Ammonia Oxidation by the Arctic Terrestrial Thaumarchaeote Candidatus Nitrosocosmicus arcticus Is Stimulated by Increasing Temperatures

Abstract

Climate change is causing arctic regions to warm disproportionally faster than those at lower latitudes, leading to alterations in carbon and nitrogen cycling, and potentially higher greenhouse gas emissions. It is thus increasingly important to better characterize the microorganisms driving arctic biogeochemical processes and their potential responses to changing conditions. Here, we describe a novel thaumarchaeon enriched from an arctic soil, Candidatus Nitrosocosmicus arcticus strain Kfb, which has been maintained for seven years in stable laboratory enrichment cultures as an aerobic ammonia oxidizer, with ammonium or urea as substrates. Genomic analyses show that this organism harbors all genes involved in ammonia oxidation and in carbon fixation via the 3-hydroxypropionate/4-hydroxybutyrate cycle, characteristic of all AOA, as well as the capability for urea utilization and potentially also for heterotrophic metabolism, similar to other AOA. Ca . N. arcticus oxidizes ammonia optimally between 20 and 28°C, well above average temperatures in its native high arctic environment (−13–4°C). Ammonia oxidation rates were nevertheless much lower than those of most cultivated mesophilic AOA (20–45°C). Intriguingly, we repeatedly observed apparent faster growth rates (based on marker gene counts) at lower temperatures (4–8°C) but without detectable nitrite production. Together with potential metabolisms predicted from its genome content, these observations indicate that Ca . N. arcticus is not a strict chemolithotrophic ammonia oxidizer and add to cumulating evidence for a greater metabolic and physiological versatility of AOA. The physiology of Ca . N. arcticus suggests that increasing temperatures might drastically affect nitrification in arctic soils by stimulating archaeal ammonia oxidation.

Gene duplication drives genome expansion in a major lineage of Thaumarchaeota

“…The class Nitrososphaeria represent the most environmentally widespread archaea on the planet, despite their apparent specific metabolic niche for ammonia oxidation. The present work confirmed that core metabolic capacities are maintained for ammonia oxidation and autotrophy but, importantly, revealed that their diversification is linked to acquisition of many different traits to survive in diverse environments, explaining the previously suggested vast protein family differences required for environment-specific adaptation 17 , 29 , 39 , 43 . The transition of Thaumarchaeota to an autotrophic ammonia-oxidising lifestyle has been proposed to result from a large lateral gene transfer event in the last common ancestor of AOA 12 .…”

“…These transport and synthesis genes were previously detected in three Ca . Nitrosocosmicus strains 39 and appear to be also present in several of the newly represented Nitrososphaerales lineages (Fig. 2 ).…”

Nitrogen Isotope Fractionation During Archaeal Ammonia Oxidation: Coupled Estimates From Measurements of Residual Ammonium and Accumulated Nitrite

“…Moreover, it should be noted that some ammonia oxidizers use distinct pathways of NH 4 + assimilation, even among just AOA, which may contribute to different kinetic isotope effects. For instance, some members of the AOA genus Candidatus Nitrosocosmicus appear to assimilate NH 4 + via glutamate synthase (GOGAT), whereas all other known AOA use the glutamate dehydrogenase (GDH) pathway (Alves et al, 2019).…”

Comparison of Novel and Established Nitrification Inhibitors Relevant to Agriculture on Soil Ammonia- and Nitrite-Oxidizing Isolates

“…This production of EPS is a feature shared by all Ca . Nitrosocosmicus isolates ( Jung et al, 2016 ; Lehtovirta-Morley et al, 2016 ; Sauder et al, 2017 ; Alves et al, 2019 ; Liu et al, 2019 ) and has been reported as a protection mechanism of AOB against NIs ( Powell and Prosser, 1991 ).…”