Complex archaea that bridge the gap between prokaryotes and eukaryotes

Journal name:
Date published:
Published online


The origin of the eukaryotic cell remains one of the most contentious puzzles in modern biology. Recent studies have provided support for the emergence of the eukaryotic host cell from within the archaeal domain of life, but the identity and nature of the putative archaeal ancestor remain a subject of debate. Here we describe the discovery of ‘Lokiarchaeota’, a novel candidate archaeal phylum, which forms a monophyletic group with eukaryotes in phylogenomic analyses, and whose genomes encode an expanded repertoire of eukaryotic signature proteins that are suggestive of sophisticated membrane remodelling capabilities. Our results provide strong support for hypotheses in which the eukaryotic host evolved from a bona fide archaeon, and demonstrate that many components that underpin eukaryote-specific features were already present in that ancestor. This provided the host with a rich genomic ‘starter-kit’ to support the increase in the cellular and genomic complexity that is characteristic of eukaryotes.

At a glance


  1. Identification of a novel archaeal lineage.
    Figure 1: Identification of a novel archaeal lineage.

    a, Bathymetric map of the sampling site (GC14; red circle) at the Arctic Mid-Ocean Spreading Ridge, located 15 km from Loki’s Castle active vent site. b, 16S rRNA amplicon-based assessment of microbial diversity in GC14. Bars on the left represent the fraction of the respective prokaryotic taxa and bars on the right depict archaeal diversity. Numbers refer to operational taxonomic units for each group. MHVG, Marine Hydrothermal Vent Group; DHVEG-6, Deep-sea Hydrothermal Vent Euryarchaeota Group 6; MBG-A and -B, Marine Benthic Group A and B. c, Maximum likelihood phylogeny of the archaeal 16S rRNA reads (see b), revealing that DSAG sequences cluster deeply in the TACK super-phylum. Numbers between brackets indicate relative abundance (%) of each group relative to total and archaeal reads, respectively. MCG, Miscellaneous Crenarchaeota Group; MHVG, Marine Hydrothermal Vent Group. d, Maximum-likelihood phylogeny of 16S rRNA gene sequences indicating that the DSAG operational taxonomic unit (red font) belongs to the DSAG γ cluster. Bootstrap support values above 50 are shown. c, d, Scale indicates the number of substitutions per site.

  2. Metagenomic reconstruction and phylogenetic analysis of Lokiarchaeum.
    Figure 2: Metagenomic reconstruction and phylogenetic analysis of Lokiarchaeum.

    a, Schematic overview of the metagenomics approach. BI, Bayesian inference; ML, maximum likelihood. b, Bayesian phylogeny of concatenated alignments comprising 36 conserved phylogenetic marker proteins using sophisticated models of protein evolution (Methods), showing eukaryotes branching within Lokiarchaeota. Numbers above and below branches refer to Bayesian posterior probability and maximum-likelihood bootstrap support values, respectively. Posterior probability values above 0.7 and bootstrap support values above 70 are shown. Scale indicates the number of substitutions per site. c, Phylogenetic breakdown of the Lokiarchaeum proteome, in comparison with proteomes of Korarchaeota, Aigarchaeota (Caldiarchaeum) and Miscellaneous Crenarchaeota Group (MCG) archaea. Category ‘Other’ contains proteins assigned to the root of cellular organisms, to viruses and to unclassified proteins.

  3. Identification and phylogeny of small GTPases and actin orthologues.
    Figure 3: Identification and phylogeny of small GTPases and actin orthologues.

    a, Maximum-likelihood phylogeny of 378 aligned amino acid residues of actin homologues identified in Lokiarchaeum and in the LCGC14AMP metagenome, including eukaryotic actins, ARP1–3 homologues and crenactins25. Consecutive numbers in brackets refer to the number of sequences in a respective clade from LCGC14AMP and Lokiarchaeum, respectively. b, Relative amount of small GTPases (assigned to IPR006689 and IPR001806) in the Lokiarchaeum genome in comparison with other eukaryotic, archaeal and bacterial species. Numbers refer to total amount of small GTPases per predicted proteome. c, Maximum-likelihood phylogeny of 150 aligned amino acid residues of small Ras- and Arf-type GTPases (IPR006689 and IPR001806) in all domains of life. Numbers in brackets refer to the number of sequences in the respective clades. a, c, Sequence clusters comprising Lokiarchaeum and/or LCGC14AMP sequences (red), eukaryotes (blue) and Bacteria/Archaea (grey) have been collapsed. Bootstrap values above 50 are shown. Scale indicates the number of substitutions per site.

