Abstract
AbstractPaddy 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.
Publisher
Springer Science and Business Media LLC
Reference110 articles.
1. Canfield, D. E., Glazer, A. N. & Falkowski, P. G. The evolution and future of Earth’s nitrogen cycle. Science 330, 192–196 (2010).
2. Heffer, P. & Prud’ homme, M. Global nitrogen fertiliser demand and supply: trend, current level and outlook. In Proceedings of the 2016 International Nitrogen Initiative Conference, “Solutions to Improve Nitrogen Use Efficiency for the World”. Melbourne, Australia 4–8 (2016).
3. Liu, C., Watanabe, M. & Wang, Q. Changes in nitrogen budgets and nitrogen use efficiency in the agroecosystems of the Changjiang river basin between 1980 and 2000. Nutr. Cycl. Agroecosyst. 80, 19–37 (2007).
4. Masuda, Y., Matsumoto, T., Isobe, K. & Senoo, K. Denitrification in paddy soil as a cooperative process of different nitrogen oxide reducers, revealed by metatranscriptomic analysis of denitrification-induced soil microcosm. Soil Sci. Plant. Nutr. 65, 342–345 (2019).
5. Opdyke, M. R., Ostrom, N. E. & Ostrom, P. H. Evidence for the predominance of denitrification as a source of N2O in temperate agricultural soils based on isotopologue measurements. Glob. Biogeochem. Cycles 23, GB4018 (2009).