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.
Highlights
High latitude ecosystems are warming faster than those at lower latitudes and soils in these regions are expected to exhibit higher respiration rates and overall turnover of carbon and nitrogen under rising temperatures (IPCC, 2013)
Two initial enrichment cultures of Ammonia-oxidizing archaea (AOA) were obtained from arctic mineral soils from a frost boil in a peatland and from upland moss tundra in Svalbard, by screening ammonia oxidation activity in approximately 100 initial cultures inoculated with diverse arctic soils, as described by Alves et al (2013)
After ∼3 years of continuous cultivation, these ammonia-oxidizing cultures were shown to contain only a single AOA phylotype related to fosmid clone 29i4 (Quaiser et al, 2002), based on amoA and 16S rRNA genes (Alves et al, 2013), which is represented by the candidate genus
Summary
High latitude ecosystems are warming faster than those at lower latitudes and soils in these regions are expected to exhibit higher respiration rates and overall turnover of carbon and nitrogen under rising temperatures (IPCC, 2013). Arctic and boreal soils store large amounts of organic matter, and considerable carbon losses as carbon dioxide (CO2) emissions have been observed in these ecosystems under a temperature increase of just 1◦C (Crowther et al, 2016) Such climate feedbacks are expected to increase greatly due to permafrost thawing, higher rates of soil organic matter decomposition and consequent higher nutrient bioavailability ( of nitrogen), eventually leading to higher greenhouse gas emissions, including CO2, methane, and nitrous oxide (N2O) (e.g., Dorrepaal et al, 2009; Wild et al, 2014; Capek et al, 2015; Voigt et al, 2017). AOA are typically the dominant and often the only detectable ammonia oxidizers in extreme and oligotrophic environments (Hatzenpichler, 2012; Stahl and de la Torre, 2012; Alves et al, 2018), they are abundant in highly organic and nutrient-rich environments, such as fertilized soils, peatlands and wastewater treatment systems (Stopnisek et al, 2010; Limpiyakorn et al, 2013; Sauder et al, 2017; Alves et al, 2018)
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