Microbial mechanisms and ecosystem flux estimation for aerobic NOy emissions from deciduous forest soils

Abstract

Reactive nitrogen oxides (NO_y; NO_y = NO + NO₂ + HONO) decrease air quality and impact radiative forcing, yet the factors responsible for their emission from nonpoint sources (i.e., soils) remain poorly understood. We investigated the factors that control the production of aerobic NO_y in forest soils using molecular techniques, process-based assays, and inhibitor experiments. We subsequently used these data to identify hotspots for gas emissions across forests of the eastern United States. Here, we show that nitrogen oxide soil emissions are mediated by microbial community structure (e.g., ammonium oxidizer abundances), soil chemical characteristics (pH and C:N), and nitrogen (N) transformation rates (net nitrification). We find that, while nitrification rates are controlled primarily by chemoautotrophic ammonia-oxidizing archaea (AOA), the production of NO_y is mediated in large part by chemoautotrophic ammonia-oxidizing bacteria (AOB). Variation in nitrification rates and nitrogen oxide emissions tracked variation in forest communities, as stands dominated by arbuscular mycorrhizal (AM) trees had greater N transformation rates and NO_y fluxes than stands dominated by ectomycorrhizal (ECM) trees. Given mapped distributions of AM and ECM trees from 78,000 forest inventory plots, we estimate that broadleaf forests of the Midwest and the eastern United States as well as the Mississippi River corridor may be considered hotspots of biogenic NO_y emissions. Together, our results greatly improve our understanding of NO_y fluxes from forests, which should lead to improved predictions about the atmospheric consequences of tree species shifts owing to land management and climate change.

Keywords: deciduous forests; nitric oxide; nitrification; nitrous acid; soil emissions.

Fig. 1.

Overview of soil N-cycle processes showing major transformations and products. Color shading indicates process grouping: gray (nitrification), red (nitrifier denitrification), and blue (denitrification).

Fig. 2.

Rates of total, 1-octyne, and acetylene net nitrification. Inset indicates the NH₃-oxidizer effect on nitrification rates for AM and ECM soil, which for AOB, is calculated as the difference in nitrification rate between the no inhibitor and 1-octyne treatments. For AOA, NH₃-oxidizer effect is calculated as the differences between nitrification rate under 1-octyne and acetylene additions (n = 8).

Fig. 3.

Quantification of AOB and AOA amoA based on copy number per gram of soil (n = 8). Inset indicates the ratio of AOA to AOB.

Fig. 4.

Mean fluxes of NO, NO₂, and HONO from hours 14, 15, and 16 of their respective incubation in response to inhibitor additions (n = 8). Inset indicates the NH₃-oxidizer effect on NO_y fluxes, where the AOB effect is the difference in nitrification rate between the no inhibitor and 1-octyne treatments and the AOA effect is the difference between nitrification rate under 1-octyne and acetylene additions. NH₃-oxidizer effect is based on the combined effect of all NO_y gases (NO, NO₂, and HONO).

Fig. 5.

Proposed mechanism for AOA- and AOB-dependent NO_y production. Arrow width symbolizes the amount of substrate being transformed relative to starting substrate (i.e., NH₃). Enzymes are listed above arrows. Cu “P460,” putative copper-containing enzyme; E, unknown nitric oxide oxidoreductase; HAO, hydroxylamine oxidoreductase; NC, nitrosocyanin; NIR, nitrite reductase; NOR, nitric oxide reductase.

Fig. 6.

Map of estimated NO_y flux based on mycorrhizal association for forest inventory analysis data points throughout the eastern United States. Areas are segmented into ecological provinces of the eastern United States.