Nitrous oxide production by ammonia oxidizers: Physiological diversity, niche differentiation and potential mitigation strategies

Oxidation of ammonia to nitrite by bacteria and archaea is responsible for global emissions of nitrous oxide directly and indirectly through provision of nitrite and, after further oxidation, nitrate to denitrifiers. Their contributions to increasing N₂ O emissions are greatest in terrestrial environments, due to the dramatic and continuing increases in use of ammonia-based fertilizers, which have been driven by requirement for increased food production, but which also provide a source of energy for ammonia oxidizers (AO), leading to an imbalance in the terrestrial nitrogen cycle. Direct N₂ O production by AO results from several metabolic processes, sometimes combined with abiotic reactions. Physiological characteristics, including mechanisms for N₂ O production, vary within and between ammonia-oxidizing archaea (AOA) and bacteria (AOB) and comammox bacteria and N₂ O yield of AOB is higher than in the other two groups. There is also strong evidence for niche differentiation between AOA and AOB with respect to environmental conditions in natural and engineered environments. In particular, AOA are favored by low soil pH and AOA and AOB are, respectively, favored by low rates of ammonium supply, equivalent to application of slow-release fertilizer, or high rates of supply, equivalent to addition of high concentrations of inorganic ammonium or urea. These differences between AOA and AOB provide the potential for better fertilization strategies that could both increase fertilizer use efficiency and reduce N₂ O emissions from agricultural soils. This article reviews research on the biochemistry, physiology and ecology of AO and discusses the consequences for AO communities subjected to different agricultural practices and the ways in which this knowledge, coupled with improved methods for characterizing communities, might lead to improved fertilizer use efficiency and mitigation of N₂ O emissions.