Non-denitrifier nitrous oxide reductases dominate marine biomes

Abstract

Microbial enzymes often occur as distinct variants that share the same substrate but differ in substrate affinity, sensitivity to environmental conditions, or phylogenetic ancestry. Determining where variants occur in the environment helps identify thresholds that constrain microbial cycling of key chemicals, including the greenhouse gas nitrous oxide (N2O). To understand the enzymatic basis of N2O cycling in the ocean, we mined metagenomes to characterize genes encoding bacterial nitrous oxide reductase (NosZ) catalyzing N2O reduction to N2. We examined data sets from diverse biomes but focused primarily on those from oxygen minimum zones where N2O levels are often elevated. With few exceptions, marine nosZ data sets were dominated by ‘atypical’ clade II gene variants. Atypical nosZ has been associated with low oxygen, enhanced N2O affinity, and organisms lacking enzymes for complete denitrification, i.e., non-denitrifiers. Atypical nosZ often occurred in metagenome-assembled genomes (MAGs) with nitrate or nitrite respiration genes, although MAGs with genes for complete denitrification were rare. We identified atypical nosZ in several taxa not previously associated with N2O consumption, in addition to known N2O-associated groups. The data suggest that marine environments generally select for high N2O-scavenging ability across diverse taxa and have implications for how N2O concentration may affect N2O removal rates.