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Expanded diversity of Asgard archaea points to Idunnarchaeota as closest relatives of eukaryotes
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology. Laboratoire Écologie, Systématique, Évolution, CNRS, Université Paris-Sud, Université Paris-Saclay, AgroParisTech.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology. Wageningen University and Research, Laboratory of Microbiology.ORCID iD: 0000-0003-2890-2631
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology. Wageningen University and Research, Laboratory of Microbiology.
(University of Texas Austin, Marine Science Institute, Department of Marine Science)
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(English)Manuscript (preprint) (Other academic)
National Category
Natural Sciences
Identifiers
URN: urn:nbn:se:uu:diva-393590OAI: oai:DiVA.org:uu-393590DiVA, id: diva2:1354691
Available from: 2019-09-25 Created: 2019-09-25 Last updated: 2019-09-26
In thesis
1. Genomic and evolutionary exploration of Asgard archaea
Open this publication in new window or tab >>Genomic and evolutionary exploration of Asgard archaea
2019 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Current evolutionary theories postulate that eukaryotes emerged from the symbiosis of an archaeal host with, at least, one bacterial symbiont. However, our limited grasp of microbial diversity hampers insights into the features of the prokaryotic ancestors of eukaryotes. This thesis focuses on the study of a group of uncultured archaea to better understand both existing archaeal diversity and the origin of eukaryotes.

In a first study, we used short-read metagenomic approaches to obtain eight genomes of Lokiarchaeum relatives. Using these data we described the Asgard superphylum, comprised of at least four different phyla: Lokiarchaeota, Odinarchaeota, Thorarchaeota and Heimdallarchaoeta. Phylogenetic analyses suggested that eukaryotes affiliate with the Asgard group, albeit the exact position of eukaryotes with respect to Asgard archaea members remained inconclusive. Comparative genomics showed that Asgard archaea genomes encoded homologs of numerous eukaryotic signature proteins (ESPs), which had never been observed in Archaea before. Among these, there were several components of proteins involved in vesicle formation and membrane remodelling.

In a second study, we used similar approaches to uncover additional members of the Asgard superphylum. Based on genome-centric metagenomics we recovered 69 new genomes from which we identified five additional candidate phyla: Freyarchaeota, Baldrarchaeota, Gefionarchaeota, Friggarchaeota and Idunnarchaeota. In this expanded dataset we could detect additional homologs for unreported ESPs. Updated phylogenies showed support for a scenario in which eukaryotes emerged from within Asgard archaea.

We further took advantage of the increased Asgard diversity to delimit the gene content of the last common archaeal ancestor of eukaryotes using ancestral reconstruction analyses. The results suggest that the archaeal host cell who gave rise to eukaryotes already contained many of the genes associated with eukaryotic cellular complexity. Based on these analyses, we discussed the metabolic capabilities of the archaeal ancestor of eukaryotes.

Finally, we reconstructed several nearly complete Lokiarchaeota genomes, one of them in only three contigs, using both short- and long-read metagenomics. These analyses indicate that long-read metagenomics is a promising approach to obtain highly complete and contiguous genomes directly from environmental samples, even from complex populations in the presence of microdiversity and low abundant members. This study further supports that the presence of ESPs in Asgard genomes is not the result of assembly and binning artefacts. 

In conclusion, this thesis highlights the value of using culture-independent approaches together with phylogenomics and comparative genomics to improve our understanding of microbial diversity and to shed light into relevant evolutionary questions.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2019. p. 88
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1861
Keywords
archaea, Asgard, eukaryogenesis, metagenomics, genome binning, phylogenetics, phylogenomics, comparative genomics, gene tree-species tree reconciliation, ancestral reconstruction, long-read metagenomics
National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-393710 (URN)978-91-513-0761-9 (ISBN)
Public defence
2019-11-14, B22, Biomedical Center (BMC), Husargatan 3, Uppsala, 09:15 (English)
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Supervisors
Available from: 2019-10-24 Created: 2019-09-26 Last updated: 2019-11-12

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