Reduced methane emissions in transgenic rice genotypes are associated with altered rhizosphere microbial hydrogen cycling

Rice paddies significantly contribute to atmospheric methane (CH₄). Here, we show that two independent rice genotypes overexpressing genes for PLANT PEPTIDES CONTAINING SULFATED TYROSINE (PSY) reduce cumulative CH₄ emissions by 38% (PSY1) and 58% (PSY2) over 70 days of growth compared with controls. Genome-resolved metatranscriptomic data from PSY rhizosphere soils reveal lower ratios of gene activities for (mostly hydrogenotrophic) CH₄ production versus consumption, decreased activity of H₂-producing genes, and increased activity of bacterial H₂ oxidation pathways. Metabolic modeling using metagenomic and metabolomic data predicts elevated H₂ oxidation and suppressed H₂ production in the PSY rhizosphere. Assembled genomes of rhizosphere H₂-oxidizing bacteria are enriched in genes utilizing gluconeogenic acids compared with H₂-producing counterparts, and their activities are likely stimulated by elevated levels of gluconeogenic acids, primarily amino acids, in PSY root exudates. Overall, our study indicates that decreased CH₄ emissions are due to a lower amount of H₂ available for hydrogenotrophic methanogenesis and provides a powerful strategy to mitigate CH₄ emissions from increasingly widespread rice cultivation.