Ammonia Oxidizing Archaea in Arctic Tundra Soils

The functioning of Arctic soil ecosystems is crucially important for the global climate. Permafrost soils contain nearly twice as much carbon as the atmosphere and it is assumed that large quantities of carbon are lost (in the form of methane and carbon dioxide) when these soils thaw. Understanding the composition and functioning of the microbial communities in arctic soils is therefore crucial in order to be able to predict their vulnerability and reactions in a changing climate. Nitrification is considered important for ecosystem functioning in the arctic, because the availability of nitrogen, the major limiting nutrient in the system, is directly dependent on it. But the major drivers of nitrification in the arctic are currently unknown. We have recently measured different gross in situ and potential nitrification rates in arctic soils that were dominated by distinct phylogenetic clades of ammonia oxidizing archaea (AOA) suggesting differences in the activities of various clades and also dominance of AOA over ammonia oxidizing bacteria (AOB) in most soils or even their exclusive presence in some. Furthermore, an enrichment of an arctic AOA of an uncharacterized lineage was obtained that is abundant in the European arctic tundra. The overall goal of this proposal is to get insight into the distribution and activity of AOA in arctic ecosystems. To achieve this we will follow two experimental paths: One involves the study of AOA in diverse arctic ecosystems and the second the characterization of Candidatus Nitrosovradea arctica, an organism representing one of the abundant lineages in arctic soils. We will study the distribution and abundance of the six major AOA clades in various arctic soils, using deep sequencing and a clade-specific quantitative PCR assay and will link these to environmental parameters and gross nitrification rates. Samples will be obtained in the frame of two international projects studying terrestrial arctic ecosystems, in which we participate (CryoCarb, ESF) or collaborate (CryoN/PAGE21, EU). The direct and indirect contribution of AOA to N2 O production and nitrification will be studied in incubation experiments with various inhibitors. Metatranscriptomics will be employed in order to investigate their activity in soils at in situ and increased temperatures. In the second part of the project, the enrichment culture of the arctic strain will be used to study growth characteristics, inhibitors, and N2 O emission. Furthermore, the genomic sequence will be determined and transcription studies will be performed in order to analyse adaptations and physiological characteristics. Both project parts will be closely interlinked. In total, we will contribute to a better understanding of arctic ammonia oxidizers including their direct or indirect influence on nitrification and N2 O production and we will contribute to a better understanding of the physiology of ammonia oxidizing archaea in general.

The Arctic is currently experiencing dramatic changes that are predicted to increase drastically as a result of climate change. With rising temperatures, permafrost areas will increasingly thaw setting free huge amounts of organic material that is stored in the underground and will become available for the degradation through microorganisms. Since an estimated 50% of the total terrestrial carbon is stored in deeper soil layers in the arctic and boreal regions, this decomposition and concomitant greenhouse gas productions are likely to cause a major positive feedback mechanism for climate change. Nitrogen is a limiting nutrient for microorganisms in most Arctic soils. Its availability is affected by the microbial process of nitrification, i.e. the oxidation of ammonia (NH3) to nitrate (NO3). Therefore it is important to characterize the organisms that drive this process, as it will affect all microbial activities involved in the biogeochemical transformations. In this project we have demonstrated that ammonia oxidizing archaea (AOA) of specific clades are the dominant organisms involved in nitrification in arctic soils, in particular in those with high organic content (peat) and that their activity is affected by temperature. We have established a broad phylogeny-based taxonomy using a gene specific to AOA to be able to map the large datasets available for these organisms and to map molecular data from arctic ecosystems of this project. By analysing peat soils from very distant areas in Northern Finland and Northern Siberia, we discovered only two to three taxa in different environments that span huge distances in the Arctic. One of these AOA species was dominating and becoming more abundant and active upon temperature increase in our experimental warming setups. The strain of the Archaeon Nitrosocosmicus arcticus that we obtained in laboratory enrichments was found to be a representative of this group. It exhibited an unexpected and still uncharacterized nitrification-independent growth-mode at lower temperatures, and switched to ammonia oxidation at higher temperatures. We conclude from our data that upon global temperature increase, nitrogen availability and in consequence also production of the greenhouse gas nitrous oxide will in arctic soils to a large extend be influenced by the activity of ammonia oxidizing archaea.