Distinct N-cycling microbial communities contribute to microtopographic variation in soil N2O emissions from denitrification

Climate change is increasing the frequency and intensity of large precipitation events that flood soils and establish anoxic conditions that promote microbial denitrification, a predominant source of atmospheric nitrous oxide (N 2 O, a strong greenhouse gas). Denitrification may be favored within topographic depressions in otherwise flat fields that are prone to ponding, establishing “hotspots” of N 2 O emissions. The location of N 2 O hotspots may also depend on the distribution of soil microbial communities that are responsible for the production and consumption of N 2 O in soils. Yet, relating soil microbial community composition to N 2 O emissions remains challenging. To assess how spatial variation in soil microbial communities affects N 2 O emissions, we measured the community composition of active microorganisms using amplicon-based sequencing of cDNA generated from mRNA transcripts associated with N-cycling processes in response to experimentally flooding and draining soils in the lab. We also used stable isotope tracers to relate microbial communities to process rates. Consistent with the hypothesis that denitrifying microbial communities are not functionally redundant, we found that the diversity of microbial taxa expressing nitrite reduction genes ( nirK ) and N 2 O reduction genes (Clade I nosZ) were correlated with denitrifier-derived N 2 O emissions. Depressional soils had more diverse active N 2 O consuming communities (assessed using Clade I nosZ ) under flooded conditions, limiting net N 2 O emissions compared to upslope soils. Our results show that depressional soils maintain distinct microbial communities that likely promote higher rates of N 2 O reduction compared to upslope soils. Soil microtopography can, therefore, select for distinct microbial communities that emit different amount of N 2 O in response to large precipitation events. • Active denitrifying microbial communities were not functionally redundant. • Transcript diversity of denitrification genes was associated with N 2 O emissions. • Soils with more diverse nitrite reductase transcripts emitted more N 2 O. • Depressional soils had diverse N 2 O-reducing transcripts and emitted less N 2 O. • Microtopographic variation in denitrifier communities affects soil N 2 O emissions.