  4. Identification of ESCRT components in the Lokiarchaeum genome.
    Figure 4: Identification of ESCRT components in the Lokiarchaeum genome.

    a, Schematic overview of ESCRT gene clusters identified in Lokiarchaeum and Loki2/3. Intensity of shading between homologous sequences is correlated with BLAST bit score. b, Maximum-likelihood phylogeny of 207 aligned amino acid residues of ESCRT-III homologues identified in Lokiarchaeum, LCGC14AMP and other archaeal lineages. Eukaryotic homologues include the two distantly related families Vps2/24/46 and Vps20/32/60. Bootstrap support values above 50 are shown. c, Maximum-likelihood phylogeny of 388 aligned amino acid residues of AAA-type Vps4 ATPases including representatives for each of the four major eukaryotic sub-groups (membrane scaffold protein (MSP), katanin, spastin/fidgetin and Vps4) as well as homologues identified in the Lokiarchaeum genome, in LCGC14AMP and in sequenced archaeal genomes. Bootstrap support values below 45 are not shown. b, c, Scale indicates the number of substitutions per site. Numbers in brackets refer to the number of sequences in the respective clades.

  5. The complex archaeal ancestry of eukaryotes.
    Figure 5: The complex archaeal ancestry of eukaryotes.

    Schematic overview of the distribution of ESPs in major archaeal lineages across the tree of life. Each ESP is depicted as a coloured circle and losses are indicated with a cross. Patchy distribution and absence of a particular ESP in archaeal phyla is indicated by half-shaded and white circles, respectively. aWhile eukaryotes and Lokiarchaeota contain bona fide actins, other archaea encode the more distantly related Crenactins. bOnly few members of the Thaumarchaeota contain distantly related homologs of tubulins (ar-tubulins). cThaum-, Aig- and some Crenarchaeota contain distant homologues of ESCRT-III (SNF7 domain proteins).


