Flavobacteria consume nitrous oxide produced by partial denitrifiers in coastal sediments

Abstract Nearly one-fifth of global emissions of the potent greenhouse gas nitrous oxide (N2O) originate from the ocean, particularly from nutrient-polluted coastal regions. Permeable (sandy) sediments, which cover half of the continental shelf worldwide, are potential sources of N2O due to increasing nutrient inputs from urbanization and agriculture. Yet, the microbial processes determining N2O emissions in these dynamic and unique ecosystems remain understudied. Here, we combined environmental measurements, bacterial cultivation, and genomic analyses to understand the microbes and processes controlling N2O cycling in permeable sediments from Port Phillip Bay (Australia). We established a genomic resource comprising 249 metagenome-assembled genomes and 95 new isolate genomes. Genome-based metabolic reconstructions and culture-based gas measurements revealed diverse bacteria in these sediments produce N2O through incomplete denitrification pathways. However, these bacteria co-occurred with highly abundant clade II N2O-reducing bacteria from the Flavobacteriaceae family. Kinetic profiling showed that both clade II nosZ flavobacterial isolates and whole sand communities exhibited a low apparent affinity for N2O under the tested experimental conditions, expanding the currently limited kinetic data available for N2O reducing microorganisms from coastal permeable sediments, including flavobacterial clade II N2O reducers. Collectively, these findings indicate that abundant N₂O reducing communities can substantially consume N2O within permeable sediments, thus limiting N2O accumulation despite active N2O production. Together with previous hydrodynamic models predicting low N2O release from permeable sediments, our results highlight the important role of specialized microbial communities in regulating N2O cycling under increasing nutrient pollution.