Processes and microorganisms driving nitrous oxide production in the Benguela Upwelling System

Abstract

Upwelling systems and their associated oxygen deficient zones (ODZs) are hotspots of nitrous oxide (N2O) production in the ocean. The Benguela Upwelling System (BUS) is a highly productive region and an important, yet variable source of N2O to the atmosphere. This study examined underlying processes and microbial key players governing N2O production in the BUS during the austral winter. 15N‐tracer incubation experiments were conducted to track N2O production from NH4+ oxidation and denitrification. N2O production and consumption mechanisms over a longer temporal scale were determined through natural‐abundance isotope analyses. Metagenomics and 16S rRNA gene amplicon sequencing were used to identify potential key prokaryotes driving N2O production. Our results showed that, compared with permanent ODZs, the BUS is characterized by a higher oxidative and a lower reductive N2O production, both of which exhibit substantial spatial variability. N2O production peaked in low‐oxygen (O2) waters, with nearly equal contributions of oxidative and reductive processes, suggesting their co‐occurrence across an O2 concentration range broader than previously thought. However, the observed N2O isotope signatures implied a legacy of recent and extensive N2O reduction to N2. Metagenomic and 16S rRNA gene data identified denitrifiers belonging to Thioglobaceae and the archaeal ammonia‐oxidizers Nitrosopumilaceae among the potential key drivers of N2O production. Our study provides a comprehensive picture of N2O production in the BUS, revealing significant variability in the N‐cycling regime and underlying N2O production mechanisms, and demonstrating the value of combining direct rate measurements with more integrative approaches, such as molecular omics and natural‐abundance stable isotope tracers.