Flavobacteria buffer nitrous oxide emissions from partial denitrifiers in coastal sediments

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Abstract

Nearly one-fifth of global emissions of the potent greenhouse gas nitrous oxide (N 2 O) 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 N 2 O due to increasing nutrient inputs from urbanization and agriculture. Yet, the microbial processes determining N 2 O 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 N 2 O 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 N 2 O through incomplete denitrification pathways. However, these bacteria co-occurred with highly abundant clade II N 2 O-reducing bacteria from the Flavobacteriaceae family. Kinetic profiling revealed both clade II nosZ flavobacterial isolates and whole sand communities exhibit a low affinity for N 2 O, contrary to previous reports that clade II N 2 O reducers generally have a high substrate affinity. This indicates adaptation to the high residence times of N 2 O within production and consumption zones in the sands. Collectively, these N 2 O reducers remove most N 2 O 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 N 2 O emissions and buffer marine nitrogen cycling amid rising nutrient pollution.

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