  1. Overview of Lokiarchaeal ESPs
    Extended Data Table 1: Overview of Lokiarchaeal ESPs

Accession codes

Primary accessions


NCBI Reference Sequence

Sequence Read Archive


  1. Embley, T. M. & Martin, W. Eukaryotic evolution, changes and challenges. Nature 440, 623630 (2006)
  2. Koonin, E. V. & Yutin, N. The dispersed archaeal eukaryome and the complex archaeal ancestor of eukaryotes. Cold Spring Harb. Perspect. Biol. 6, a016188 (2014)
  3. Koumandou, V. L. et al. Molecular paleontology and complexity in the last eukaryotic common ancestor. Crit. Rev. Biochem. Mol. Biol. 48, 373396 (2013)
  4. Woese, C. R. & Fox, G. E. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc. Natl Acad. Sci. USA 74, 50885090 (1977)
  5. Woese, C. R., Kandler, O. & Wheelis, M. L. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl Acad. Sci. USA 87, 45764579 (1990)
  6. Pühler, G. et al. Archaebacterial DNA-dependent RNA polymerases testify to the evolution of the eukaryotic nuclear genome. Proc. Natl Acad. Sci. USA 86, 45694573 (1989)
  7. Bult, C. J. et al. Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science 273, 10581073 (1996)
  8. Rivera, M. C., Jain, R., Moore, J. E. & Lake, J. A. Genomic evidence for two functionally distinct gene classes. Proc. Natl Acad. Sci. USA 95, 62396244 (1998)
  9. McInerney, J. O., O’Connell, M. J. & Pisani, D. The hybrid nature of the Eukaryota and a consilient view of life on Earth. Nature Rev. Microbiol.. 12, 449–455 (2014)
  10. Gribaldo, S., Poole, A. M., Daubin, V., Forterre, P. & Brochier-Armanet, C. The origin of eukaryotes and their relationship with the Archaea: are we at a phylogenomic impasse? Nature Rev. Microbiol.. 8, 743–752 (2010)
  11. Yutin, N., Makarova, K. S., Mekhedov, S. L., Wolf, Y. I. & Koonin, E. V. The deep archaeal roots of eukaryotes. Mol. Biol. Evol.. 25, 1619–1630 (2008)
  12. Rochette, N. C., Brochier-Armanet, C. & Gouy, M. Phylogenomic test of the hypotheses for the evolutionary origin of eukaryotes. Mol. Biol. Evol.. 31, 832–845 (2014)
  13. Thiergart, T., Landan, G., Schenk, M., Dagan, T. & Martin, W. F. An evolutionary network of genes present in the eukaryote common ancestor polls genomes on eukaryotic and mitochondrial origin. Genome Biol. Evol.. 4, 466–485 (2012)
  14. Henderson, E. et al. A new ribosome structure. Science 225, 510512 (1984)
  15. Koonin, E. V. The origin and early evolution of eukaryotes in the light of phylogenomics. Genome Biol. 11, 209 (2010)
  16. Lake, J. A. Origin of the eukaryotic nucleus determined by rate-invariant analysis of rRNA sequences. Nature 331, 184–186 (1988)
  17. Williams, T. A., Foster, P. G., Cox, C. J. & Embley, T. M. An archaeal origin of eukaryotes supports only two primary domains of life. Nature 504, 231–236 (2013)
  18. Cox, C. J., Foster, P. G., Hirt, R. P., Harris, S. R. & Embley, T. M. The archaebacterial origin of eukaryotes. Proc. Natl Acad. Sci.. USA 105, 20356–20361 (2008)
  19. Foster, P. G., Cox, C. J. & Embley, T. M. The primary divisions of life: a phylogenomic approach employing composition-heterogeneous methods. Phil. Trans. R. Soc. Lond.. B 364, 2197–2207 (2009)
  20. Guy, L., Saw, J. H. & Ettema, T. J. The archaeal legacy of eukaryotes: a phylogenomic perspective. Cold Spring Harb. Perspect. Biol. 6, a016022. (2014)
  21. Lasek-Nesselquist, E. & Gogarten, J. P. The effects of model choice and mitigating bias on the ribosomal tree of life. Mol. Phylogenet. Evol.. 69, 17–38 (2013)
  22. Williams, T. A., Foster, P. G., Nye, T. M., Cox, C. J. & Embley, T. M. A congruent phylogenomic signal places eukaryotes within the Archaea. Proc. R. Soc. Lond.. B 279, 4870–4879 (2012)
  23. Guy, L. & Ettema, T. J. The archaeal ‘TACK’ superphylum and the origin of eukaryotes. Trends Microbiol. 19, 580587 (2011)
  24. Hartman, H. & Fedorov, A. The origin of the eukaryotic cell: a genomic investigation. Proc. Natl Acad. Sci.. USA 99, 1420–1425 (2002)
  25. Ettema, T. J., Lindås, A.-C. & Bernander, R. An actin-based cytoskeleton in archaea. Mol. Microbiol.. 80, 1052–1061 (2011)
  26. Yutin, N. & Koonin, E. V. Archaeal origin of tubulin. Biol. Direct 7, 10 (2012)
  27. Lindås, A.-C., Karlsson, E. A., Lindgren, M. T., Ettema, T. J. & Bernander, R. A unique cell division machinery in the Archaea. Proc. Natl Acad. Sci.. USA 105, 18942–18946 (2008)
  28. Martijn, J. & Ettema, T. J. From archaeon to eukaryote: the evolutionary dark ages of the eukaryotic cell. Biochem. Soc. Trans.. 41, 451–457 (2013)
  29. Pedersen, R. B. et al. Discovery of a black smoker vent field and vent fauna at the Arctic Mid-Ocean Ridge. Nat. Commun.. 1, 126 (2010)
  30. Jørgensen, S. L. et al. Correlating microbial community profiles with geochemical data in highly stratified sediments from the Arctic Mid-Ocean Ridge. Proc. Natl Acad. Sci.. USA 109, E2846–E2855 (2012)
  31. Jørgensen, S. L., Thorseth, I. H., Pedersen, R. B., Baumberger, T. & Schleper, C. Quantitative and phylogenetic study of the Deep Sea Archaeal Group in sediments of the Arctic mid-ocean spreading ridge. Front. Microbiol. 4, 299 (2013)
