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Evolutionary history and ecological adaptations of ammonia oxidizing Thaumarchaeota.

Periodic Reporting for period 1 - THAUMECOPHYL (Evolutionary history and ecological adaptations of ammonia oxidizing Thaumarchaeota.)

Reporting period: 2016-04-01 to 2018-03-31

Ammonia oxidizing archaea (AOA), a clade of the Thaumarchaeota phylum, diversified in a variety of marine and terrestrial environments. Due to their abundance and metabolic activities, AOA are deemed major players in the global cycle of nitrogen and carbon (N-cycle and C-cycle). They also produce greenhouse gases. Despite their ecological importance, the nature and origin of ammonia oxidizing metabolism and the reasons for the ecological success of these archaea are still unknown. This project aimed at performing the first comprehensive evolutionary and comparative genomic analysis of Thaumarchaeota to identify crucial metabolic and genomic features. Metagenomic data were produced in the laboratory and gave access to genomes of crucial taxa for the understanding of AOA evolution. We could access the genome content of ammonia-oxidizing archaea from lineages that were never sequenced before. These genomes were extracted and analysed together with AOA genomes available in the public databanks with a phylogenomic approach to reconstruct the phylogenetic tree of the AOA species, and understand their genome evolution and adaptation to different environments. We could thus clarify some aspects of the highly conserved nitrogen and carbon metabolism in archaea, which is crucial to complete our understanding of the functioning, and of the role of these organisms in global biogeochemical processes and climate change.
We assembled genomes from lineages of AOA not sequenced so far, thus enriching considerably the diversity of the organisms to be included in our evolutionary analysis. To do that, we used metagenomic approaches and obtained sequencing data from cultures in the lab, or from environmental samples collected by our collaborators. We obtained six genome bins. This new genomic dataset was completed with publicly available genomes, plus another genome previously obtained in the host lab.
We constructed a species tree for the genomes gathered based on the phylogenetic analysis of several dozens of shared genes. We then performed an analysis of the genome evolution of AOA in the context of their environmental distribution. This resulted in the proposition of adaptive features that could explain the evolutionary success and widespread distribution of AOA in many environments.

Results obtained during this project were/will be disseminated in publications and conferences:
- An article was published in the journal Proceedings of the National Academy of Sciences, USA (Kerou et al. 2016).
- Two articles in scientific journals are currently being drafted.
- A poster was presented at the “Molecular Biology of Archaea 5” conference in London (July 2016).
- Invitation for plenary talk at the ICoN5 conference in July 2017 (5th International Conference on Nitrification and Related Processes, Vienna, Austria).
- The data generated during this project will be released publicly in dedicated databases upon the publication of the corresponding results.
The sequencing effort made in this project resulted in a considerable expansion of available AOA genomes, in particular from deeply branching lineages that were not represented before. This is a significant progress in the field. The availability of these new genomes together with public ones, helped us to better understand the evolutionary success of AOA in very diverse habitats, and the functioning of ammonia oxidation in archaea, one of the most abundant groups of microorganisms on Earth. We also showed that coupling metagenomic, phylogenomic and comparative genomic approaches can help to address long-standing questions in the field, as e.g. the metabolic processes within global biogeochemical cycles. Altogether, this will lead to a better characterization of the role of AOA in the N-cycle and C-cycle, only a dozen years after the 1st recognition of the existence of AOA.
scanning electron microscopic picture of Nitrososphaera viennensis, copyright: Christa Schleper
an overview of the project