The consequences of niche and physiological differentiation of archaeal and bacterial ammonia oxidisers for nitrous oxide emissions

Abstract

High and low rates of ammonium supply are believed to favour ammonia-oxidising bacteria (AOB) and archaea (AOA), respectively. Although their contrasting affinities for ammonium are suggested to account for these differences, the influence of ammonia concentration on AOA and AOB has not been tested under environmental conditions. In addition, while both AOB and AOA contribute to nitrous oxide (N2O) emissions from soil, N2O yields (N2O–N produced per NO2−–N generated from ammonia oxidation) of AOA are lower, suggesting lower emissions when AOA dominate ammonia oxidation. This study tested the hypothesis that ammonium supplied continuously at low rates is preferentially oxidised by AOA, with lower N2O yield than expected for AOB-dominated processes. Soil microcosms were supplied with water, urea or a slow release, urea-based fertiliser and 1-octyne (inhibiting only AOB) was applied to distinguish AOA and AOB activity and associated N2O production. Low ammonium supply, from mineralisation of organic matter, or of the fertiliser, led to growth, ammonia oxidation and N2O production by AOA only, with low N2O yield. High ammonium supply, from free urea within the fertiliser or after urea addition, led to growth of both groups, but AOB-dominated ammonia oxidation was associated with twofold greater N2O yield than that dominated by AOA. This study therefore demonstrates growth of both AOA and AOB at high ammonium concentration, confirms AOA dominance during low ammonium supply and suggests that slow release or organic fertilisers potentially mitigate N2O emissions through differences in niche specialisation and N2O production mechanisms in AOA and AOB.

Complete nitrification: insights into the ecophysiology of comammox Nitrospira

“…In contrast, AOA produce lower amounts of N 2 O, which is mainly generated by abiotic reactions from ammonia oxidation intermediates (Kozlowski et al 2016b; Stieglmeier et al 2014). In agreement with these data from pure culture studies, mesocosm experiments revealed an increased N 2 O yield in fertilized soil when ammonia oxidation was dominated by AOB (Hink et al 2018). In AOB, enzymatic N 2 O production is catalyzed by nitric oxide reductases (NOR) that convert NO derived from nitrite reduction (Kozlowski et al 2016a), and cytochrome P460, a periplasmic metalloenzyme shown to directly convert NH 2 OH to N 2 O under anaerobic conditions (Caranto et al 2016).…”

Genetic variation in tree leaf chemistry predicts the abundance and activity of autotrophic soil microorganisms

“…However, several studies have demonstrated that amoA gene abundance derived from qPCR varies in response to factors that also affect nitrification rates (Carey et al 2016). Several lines of Lu et al 2015, Hink et al 2018, as was the case in our study system. However, our study system differs from most of the studies included in the Carey et al (2016) metaanalysis in two fundamental ways.…”

“…This knowledge gap exists in part because, within the last decade, evidence has accumulated for a previously unknown, large, and nearly ubiquitous group of soil ammonia oxidizers in the domain Archaea (Francis et al 2005, Nicol and. More recent studies indicate that ammonia-oxidizing archaea (AOA) in the Thaumarchaeota outnumber ammonia-oxidizing bacteria (AOB) in most soils (Leininger et al 2006, Adair andSchwartz 2008), and that AOA may dominate over AOB in controlling nitrification rates in terrestrial ecosystems with low-to-moderate N availability (Carey et al 2016, Hink et al 2018). More recent studies indicate that ammonia-oxidizing archaea (AOA) in the Thaumarchaeota outnumber ammonia-oxidizing bacteria (AOB) in most soils (Leininger et al 2006, Adair andSchwartz 2008), and that AOA may dominate over AOB in controlling nitrification rates in terrestrial ecosystems with low-to-moderate N availability (Carey et al 2016, Hink et al 2018).…”

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

“…AOB growth is favored in soils fertilized by single additions of high levels of inorganic NH 3 , while AOA grow preferentially when NH 3 is produced through mineralization of organic N (Hink, Gubry-Rangin, Nicol, & Prosser, 2018;Verhamme, Prosser, & Nicol, 2011). AOB growth is favored in soils fertilized by single additions of high levels of inorganic NH 3 , while AOA grow preferentially when NH 3 is produced through mineralization of organic N (Hink, Gubry-Rangin, Nicol, & Prosser, 2018;Verhamme, Prosser, & Nicol, 2011).…”

“…To test the potential for reduction in N 2 O through use of different fertilizer strategies, a similar approach compared single addition of urea-N at high concentration and continuous low production from a slow-release urea-N fertilizer (polymethylene urea) or organic N mineralization (Hink et al, 2018). AOA-associated N 2 O emission was also determined in unfertilized soils, in which NH 3 is supplied through mineralization of organic N, and N 2 O yields were again similar to those reported for AOA cultures.…”