Increased methane production associated with community shifts towards Methanocella in paddy soils with the presence of nanoplastics

Planetary plastic pollution poses a major threat to ecosystems and human health in the Anthropocene, yet its impact on biogeochemical cycling remains poorly understood. Waterlogged rice paddies are globally important sources of CH4. Given the widespread use of plastic mulching in soils, it is urgent to unravel whether low-density polyethylene (LDPE) will affect the methanogenic community in flooded paddy soils. Here, we employed a combination of process measurements, short-chain and long-chain fatty acid (SCFAs and LCFAs) profiling, Fourier-transform ion cyclotron resonance mass spectrometry, quantitative PCR, metagenomics, and mRNA profiling to investigate the impact of LDPE nanoplastics (NPs) on dissolved organic carbon (DOC) and CH4 production in both black and red paddy soils under anoxic incubation over a 160-day period. Despite significant differences in microbiome composition between the two soil types, both exhibited similar results to NPs exposure. NPs induced a change in DOC content and CH4 production up to 1.8-fold and 10.1-fold, respectively. The proportion of labile dissolved organic matter decreased, while its recalcitrance increased. Genes associated with the degradation of complex carbohydrates and aromatic carbon were significantly enriched. The elevated CH4 production was significantly correlated to increases in both the PCR-quantified mcrA gene copy numbers and the metagenomic methanogen-to-bacteria abundance ratio. Notably, the latter was linked to an enrichment of the hydrogenotrophic methanogenesis pathway. Among 391 metagenome-assembled genomes (MAGs), the abundance of several Syntrophomonas and Methanocella MAGs increased concomitantly, suggesting that the NPs treatments stimulated the syntrophic oxidation of fatty acids. mRNA profiling further identified Methanosarcinaceae and Methanocellaceae to be the key players in the NPs-induced CH4 production. The specific enrichment of Syntrophomonas and Methanocella indicates that LDPE NPs stimulate the syntrophic oxidation of LCFAs and SCFAs, with Methanocella acting as the hydrogenotrophic methanogen partner. Our findings enhance the understanding of how LDPE NPs affect the methanogenic community in waterlogged paddy soils. Given the importance of this ecosystem, our results are crucial for elucidating the mechanisms that govern carbon fluxes, which are highly relevant to global climate change.