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Asgard archaea illuminate the origin of eukaryotic cellular complexity

Nature volume 541, pages 353–358 (2017)Cite this article

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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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Figure 1: Identification and phylogenomics of Asgard archaea.
Figure 2: Vesicular trafficking components in Asgard archaea.

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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.).

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Author notes

  1. Emmelien Vancaester

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

  2. Katarzyna Zaremba-Niedzwiedzka, Eva F. Caceres and Jimmy H. Saw: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Cell and Molecular Biology, Science for Life Laboratory, Uppsala University, Uppsala, SE-75123, 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. Department of Bioscience, Section for Microbiology and Center for Geomicrobiology, Aarhus University, Aarhus, DK-8000, 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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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.

Corresponding author

Correspondence to Thijs J. G. Ettema.

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The authors declare no competing financial interests.

Additional information

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.

Extended data figures and tables

Extended Data Figure 1 Sample origin, metagenomics workflow and global distribution of Asgard archaea.

a, World map showing the sampling locations of the current study. Abbreviations of the sites mentioned are as follows: LC, Loki’s Castle; CR, Colorado River aquifer (USA); LCB, Lower Culex Basin (Yellowstone National Park, USA); WOR, White Oak River (USA); AB, Aarhus Bay (Denmark); RP, Radiata Pool (New Zealand); and TIV, Taketomi Island Vent (Japan). The world map was drawn using the Matplotlib Basemap Toolkit (http://matplotlib.org/basemap/). b, Simplified schematic overview of the metagenomics approach that was used to obtain Asgard genomes. Software used during the assembly and binning processes are shown in grey. c, Normalized distribution of major Asgard archaeal groups across various environments based on 16S rRNA gene survey datasets. Numbers on the right side of the bar graph represent total number of identified sequences.

Extended Data Figure 2 Bayesian phylogenetic inference of 48 concatenated marker genes.

The tree was inferred using CAT + GTR model and rooted with Bacteria, showing high support for the phylogenetic affiliation between Asgard archaea and eukaryotes (support value in red). Numbers at branches represent posterior probabilities and scale bar indicates the number of substitutions per site.

Extended Data Figure 3 Asgard genomes encode an expanded GTPase repertoire.

Graph showing small Ras and Arf-type GTPases (containing any of the following domains: IPR006762, IPR024156, IPR006689, IPR006687, IPR001806, IPR003579, IPR020849, IPR003578, IPR021181, IPR031260, IPR002041, IPR019009) per Asgard genomic bin normalized to the total amount of proteins predicted per genome and compared with selected eukaryotic, archaeal and bacterial taxa. Numbers refer to the total amount of GTPases per genome.

Extended Data Figure 4 Phylogenetic analysis of oligosaccharyl-transferase-complex-related proteins.

a, Bayesian inference of STT3-domain proteins (598 aligned amino acid positions) present in all three domains of life. This phylogenetic tree was rooted with bacterial sequences. Numbers at branches refer to Bayesian and non-parametric RAxML bootstrap values, respectively. b, Unrooted maximum likelihood phylogenetic analysis of ribophorin domain proteins (357 aligned amino acid positions) including all prokaryotic homologues identified so far. Numbers at branches show slow, non-parametric maximum-likelihood bootstrap support values. Scale bars indicate the number of substitutions per site.

Extended Data Figure 5 Genomic conservation links ESCRT and ubiquitin modifier systems.

Schematic overview of ubiquitin and ESCRT gene clusters identified in Asgard genomes. Contiguous contigs from Heimdallarchaeote AB_125 are represented with a double line at the end of the contig. E1-like and putative deubiquitinating proteins not belonging to any ubiquitin cluster are not shown.

Extended Data Figure 6 Phylogenetic analyses of selected ESPs.

a, Tubulin protein family maximum-likelihood tree, highlighting Odinarchaeota homologues branching basal to major eukaryotic tubulin families (red clades). Green clade reflects bacterial tubulin genes probably acquired horizontally from eukaryotes. The tree was rooted with thaumarchaeal artubulins. b, Unrooted maximum-likelihood phylogenetic tree of the replicative polymerase B family depicting a Heimdallarchaeote LC_3 sequence and its corresponding protein model (red), branching basal to the eukaryotic Pol-ε (protein model in grey: PDB ID 4M8O of S. cerevisiae). Bootstrap support values of ≥99, ≥90 and ≥50 for major clades are indicated by black, grey and white circles, respectively. Eukaryotic, bacterial and archaeal clades are shaded red, green and purple, respectively. c, PFAM domain topology analysis of family B polymerases, indicating that the heimdallarchaeal homologue lacks the C-terminal DUF1744 domain characteristic of eukaryotic Pol-ε. d, Unrooted maximum-likelihood tree of RPL28e homologues, including eukaryotic RPL28e and MAK16, a RPL28e-like sequence identified in the Heimdallarchaeote LC_3 genome and a metagenomic homologue. Eukaryotic MAK16 proteins (implicated in rRNA maturation) contain an additional C-terminal domain absent in the heimdallarchaeal protein. a, b, d, Scale bars indicate the number of substitutions per site and numbers at branches show slow, non-parametric maximum-likelihood bootstrap support values.

Extended Data Figure 7 Asgard ESPs are enriched for intracellular trafficking and secretion functions.

Overview of functional classification (arCOGs and EggNOG categories) of Asgard proteins assigned to major taxonomic levels. Taxonomic levels are shown in different colours. Note that, in some cases, one protein can be assigned to more than one functional category.

Extended Data Figure 8 Eukaryotic signatures in Asgard archaea.

Schematic representation of a eukaryotic cell in which ESPs that have been identified in Asgard archaea are highlighted, including their phylogenetic distribution pattern. The overall picture indicates that the archaeal ancestor of eukaryotes already contained many key components underlying the emergence of cellular complexity that is characteristic of eukaryotes. DUB, deubiquitinating enzyme; MVB, multi-vesicular body; ER, endoplasmatic reticulum.

Extended Data Table 1 Assembly statistics and quality metrics of reconstructed Asgard genome bins
Full size table
Extended Data Table 2 Overview of presence/absence pattern of Asgard ESPs
Full size table

Supplementary information

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. (PDF 5144 kb)

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Zaremba-Niedzwiedzka, K., Caceres, E., Saw, J. et al. Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature 541, 353–358 (2017). https://doi.org/10.1038/nature21031

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