  32. Inagaki, F. et al. Microbial communities associated with geological horizons in coastal subseafloor sediments from the Sea of Okhotsk. Appl. Environ. Microbiol. 69, 72247235 (2003)
  33. Vetriani, C., Jannasch, H. W., MacGregor, B. J., Stahl, D. A. & Reysenbach, A. L. Population structure and phylogenetic characterization of marine benthic Archaea in deep-sea sediments. Appl. Environ. Microbiol. 65, 43754384 (1999)
  34. Von Schnurbein, S. The function of Loki in Snorri Sturluson’s Edda. Hist. Relig. 40, 109124 (2000)
  35. Deschamps, P., Zivanovic, Y., Moreira, D., Rodriguez-Valera, F. & Lopez-Garcia, P. Pangenome evidence for extensive interdomain horizontal transfer affecting lineage core and shell genes in uncultured planktonic thaumarchaeota and euryarchaeota. Genome Biol. Evol.. 6, 1549–1563 (2014)
  36. Nelson-Sathi, S. et al. Origins of major archaeal clades correspond to gene acquisitions from bacteria. Nature 517, 7780 (2015)
  37. Yutin, N., Wolf, M. Y., Wolf, Y. I. & Koonin, E. V. The origins of phagocytosis and eukaryogenesis. Biol. Direct 4, 9 (2009)
  38. Kawai, M. et al. High frequency of phylogenetically diverse reductive dehalogenase-homologous genes in deep subseafloor sedimentary metagenomes. Front. Microbiol. 5, 80 (2014)
  39. Pollard, T. D. & Cooper, J. A. Actin, a central player in cell shape and movement. Science 326, 1208–1212 (2009)
  40. Bernander, R., Lind, A. E. & Ettema, T. J. An archaeal origin for the actin cytoskeleton: Implications for eukaryogenesis. Commun. Integr. Biol. 4, 664667 (2011)
  41. Pollard, T. D. & Borisy, G. G. Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453465 (2003)
  42. Takai, Y., Sasaki, T. & Matozaki, T. Small GTP-binding proteins. Physiol. Rev. 81, 153208 (2001)
  43. Zhang, Y., Franco, M., Ducret, A. & Mignot, T. A bacterial Ras-like small GTP-binding protein and its cognate GAP establish a dynamic spatial polarity axis to control directed motility. PLoS Biol. 8, e1000430 (2010)
  44. Hurley, J. H. The ESCRT complexes. Crit. Rev. Biochem. Mol. Biol.. 45, 463–487 (2010)
  45. Field, M. C. & Dacks, J. B. First and last ancestors: reconstructing evolution of the endomembrane system with ESCRTs, vesicle coat proteins, and nuclear pore complexes. Curr. Opin. Cell Biol.. 21, 4–13 (2009)
  46. Leung, K. F., Dacks, J. B. & Field, M. C. Evolution of the multivesicular body ESCRT machinery; retention across the eukaryotic lineage. Traffic 9, 1698–1716 (2008)
  47. Kostelansky, M. S. et al. Structural and functional organization of the ESCRT-I trafficking complex. Cell 125, 113–126 (2006)
  48. Raiborg, C. & Stenmark, H. The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 458, 445–452 (2009)
  49. Nunoura, T. et al. Insights into the evolution of Archaea and eukaryotic protein modifier systems revealed by the genome of a novel archaeal group. Nucleic Acids Res. 39, 3204–3223 (2011)
  50. Poole, A. M. & Gribaldo, S. Eukaryotic origins: how and when was the mitochondrion acquired? Cold Spring Harb. Perspect. Biol. 6, a015990. (2014)
  51. Jorgensen, S. L. et al. Correlating microbial community profiles with geochemical data in highly stratified sediments from the Arctic Mid-Ocean Ridge. Proc. Natl Acad. Sci.. USA 109, E2846–E2855 (2012)
  52. Jorgensen, S. L., Thorseth, I. H., Pedersen, R. B., Baumberger, T. & Schleper, C. Quantitative and phylogenetic study of the deep sea archaeal group in sediments of the Arctic Mid-Ocean spreading ridge. Front. Microbiol. 4, 299 (2013)
  53. Hugenholtz, P., Pitulle, C., Hershberger, K. L. & Pace, N. R. Novel division level bacterial diversity in a Yellowstone hot spring. J. Bacteriol. 180, 366376 (1998)
  54. Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014)
  55. Altschul, S. F. et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 33893402 (1997)
  56. Edgar, R. C. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods 10, 996–998 (2013)
  57. Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C. & Knight, R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200 (2011)
  58. Schloss, P. D. et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol.. 75, 7537–7541 (2009)
  59. Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2013)
  60. Durbin, A. M. & Teske, A. Archaea in organic-lean and organic-rich marine subsurface sediments: an environmental gradient reflected in distinct phylogenetic lineages. Front. Microbiol. 3, 168 (2012)
  61. Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol.. 30, 772–780 (2013)
  62. Capella-Gutiérrez, S., Silla-Martinez, J. M. & Gabaldon, T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973 (2009)
  63. Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014)
  64. Letunic, I. & Bork, P. Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res. 39, W475–W478 (2011)
  65. Pruesse, E., Peplies, J. & Glockner, F. O. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28, 1823–1829 (2012)
  66. Gouy, M., Guindon, S. & Gascuel, O. SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol. Biol. Evol.. 27, 221–224 (2010)
