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

Rice paddies contribute substantially to atmospheric methane (CH ₄ ) and these emissions are expected to increase as the need to feed the human population grows. Here, we show that two independent rice genotypes overexpressing genes for PLANT PEPTIDES CONTAINING SULFATED TYROSINE ( PSY ) reduced cumulative CH ₄ emissions by 38% (PSY1) and 58% (PSY2) over the growth period compared with controls. Genome-resolved metatranscriptomic data from rhizosphere soils reveal lower ratios of gene activities for CH ₄ production versus consumption, decrease in activity of H ₂ -producing genes, and increase in bacterial H ₂ oxidation pathways in the PSY genotypes. Metabolic modeling using metagenomic and metabolomic data predicts elevated levels of H ₂ oxidation and suppressed H ₂ production in the PSY rhizosphere. The H ₂ -oxidizing bacteria have more genes for utilization of gluconeogenic acids than H ₂ -producing counterparts, and their activities were likely stimulated by the observed enrichment of gluconeogenic acids (mostly amino acids) in PSY root exudates. Together these results suggest that decreased CH ₄ emission is due to the reduction of H ₂ available for hydrogenotrophic methanogenesis. The combination of rice phenotypic characterization, microbiome multi-omic analysis, and metabolic modeling described here provides a powerful strategy to discover the mechanisms by which specific plant genotypes can alter biogeochemical cycles to reduce CH ₄ emissions.