Metabolic coupling between soil aerobic methanotrophs and denitrifiers in rice paddy fields

Kang-Hua Chen, Jiao Feng (), Paul L. E. Bodelier, Ziming Yang, Qiaoyun Huang, Manuel Delgado-Baquerizo, Peng Cai, Wenfeng Tan and Yu-Rong Liu ()
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Kang-Hua Chen: Huazhong Agricultural University
Jiao Feng: Huazhong Agricultural University
Paul L. E. Bodelier: Netherlands Institute of Ecology (NIOO-KNAW)
Ziming Yang: Oakland University
Qiaoyun Huang: Huazhong Agricultural University
Manuel Delgado-Baquerizo: CSIC
Peng Cai: Huazhong Agricultural University
Wenfeng Tan: Huazhong Agricultural University
Yu-Rong Liu: Huazhong Agricultural University

Nature Communications, 2024, vol. 15, issue 1, 1-15

Abstract: Abstract Paddy fields are hotspots of microbial denitrification, which is typically linked to the oxidation of electron donors such as methane (CH4) under anoxic and hypoxic conditions. While several anaerobic methanotrophs can facilitate denitrification intracellularly, whether and how aerobic CH4 oxidation couples with denitrification in hypoxic paddy fields remains virtually unknown. Here we combine a ~3300 km field study across main rice-producing areas of China and 13CH4-DNA-stable isotope probing (SIP) experiments to investigate the role of soil aerobic CH4 oxidation in supporting denitrification. Our results reveal positive relationships between CH4 oxidation and denitrification activities and genes across various climatic regions. Microcosm experiments confirm that CH4 and methanotroph addition promote gene expression involved in denitrification and increase nitrous oxide emissions. Moreover, 13CH4-DNA-SIP analyses identify over 70 phylotypes harboring genes associated with denitrification and assimilating 13C, which are mostly belonged to Rubrivivax, Magnetospirillum, and Bradyrhizobium. Combined analyses of 13C-metagenome-assembled genomes and 13C-metabolomics highlight the importance of intermediates such as acetate, propionate and lactate, released during aerobic CH4 oxidation, for the coupling of CH4 oxidation with denitrification. Our work identifies key microbial taxa and pathways driving coupled aerobic CH4 oxidation and denitrification, with important implications for nitrogen management and greenhouse gas regulation in agroecosystems.

Date: 2024
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DOI: 10.1038/s41467-024-47827-y

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