  67. Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010)
  68. Junier, T. & Zdobnov, E. M. The Newick utilities: high-throughput phylogenetic tree processing in the UNIX shell. Bioinformatics 26, 1669–1670 (2010)
  69. Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455477 (2012)
  70. Hyatt, D. et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11, 119 (2010)
  71. Lagesen, K. et al. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 35, 3100–3108 (2007)
  72. Lowe, T. M. & Eddy, S. R. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25, 955964 (1997)
  73. Sugahara, J. et al. SPLITS: a new program for predicting split and intron-containing tRNA genes at the genome level. In Silico Biol. 6, 411418 (2006)
  74. Wolf, Y. I., Makarova, K. S., Yutin, N. & Koonin, E. V. Updated clusters of orthologous genes for Archaea: a complex ancestor of the Archaea and the byways of horizontal gene transfer. Biol. Direct 7, 46 (2012)
  75. Kristensen, D. M. et al. A low-polynomial algorithm for assembling clusters of orthologous groups from intergenomic symmetric best matches. Bioinformatics 26, 1481–1487 (2010)
  76. Lartillot, N., Rodrigue, N., Stubbs, D. & Richer, J. PhyloBayes MPI: phylogenetic reconstruction with infinite mixtures of profiles in a parallel environment. Syst. Biol.. 62, 611–615 (2013)
  77. Sukumaran, J. & Holder, M. T. DendroPy: a Python library for phylogenetic computing. Bioinformatics 26, 1569–1571 (2010)
  78. Viklund, J., Ettema, T. J. & Andersson, S. G. Independent genome reduction and phylogenetic reclassification of the oceanic SAR11 clade. Mol. Biol. Evol.. 29, 599–615 (2012)
  79. Guy, L., Saw, J. H. & Ettema, T. J. The Archaeal Legacy of Eukaryotes: A Phylogenomic Perspective. Cold Spring Harb. Perspect. Biol.. 6, a016022 (2014)
  80. Shimodaira, H. An approximately unbiased test of phylogenetic tree selection. Syst. Biol.. 51, 492–508 (2002)
  81. Shimodaira, H. & Hasegawa, M. CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17, 12461247 (2001)
  82. Guy, L., Spang, A., Saw, J. H. & Ettema, T. J. ‘Geoarchaeote NAG1’ is a deeply rooting lineage of the archaeal order Thermoproteales rather than a new phylum. ISME J. 8, 13531357 (2014)
  83. R Core Team R: A Language and Environment for Statistical Computing (2014)
  84. Venables, W. N. & Ripley, B. D. Modern Applied Statistics with S 4th edn (Springer, 2002)
  85. Brady, A. & Salzberg, S. L. Phymm and PhymmBL: metagenomic phylogenetic classification with interpolated Markov models. Nature Methods 6, 673–676 (2009)
  86. Rinke, C. et al. Insights into the phylogeny and coding potential of microbial dark matter. Nature 499, 431437 (2013)
  87. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009)
  88. Seemann, T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30, 2068–2069 (2014)
  89. Huson, D. H., Auch, A. F., Qi, J. & Schuster, S. C. MEGAN analysis of metagenomic data. Genome Res. 17, 377–386 (2007)
  90. Zdobnov, E. M. & Apweiler, R. InterProScan–an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17, 847848 (2001)
  91. Vallenet, D. et al. MaGe: a microbial genome annotation system supported by synteny results. Nucleic Acids Res. 34, 53–65 (2006)
  92. Kelley, L. A. & Sternberg, M. J. Protein structure prediction on the Web: a case study using the Phyre server. Nature Protocols 4, 363–371 (2009)
  93. Yutin, N., Puigbo, P., Koonin, E. V. & Wolf, Y. I. Phylogenomics of prokaryotic ribosomal proteins. PLoS ONE 7, e36972 (2012)
  94. Powell, S. et al. eggNOG v4.0: nested orthology inference across 3686 organisms. Nucleic Acids Res. 42, D231–D239 (2014)
  95. Kawai, M. et al. High frequency of phylogenetically diverse reductive dehalogenase-homologous genes in deep subseafloor sedimentary metagenomes. Front. Microbiol. 5, 80 (2014)
  96. Morono, Y., Terada, T., Hoshino, T. & Inagaki, F. Hot-alkaline DNA extraction method for deep-subseafloor archaeal communities. Appl. Environ. Microbiol.. 80, 1985–1994 (2014)
  97. Makarova, K. S., Yutin, N., Bell, S. D. & Koonin, E. V. Evolution of diverse cell division and vesicle formation systems in Archaea. Nature Rev. Microbiol.. 8, 731–741 (2010)
  98. Quevillon, E. et al. InterProScan: protein domains identifier. Nucleic Acids Res. 33, W116–W120 (2005)
  99. Dong, J. H., Wen, J. F. & Tian, H. F. Homologs of eukaryotic Ras superfamily proteins in prokaryotes and their novel phylogenetic correlation with their eukaryotic analogs. Gene 396, 116–124 (2007)
  100. Ettema, T. J., Lindas, A. C. & Bernander, R. An actin-based cytoskeleton in archaea. Mol. Microbiol.. 80, 1052–1061 (2011)
  101. Yutin, N., Wolf, M. Y., Wolf, Y. I. & Koonin, E. V. The origins of phagocytosis and eukaryogenesis. Biol. Direct 4, 9 (2009)
  102. Goodson, H. V. & Hawse, W. F. Molecular evolution of the actin family. J. Cell Sci. 115, 26192622 (2002)
  103. Wu, D. et al. A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea. Nature 462, 1056–1060 (2009)
  104. Guy, L., Roat Kultima, J. & Andersson, S. G. E. genoPlotR: comparative gene and genome visualization in R. Bioinformatics 26, 23342335 (2010)

