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

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.