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  • 1.
    Caceres, Eva F.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology.
    Genomic and evolutionary exploration of Asgard archaea2019Doctoral 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.

    List of papers
    1. Asgard archaea illuminate the origin of eukaryotic cellular complexity
    Open this publication in new window or tab >>Asgard archaea illuminate the origin of eukaryotic cellular complexity
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    2017 (English)In: Nature, ISSN 0028-0836, E-ISSN 1476-4687, Vol. 541, no 7637, p. 353-+Article in journal (Refereed) Published
    Abstract [en]

    The origin and cellular complexity of eukaryotes represent a major enigma in biology. Current data support scenarios in which an archaeal host cell and an alphaproteobacterial (mitochondrial) endosymbiont merged together, resulting in the first eukaryotic cell. The host cell is related to Lokiarchaeota, an archaeal phylum with many eukaryotic features. The emergence of the structural complexity that characterizes eukaryotic cells remains unclear. Here we describe the 'Asgard' superphylum, a group of uncultivated archaea that, as well as Lokiarchaeota, includes Thor-, Odin- and Heimdallarchaeota. Asgard archaea affiliate with eukaryotes in phylogenomic analyses, and their genomes are enriched for proteins formerly considered specific to eukaryotes. Notably, thorarchaeal genomes encode several homologues of eukaryotic membrane-trafficking machinery components, including Sec23/24 and TRAPP domains. Furthermore, we identify thorarchaeal proteins with similar features to eukaryotic coat proteins involved in vesicle biogenesis. Our results expand the known repertoire of 'eukaryote-specific' proteins in Archaea, indicating that the archaeal host cell already contained many key components that govern eukaryotic cellular complexity.

    Place, publisher, year, edition, pages
    NATURE PUBLISHING GROUP, 2017
    National Category
    Evolutionary Biology
    Identifiers
    urn:nbn:se:uu:diva-319133 (URN)10.1038/nature21031 (DOI)000396128800034 ()28077874 (PubMedID)
    Funder
    Swedish Research Council, 2015-04959Knut and Alice Wallenberg FoundationEU, European Research Council, 310039-PUZZLE_CELL 294200-MICROENERGY 331291Swedish Foundation for Strategic Research , SSF-FFL5
    Available from: 2017-04-03 Created: 2017-04-03 Last updated: 2019-09-26Bibliographically approved
    2. Expanded diversity of Asgard archaea points to Idunnarchaeota as closest relatives of eukaryotes
    Open this publication in new window or tab >>Expanded diversity of Asgard archaea points to Idunnarchaeota as closest relatives of eukaryotes
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    (English)Manuscript (preprint) (Other academic)
    National Category
    Natural Sciences
    Identifiers
    urn:nbn:se:uu:diva-393590 (URN)
    Available from: 2019-09-25 Created: 2019-09-25 Last updated: 2019-09-26
    3. Ancestral reconstruction of Asgard archaea provides insight into the gene content of the archaeal ancestor of eukaryotes
    Open this publication in new window or tab >>Ancestral reconstruction of Asgard archaea provides insight into the gene content of the archaeal ancestor of eukaryotes
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    (English)Manuscript (preprint) (Other academic)
    National Category
    Natural Sciences
    Identifiers
    urn:nbn:se:uu:diva-393589 (URN)
    Available from: 2019-09-25 Created: 2019-09-25 Last updated: 2019-09-26
    4. Reconstruction of a near-complete Lokiarchaeota genome using long- and short-read metagenomics of complex sediment samples
    Open this publication in new window or tab >>Reconstruction of a near-complete Lokiarchaeota genome using long- and short-read metagenomics of complex sediment samples
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    (English)Manuscript (preprint) (Other academic)
    National Category
    Natural Sciences
    Identifiers
    urn:nbn:se:uu:diva-393111 (URN)
    Available from: 2019-09-25 Created: 2019-09-25 Last updated: 2019-09-26
  • 2.
    Caceres, Eva F.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology. Wageningen University and Research, Department of Microbiology.
    Lewis, William H.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology. Wageningen University and Research, Department of Microbiology.
    Martin, Tom
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology.
    Homa, Felix
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology. Wageningen University and Research, Department of Microbiology.
    Schramm, Andreas
    Aarhus University, Section for Microbiology and Center for Geomicrobiology, Department of Bioscience.
    Kjeldsen, Kasper U.
    Aarhus University, Section for Microbiology and Center for Geomicrobiology, Department of Bioscience.
    Ettema, Thijs J. G.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology. Wageningen University and Research, Department of Microbiology.
    Reconstruction of a near-complete Lokiarchaeota genome using long- and short-read metagenomics of complex sediment samplesManuscript (preprint) (Other academic)
  • 3.
    Eme, Laura
    et al.
    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.
    Caceres, Eva F.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology. Wageningen University and Research, Laboratory of Microbiology.
    Tamarit, Daniel
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology. Wageningen University and Research, Laboratory of Microbiology.
    Seitz, Kiley W.
    Dombrowski, Nina
    Royal Netherlands Institute for Sea Research, Department of Marine Microbiology and Biogeochemistry.
    Homa, Felix
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology.
    Saw, Jimmy
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology. George Washington University.
    Lombard, Jonathan
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology.
    Li, Wen-Jun
    Hua, Zheng-Shuang
    Chen, Lin-Xing
    Banfield, Jillian
    Reysenbach, Anna-Louise
    Takuro, Nunoura
    Stott, Matthew B.
    Schramm, Andreas
    Kjeldsen, Kasper U.
    Baker, Brett J.
    Ettema, Thijs J. G.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology. Wageningen University and Research, Laboratory of Microbiology.
    Expanded diversity of Asgard archaea points to Idunnarchaeota as closest relatives of eukaryotesManuscript (preprint) (Other academic)
  • 4.
    Fernandez Caceres, Eva
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology. Wageningen University and Research, Laboratory of Microbiology.
    Eme, Laura
    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.
    De Anda, Valerie
    Baker, Brett J.
    Ettema, Thijs J. G.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology. Wageningen University and Research, Laboratory of Microbiology.
    Ancestral reconstruction of Asgard archaea provides insight into the gene content of the archaeal ancestor of eukaryotesManuscript (preprint) (Other academic)
1 - 4 of 4
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