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Type I methanotrophs dominated methane oxidation and assimilation in rice paddy fields by the consequence of niche differentiation

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A Correction to this article was published on 28 December 2023

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Abstract

Conventional aerobic methanotrophs oxidize methane (CH4) and covert CH4-derived carbon (C) into biomass at the oxic-anoxic interface of inundated rice paddy fields, playing indispensable role in mitigating greenhouse gas emissions and loss of organic C from methanogenesis. Two phylogenetically distinct groups of methanotrophs, type I (γ-proteobacteria) and type II (α-proteobacteria) methanotrophs, often co-exist in rice paddy soil and compete for CH4 biotransformation. Since these two methanotrophic groups also possess differential kinetics of CH4 oxidation and pathways of C assimilation, the consequence of their niche differentiation and metabolic differences in soil is expected to affect the CH4 oxidation rate and C conversion efficiency. Here, we examined the microbiology, chemistry, and CH4 metabolism in 24 geographically different paddy soils, covering four climate zones of eastern China. High-throughput sequencing of pmoA gene displayed a clear separation of in situ methanotrophic compositions between temperate (warm and mid-temperate) and warmer (subtropics and tropics) climate zones, likely driven by soil pH. Both methanotrophic groups were detected in soils but proportions of type I methanotrophs increased in temperate soils of higher pH (accounting for 76.1 ± 12.4% and 44.1 ± 14.8% in warm temperate and mid-temperate, respectively). Type II methanotrophs prevailed in warmer zones (accounting for 66.2 ± 21.6% and 70.5 ± 12.1% in tropics and subtropics, respectively) where soils were more acidic. Higher incorporation of 13C for synthesis in C14+C16 PLFAs (63.1–93.4% of total production of 13C-PLFAs) was found based on microcosm incubation, reflecting type I methanotrophs dominated the CH4 assimilation in paddy soils. Particularly, temperate soils with increased proportions of type I methanotrophs showed higher CH4 oxidation rate and C conversion efficiency. Collectively, this study depicts a continental-scale disparity of methanotrophic dynamics that tightly associates with consequence of niche differentiation of different types of methanotrophs and highlights the importance of microbiological control to maximize the rate and efficiency of methanotrophy.

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Funding

This work was financially supported by the National Key Research Program (2021YFD1901204, 2021YFD1901203), National Natural Science Foundation of China (grant numbers 42377348, 42177295), Natural Science Foundation of Fujian Province (2022J05263), Nanping City Science and Technology Plan Project (NP2021KTS02), Talent Introduction Project of Wuyi University (YJ202117), and Open Foundation of State Key Laboratory of Microbial Technology in Shandong University (M2022-05).

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J.S.W., Y.R.S., and X.B.C. conceived and designed the experiments. S.M.Z., S.H.D., C.M., Y.H.X., and H.Q. performed the experiments and collected the data. S.M.Z. and S.H.D. analyzed the data. S.M.Z. illustrated the figures and wrote the first draft of the manuscript. J.Z., W.G., Q.T., Y.M.Z., Y.C.R., J.S.W., Y.R.S., and X.B.C. revised the manuscript. All authors contributed to the final draft of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Xiangbi Chen.

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The original online version of this article was revised: The article title has been corrected.

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Zheng, S., Deng, S., Ma, C. et al. Type I methanotrophs dominated methane oxidation and assimilation in rice paddy fields by the consequence of niche differentiation. Biol Fertil Soils 60, 153–165 (2024). https://doi.org/10.1007/s00374-023-01773-x

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  • DOI: https://doi.org/10.1007/s00374-023-01773-x

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