Abstract

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.

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Acknowledgements

We thank L. Guy, S. L. Jørgensen, T. Williams, N. Lartillot, B. Quang Minh and J. Dacks for useful advice and discussions. We are grateful to D. R. Colman and C. Takacs-Vesbach for collecting the YNP sediment samples under permit #YELL-2010-SCI-5344, to the Japan Agency for Marine-Earth Science & Technology (JAMSTEC) for taking sediment samples from the Taketomi shallow submarine hydrothermal system, and to the Ngāti Tahu Ngāti Whaoa Runanga Trust for their enthusiasm for our research, and assistance in access and sampling of the Ngatamariki geothermal features. We acknowledge the Yellowstone Center for Resources for their assistance and for facilitating this research. We thank A. Simpson for suggesting the name ‘Heimdallarchaeota’. Sequencing of the White Oak River and Colorado River sediment metagenomes was conducted at the Joint Genome Institute, a US Department of Energy Office of Science User Facility, via the Community Science Program. The remaining metagenomes were sequenced at the National Genomics Infrastructure sequencing platforms at the Science for Life Laboratory at Uppsala University, a national infrastructure supported by the Swedish Research Council (VR-RFI) and the Knut and Alice Wallenberg Foundation. We thank the Uppsala Multidisciplinary Center for Advanced Computational Science (UPPMAX) at Uppsala University and the Swedish National Infrastructure for Computing (SNIC) at the PDC Center for High-Performance Computing for providing computational resources. This work was supported by grants of the European Research Council (ERC Starting grant 310039-PUZZLE_CELL), the Swedish Foundation for Strategic Research (SSF-FFL5) and the Swedish Research Council (VR grant 2015-04959) to T.J.G.E., by Marie Curie IIF (331291 to J.H.S.) and IEF (625521 to A.S.) grants by the European Union to the Ettema laboratory, by grants to Bo Barker Jørgensen (Aarhus University, Denmark) from the European Research Council (ERC Advanced Grant 294200-MICROENERGY) and the Danish National Research Foundation (DNRF104) to support the Center for Geomicrobiology at Aarhus University, and by the US Department of Energy (Sustainable Systems Scientific Focus Area grant DE-AC02-05CH11231 to J.F.B.).

Author information

Author notes

    • Emmelien Vancaester

    Present address: Department of Plant Systems Biology, VIB and Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 927, B-9052 Ghent, Belgium.

    • Katarzyna Zaremba-Niedzwiedzka
    • , Eva F. Caceres
    •  & Jimmy H. Saw

    These authors contributed equally to this work.

Affiliations

  1. Department of Cell and Molecular Biology, Science for Life Laboratory, Uppsala University, SE-75123 Uppsala, Sweden

    • Katarzyna Zaremba-Niedzwiedzka
    • , Eva F. Caceres
    • , Jimmy H. Saw
    • , Disa Bäckström
    • , Lina Juzokaite
    • , Emmelien Vancaester
    • , Anja Spang
    •  & Thijs J. G. Ettema
  2. Department of Marine Science, University of Texas-Austin, Marine Science Institute, Port Aransas, Texas 78373, USA

    • Kiley W. Seitz
    •  & Brett J. Baker
  3. Department of Earth and Planetary Sciences, and Department of Environmental Science, Policy, and Management, University of California, Berkeley, California, USA

    • Karthik Anantharaman
    •  & Jillian F. Banfield
  4. Section for Microbiology and Center for Geomicrobiology, Department of Bioscience, Aarhus University, DK-8000 Aarhus, Denmark

    • Piotr Starnawski
    • , Kasper U. Kjeldsen
    •  & Andreas Schramm
  5. GNS Science, Extremophile Research Group, Private Bag 2000, Taupō 3352, New Zealand

    • Matthew B. Stott
  6. Research and Development Center for Marine Biosciences, Japan Agency for Marine-Earth Science and Technology, Yokosuka 237-0061, Japan

    • Takuro Nunoura

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Contributions

T.J.G.E. conceived the study. A.Sc., P.S., K.U.K., M.B.S. and T.N. took/provided environmental samples. L.J. purified environmental DNA and prepared sequencing libraries. K.Z.-N., E.F.C, J.H.S., K.A., J.F.B, K.W.S., B.J.B. and E.V. performed metagenomic sequence assemblies and metagenomic binning analyses. K.Z.-N., E.F.C., J.H.S., A.Sp. and T.J.G.E. analysed genomic data and performed phylogenetic analyses. A.Sp., D.B., E.F.C. and T.J.G.E analysed genomic signatures. K.Z.-N., E.F.C., J.H.S., A.Sp. and T.J.G.E. wrote, and all authors edited and approved, the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Thijs J. G. Ettema.

Reviewer Information Nature thanks J. Gilbert, E. Koonin, A. Roger and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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    Supplementary Information

    This file contains Supplementary Methods, Supplementary Discussions 1-4, Supplementary References, Supplementary Tables 1-14 and Supplementary Figures 1-5, which provide more details into annotations, applied methods and phylogenetic analyses.

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