Environmental distribution, physiology and genomic adaptations of arctic ammonia-oxidizing archaea

Ammonia oxidizing archaea (AOA) are the main drivers of nitrification in Arctic soils, ecosystems that are highly sensitive to climate change-induced warming and permafrost thaw, processes that may enhance nitrogen mobilization from the soil and increase emissions of the greenhouse gas nitrous oxide (N 2 O). Compared to other terrestrial environments, the diversity of AOA in arctic soils was reported to be very low, with only two specific clades detected in most arctic ecosystems. However, to date no ammonia oxidizing model organism was available in pure culture to study the effect of climate change on the arctic nitrifier communities. AOA diversity in Arctic soils has been considered low, typically dominated by two clades. However, the lack of a pure Arctic AOA isolate has constrained mechanistic understanding of how Arctic nitrifier communities respond to warming. In this study we assessed AOA diversity across soils spanning approximately half of the circumpolar Arctic by linking 16S rRNA and amoA gene taxonomies to improve clade-level resolution. We corroborated the widespread occurrence of the AOA clades NS-zeta and NS-gamma, while a third, non-ammonia oxidizing clade of Nitrososphaerales was also found to dominate specific sites suggesting putative roles in Arctic carbon cycling. These clades exhibited distinct distribution patterns and were differentially associated with soil physicochemical parameters such as pH, water content and organic carbon content. Furthermore, after 15 years of continuous cultivation, we isolated the first psychrotolerant Arctic AOA in pure culture and obtained its closed genome. The strain, Candidatus Nitrosocosmicus arcticus Kfb actively oxidized ammonia at 4 °C, the lowest temperature reported to date, extending the temperature range of reported ammonia oxidation from 4 °C to 74 °C. However, ammonia oxidation became unstable at temperatures above 20°C during prolonged incubation, indicating potential vulnerability to episodic warming. Together, these findings expand current understanding of Arctic AOA diversity and provide a genomic and physiological framework for investigating the response of Arctic nitrification processes to ongoing climate change.