Flavobacteria buffer nitrous oxide emissions from 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 revealed both clade II nosZ flavobacterial isolates and whole sand communities exhibit a low affinity for N2O, contrary to previous reports that clade II N2O reducers generally have a high substrate affinity. This indicates adaptation to the high residence times of N2O within production and consumption zones in the sands. Collectively, these N2O reducers remove most N2O produced in permeable sediments, supporting lower-than-expected coastal emissions predicted by biogeochemical models. We conclude that permeable sediments host specialised microbial communities that mitigate N2O emissions and buffer marine nitrogen cycling amid rising nutrient pollution.