Abstract: 

Seagrass meadows are critical regulators of coastal biogeochemical cycling, particularly through the exudation and accumulation of organic carbon that enriches their rhizosphere far beyond ambient marine levels. Microbially driven nitrification is a key process controlling nitrous oxide (N2O) emissions, yet the ecological roles of complete ammonia oxidizers (Comammox) and canonical nitrifiers in seagrass ecosystems are poorly understood. Here, we show that seagrass sediments (SS) exhibited significantly (p < 0.05) lower nitrification and N2O production rates than non-seagrass sediments, where nitrification was the dominant N2O source. We characterized the Comammox for the first time in a seagrass ecosystem, revealing that they displayed potential nitrification rates lower than ammonia-oxidizing bacteria (AOB) and ammonia-oxidizing archaea (AOA). Notably, Comammox showed the lowest N2O production rates and the net carbon dioxide (CO2) fixation flux among SS nitrifiers. Metagenome and metatranscriptome sequencing results revealed that genes for nitrification and N2O production pathways were less abundant and transcriptionally down-regulated in seagrass sediments, whereas genes related to sugar transport and metabolism were concomitantly up-regulated. These findings indicate that seagrass exudates promote a metabolic shift in the nitrifier community, up-regulate microbial carbon (C) metabolism, and enable mixotrophic utilization of organic C. This study provides a key microbial mechanism by which seagrass meadows suppress N2O emissions, highlighting the potential of microbiome engineering in seagrass restoration and conservation for climate mitigation.