Nitrous oxide act as an alternative electron acceptor for microbial methane oxidation in oxygen-deficient microcosms

Submerged paddy is a hotspot of nitrous oxide (N2O) and methane (CH4) emission, which is typically considered electron donor and acceptor for microbes, respectively. Theoretical calculations suggested the thermodynamic feasibility of anaerobic CH4 oxidation coupled with N2O reduction (AMNR), and ana...

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Main Authors: Fengqin Liu, Yu Zhang, Mingting Xie, Zhiliang Yuan, Zhongjun Jia, Yupeng Zhang
Format: Article
Language:English
Published: Elsevier 2025-03-01
Series:Geoderma
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Online Access:http://www.sciencedirect.com/science/article/pii/S0016706125000515
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author Fengqin Liu
Yu Zhang
Mingting Xie
Zhiliang Yuan
Zhongjun Jia
Yupeng Zhang
author_facet Fengqin Liu
Yu Zhang
Mingting Xie
Zhiliang Yuan
Zhongjun Jia
Yupeng Zhang
author_sort Fengqin Liu
collection DOAJ
description Submerged paddy is a hotspot of nitrous oxide (N2O) and methane (CH4) emission, which is typically considered electron donor and acceptor for microbes, respectively. Theoretical calculations suggested the thermodynamic feasibility of anaerobic CH4 oxidation coupled with N2O reduction (AMNR), and anaerobic methane oxidation and denitrification are typically coupled by certain anaerobic microbes, such as Ca. Methylomirabilis sinica from the NC10 phylum. However, the conventional aerobic methanotrophs underlying this novel greenhouse gas sink remain largely unclear. Four typical soil sample from different latitudes in China were used as inoculum. Enrichment reactors were constructed with continuous CH4 and N2O supply for 400 days to cultivate aerobic methanotrophs capable of N2O reduction. This study revealed that conventional methanotrophs, such as species from the Methylocystis and Methylobacterium genera, are the key taxa catalyzing the AMNR process. Consistently high N2O reduction rate (5.37–6.24 μmol·g−1-dry soil·d−1) was observed in strong association with CO2 formation, that was nearly matched with the expected stoichiometry (4:1). The N2O reduction process occurred in two distinct phases: a rapid reduction phase concurrent with CH4 oxidation, followed by a slower reduction phase. N2O was directly reduced by conventional aerobic methanotrophs harboring the nosZ gene, such as Methylocystis, or by denitrifiers using the fermentative intermediates produced by methanotrophs as electron donors. This suggests that conventional methanotrophs, which typically perform aerobic methane oxidation, could also have denitrification potential, possibly facilitated by the presence of the nosZ gene. Although methanotrophs and denitrifiers are usually considered distinct groups, these results indicate that the AMNR process could allow for the simultaneous oxidation of CH4 and reduction of N2O in paddy soils, thus enhancing the potential for greenhouse gas mitigation.
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spelling doaj-art-d7a56d7698194c65ba815ecb477a7fa02025-08-20T02:56:52ZengElsevierGeoderma1872-62592025-03-0145511721310.1016/j.geoderma.2025.117213Nitrous oxide act as an alternative electron acceptor for microbial methane oxidation in oxygen-deficient microcosmsFengqin Liu0Yu Zhang1Mingting Xie2Zhiliang Yuan3Zhongjun Jia4Yupeng Zhang5College of Life Sciences, Henan Agricultural University, No.63 Agricultural Road, Zhengzhou 450002, PR China; State Key Laboratory of Black Soils Conservation and Utilization, Northeast Institute of Geography and Agroecology, Chinese Academy of Science, Changchun 130102, PR ChinaCollege of Life Sciences, Henan Agricultural University, No.63 Agricultural Road, Zhengzhou 450002, PR ChinaCollege of Life Sciences, Henan Agricultural University, No.63 Agricultural Road, Zhengzhou 450002, PR ChinaCollege of Life Sciences, Henan Agricultural University, No.63 Agricultural Road, Zhengzhou 450002, PR ChinaState Key Laboratory of Black Soils Conservation and Utilization, Northeast Institute of Geography and Agroecology, Chinese Academy of Science, Changchun 130102, PR China; Corresponding authors at: State Key Laboratory of Black Soils Conservation and Utilization, Northeast Institute of Geography and Agroecology, Chinese Academy of Science, Changchun 130102, PR China (Z. Jia). College of Resources and Environmental Sciences, Henan Agricultural University, No.63 Agricultural Road, Zhengzhou, 450002, PR China (Y. Zhang).College of Resources and Environmental Sciences, Henan Agricultural University, No.63 Agricultural Road, Zhengzhou 450002, PR China; Corresponding authors at: State Key Laboratory of Black Soils Conservation and Utilization, Northeast Institute of Geography and Agroecology, Chinese Academy of Science, Changchun 130102, PR China (Z. Jia). College of Resources and Environmental Sciences, Henan Agricultural University, No.63 Agricultural Road, Zhengzhou, 450002, PR China (Y. Zhang).Submerged paddy is a hotspot of nitrous oxide (N2O) and methane (CH4) emission, which is typically considered electron donor and acceptor for microbes, respectively. Theoretical calculations suggested the thermodynamic feasibility of anaerobic CH4 oxidation coupled with N2O reduction (AMNR), and anaerobic methane oxidation and denitrification are typically coupled by certain anaerobic microbes, such as Ca. Methylomirabilis sinica from the NC10 phylum. However, the conventional aerobic methanotrophs underlying this novel greenhouse gas sink remain largely unclear. Four typical soil sample from different latitudes in China were used as inoculum. Enrichment reactors were constructed with continuous CH4 and N2O supply for 400 days to cultivate aerobic methanotrophs capable of N2O reduction. This study revealed that conventional methanotrophs, such as species from the Methylocystis and Methylobacterium genera, are the key taxa catalyzing the AMNR process. Consistently high N2O reduction rate (5.37–6.24 μmol·g−1-dry soil·d−1) was observed in strong association with CO2 formation, that was nearly matched with the expected stoichiometry (4:1). The N2O reduction process occurred in two distinct phases: a rapid reduction phase concurrent with CH4 oxidation, followed by a slower reduction phase. N2O was directly reduced by conventional aerobic methanotrophs harboring the nosZ gene, such as Methylocystis, or by denitrifiers using the fermentative intermediates produced by methanotrophs as electron donors. This suggests that conventional methanotrophs, which typically perform aerobic methane oxidation, could also have denitrification potential, possibly facilitated by the presence of the nosZ gene. Although methanotrophs and denitrifiers are usually considered distinct groups, these results indicate that the AMNR process could allow for the simultaneous oxidation of CH4 and reduction of N2O in paddy soils, thus enhancing the potential for greenhouse gas mitigation.http://www.sciencedirect.com/science/article/pii/S0016706125000515Paddy soilCH4 oxidationN2O reductionDenitrificationMethanotrophs
spellingShingle Fengqin Liu
Yu Zhang
Mingting Xie
Zhiliang Yuan
Zhongjun Jia
Yupeng Zhang
Nitrous oxide act as an alternative electron acceptor for microbial methane oxidation in oxygen-deficient microcosms
Geoderma
Paddy soil
CH4 oxidation
N2O reduction
Denitrification
Methanotrophs
title Nitrous oxide act as an alternative electron acceptor for microbial methane oxidation in oxygen-deficient microcosms
title_full Nitrous oxide act as an alternative electron acceptor for microbial methane oxidation in oxygen-deficient microcosms
title_fullStr Nitrous oxide act as an alternative electron acceptor for microbial methane oxidation in oxygen-deficient microcosms
title_full_unstemmed Nitrous oxide act as an alternative electron acceptor for microbial methane oxidation in oxygen-deficient microcosms
title_short Nitrous oxide act as an alternative electron acceptor for microbial methane oxidation in oxygen-deficient microcosms
title_sort nitrous oxide act as an alternative electron acceptor for microbial methane oxidation in oxygen deficient microcosms
topic Paddy soil
CH4 oxidation
N2O reduction
Denitrification
Methanotrophs
url http://www.sciencedirect.com/science/article/pii/S0016706125000515
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AT mingtingxie nitrousoxideactasanalternativeelectronacceptorformicrobialmethaneoxidationinoxygendeficientmicrocosms
AT zhiliangyuan nitrousoxideactasanalternativeelectronacceptorformicrobialmethaneoxidationinoxygendeficientmicrocosms
AT zhongjunjia nitrousoxideactasanalternativeelectronacceptorformicrobialmethaneoxidationinoxygendeficientmicrocosms
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