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Asgard archaea illuminate the origin of eukaryotic cellular complexity
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
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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. Vol. 541, no 7637, p. 353-+
National Category
Evolutionary Biology
Identifiers
URN: urn:nbn:se:uu:diva-319133DOI: 10.1038/nature21031ISI: 000396128800034PubMedID: 28077874OAI: oai:DiVA.org:uu-319133DiVA, id: diva2:1086520
Funder
Swedish Research Council, 2015-04959Knut and Alice Wallenberg FoundationEU, European Research Council, 310039-PUZZLE_CELL 294200-MICROENERGY 331291Swedish Foundation for Strategic Research , SSF-FFL5Available from: 2017-04-03 Created: 2017-04-03 Last updated: 2019-09-26Bibliographically approved
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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Zaremba-Niedzwiedzka, KatarzynaFernández Cáceres, EvaSaw, Jimmy Hser WahJuzokaite, LinaSpang, AnjaEttema, Thijs J. G.

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Zaremba-Niedzwiedzka, KatarzynaFernández Cáceres, EvaSaw, Jimmy Hser WahBäckström, DisaJuzokaite, LinaSpang, AnjaEttema, Thijs J. G.
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