Ammonia oxidation as the engine to induce denitrification to produce N2O in alkaline agricultural soils

Abstract

Ammonia oxidation contributes to global N2O emissions both by direct production and by fueling denitrification (provision of nitrite or nitrate to denitrifiers). Urea or ammonia-based fertilizers account for approximately 70% of annual nitrogen fertilizer inputs globally. This means that the subsequent coupling processes driven by ammonia oxidation are of great significance to N2O emissions. However, for this important source of N2O production, direct evidence at the process- and microorganism- level is highly lacking, leading to that the systematic mechanism of the coupling processes and microbial activities in response to environmental changes (especially O2 changes) remains unknown. Here, we investigated ammonia oxidation, other soil N transformation processes, N2O emissions and related environmental changes (e.g., O2 consumption) and microbial activities in a calcareous upland soil in Northern China, which has a strong ammonia oxidizing rate and is a global N2O hotspot, by combining field observations, microcosm, molecular and isotope techniques. The results showed that the soil has a far (5-30 times) higher nitrification potential and gross nitrification rate than other cropland soils in the world. The strong ammonia oxidation led to rapid O2 consumption and NO2- accumulation in soil matrix, causing strong emission peaks of N2O, which was in line with the N2O yield from denitrifiers. The N2O 15N site preference and 15N labeling data further revealed a major role of nitrification-induced denitrification in high N2O emissions. A higher AOB/AOA gene abundance ratio correlated the higher nitrification potential, higher NO2- transition and higher N2O emissions. A coupling expression of nitrifying and denitrifying genes (amoA, narG, nirS, nirK, nosZ) and a significant structural alteration of the soil microbiota along with the O2 consumption driven by ammonia oxidation linked to higher N2O emissions. All the evidence points to ammonia oxidation-linked denitrification being the major process generating N2O. In consequence, reducing N surplus, slowing down nitrification rate using nitrification inhibitors, and avoiding high ammonium microzones using slow-release or organic fertilizers are main measures to reduce N2O emissions per unit of urea or NH4+-based N input in intensively managed alkaline soils globally.