iron or manganese oxides as the electron acceptors, hypothetically via direct extracellular electron transfer (EET). This study investigated the response of Candidatus “Methanoperedens nitroreducens TS” (type strain), an ANME archaeon previously characterized to perform nitrate-dependent AOM, to an Fe(III)-amended condition over a prolonged period. Simultaneous consumption of methane and production of dissolved Fe(II) were observed for more than 500 days in the presence of Ca. “M. nitroreducens TS,” indicating that this archaeon can carry out Fe(III)-dependent AOM for a long period. Ca. “M. nitroreducens TS” possesses multiple multiheme c-type cytochromes (MHCs), suggesting that it may have the capability to reduce Fe(III) via EET. Intriguingly, most of these MHCs are orthologous to those identified in Candidatus “Methanoperedens ferrireducens,” an Fe(III)-reducing ANME archaeon. In contrast, the population of Ca. “M. nitroreducens TS” declined and was eventually replaced by Ca. “M. ferrireducens,” implying niche differentiation between these two ANME archaea in the environment.
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spelling doaj.art-9dff7095d1dc467c892270869defe3862022-12-22T02:57:33ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-04-011310.3389/fmicb.2022.799859799859Response of the Anaerobic Methanotrophic Archaeon Candidatus “Methanoperedens nitroreducens” to the Long-Term Ferrihydrite AmendmentChen Cai0Chen Cai1Gaofeng Ni2Jun Xia3Xueqin Zhang4Yue Zheng5Bingqing He6Bingqing He7Esteban Marcellin8Weiwei Li9Weiwei Li10Jiaoyang Pu11Zhiguo Yuan12Shihu Hu13CAS Key Laboratory of Urban Pollutant Conversion, Department of Environmental Science and Engineering, University of Science and Technology of China, Hefei, ChinaAustralian Centre for Water and Environmental Biotechnology, The University of Queensland, St Lucia, QLD, AustraliaAustralian Centre for Water and Environmental Biotechnology, The University of Queensland, St Lucia, QLD, AustraliaAustralian Centre for Water and Environmental Biotechnology, The University of Queensland, St Lucia, QLD, AustraliaAustralian Centre for Water and Environmental Biotechnology, The University of Queensland, St Lucia, QLD, AustraliaState Key Laboratory of Marine Environmental Science, College of the Environment and Ecology, Xiamen University, Xiamen, ChinaAustralian Centre for Water and Environmental Biotechnology, The University of Queensland, St Lucia, QLD, AustraliaAustralian Institute for Bioengineering and Nanotechnology, The University of Queensland, St Lucia, QLD, AustraliaAustralian Institute for Bioengineering and Nanotechnology, The University of Queensland, St Lucia, QLD, AustraliaAustralian Centre for Water and Environmental Biotechnology, The University of Queensland, St Lucia, QLD, AustraliaState Key Laboratory of Coal Mine Disaster Dynamics and Control, Chongqing University, Chongqing, ChinaAustralian Centre for Water and Environmental Biotechnology, The University of Queensland, St Lucia, QLD, AustraliaAustralian Centre for Water and Environmental Biotechnology, The University of Queensland, St Lucia, QLD, AustraliaAustralian Centre for Water and Environmental Biotechnology, The University of Queensland, St Lucia, QLD, AustraliaAnaerobic methanotrophic (ANME) archaea can drive anaerobic oxidation of methane (AOM) using solid iron or manganese oxides as the electron acceptors, hypothetically via direct extracellular electron transfer (EET). This study investigated the response of Candidatus “Methanoperedens nitroreducens TS” (type strain), an ANME archaeon previously characterized to perform nitrate-dependent AOM, to an Fe(III)-amended condition over a prolonged period. Simultaneous consumption of methane and production of dissolved Fe(II) were observed for more than 500 days in the presence of Ca. “M. nitroreducens TS,” indicating that this archaeon can carry out Fe(III)-dependent AOM for a long period. Ca. “M. nitroreducens TS” possesses multiple multiheme c-type cytochromes (MHCs), suggesting that it may have the capability to reduce Fe(III) via EET. Intriguingly, most of these MHCs are orthologous to those identified in Candidatus “Methanoperedens ferrireducens,” an Fe(III)-reducing ANME archaeon. In contrast, the population of Ca. “M. nitroreducens TS” declined and was eventually replaced by Ca. “M. ferrireducens,” implying niche differentiation between these two ANME archaea in the environment.https://www.frontiersin.org/articles/10.3389/fmicb.2022.799859/fullanaerobic oxidation of methaneFe(III) reductionANME archaeaextracellular electron transfermultiheme c-type cytochromesmethanogen
spellingShingle Chen Cai
Chen Cai
Gaofeng Ni
Jun Xia
Xueqin Zhang
Yue Zheng
Bingqing He
Bingqing He
Esteban Marcellin
Weiwei Li
Weiwei Li
Jiaoyang Pu
Zhiguo Yuan
Shihu Hu
Response of the Anaerobic Methanotrophic Archaeon Candidatus “Methanoperedens nitroreducens” to the Long-Term Ferrihydrite Amendment
Frontiers in Microbiology
anaerobic oxidation of methane
Fe(III) reduction
ANME archaea
extracellular electron transfer
multiheme c-type cytochromes
methanogen
title Response of the Anaerobic Methanotrophic Archaeon Candidatus “Methanoperedens nitroreducens” to the Long-Term Ferrihydrite Amendment
title_full Response of the Anaerobic Methanotrophic Archaeon Candidatus “Methanoperedens nitroreducens” to the Long-Term Ferrihydrite Amendment
title_fullStr Response of the Anaerobic Methanotrophic Archaeon Candidatus “Methanoperedens nitroreducens” to the Long-Term Ferrihydrite Amendment
title_full_unstemmed Response of the Anaerobic Methanotrophic Archaeon Candidatus “Methanoperedens nitroreducens” to the Long-Term Ferrihydrite Amendment
title_short Response of the Anaerobic Methanotrophic Archaeon Candidatus “Methanoperedens nitroreducens” to the Long-Term Ferrihydrite Amendment
title_sort response of the anaerobic methanotrophic archaeon candidatus methanoperedens nitroreducens to the long term ferrihydrite amendment
topic anaerobic oxidation of methane
Fe(III) reduction
ANME archaea
extracellular electron transfer
multiheme c-type cytochromes
methanogen
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.799859/full
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