Download references

Author information

  1. Present address: Groningen Institute for Evolutionary Life Sciences, University of Groningen, NL-9747AG Groningen, The Netherlands.

    • Roel van Eijk
  2. These authors contributed equally to this work.

    • Anja Spang,
    • Jimmy H. Saw,
    • Steffen L. Jørgensen &
    • Katarzyna Zaremba-Niedzwiedzka


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

    • Anja Spang,
    • Jimmy H. Saw,
    • Katarzyna Zaremba-Niedzwiedzka,
    • Joran Martijn,
    • Anders E. Lind,
    • Roel van Eijk,
    • Lionel Guy &
    • Thijs J. G. Ettema
  2. Department of Biology, Centre for Geobiology, University of Bergen, N-5020 Bergen, Norway

    • Steffen L. Jørgensen &
    • Christa Schleper
  3. Division of Archaea Biology and Ecogenomics, Department of Ecogenomics and Systems Biology, University of Vienna, A-1090 Vienna, Austria

    • Christa Schleper
  4. Department of Medical Biochemistry and Microbiology, Uppsala University, SE-75123 Uppsala, Sweden

    • Lionel Guy


T.J.G.E., S.L.J. and C.S. conceived the study. S.L.J. provided deep-sea sediments and isolated community DNA. R.v.E., J.H.S. and A.E.L. prepared sequencing libraries. A.E.L., J.H.S., S.L.J. and J.M. analysed environmental sequence data. L.G., K.Z.-N. and J.H.S. performed, optimised and analysed metagenomic sequence assemblies. L.G., J.H.S., A.S., K.Z.-N. and T.J.G.E. analysed genomic data and performed phylogenetic analyses. A.S., L.G., S.L.J. and T.J.G.E analysed genomic signatures of DSAG. T.J.G.E., A.S., S.L.J. and L.G. wrote, and all authors edited and approved the manuscript.

Competing financial interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to:

Sequence data have been deposited to the NCBI Sequence Read Archive under study number SRP045692, which includes 16 rRNA reads (experiment number SRX872366). Protein sequences of Loki2/3 were deposited to GenBank under accession numbers KP869578KP869724. The Lokiarchaeum genome bin and the LCGC14 metagenome projects have been deposited at DDBJ/EMBL/GenBank under the accessions JYIM00000000 and LAZR00000000, respectively. The versions described in this paper are versions JYIM01000000 and LAZR01000000.

Author details

Extended data figures and tables

Supplementary information

PDF files

  1. Supplementary Information (5.4 MB)

    This file contains a Supplementary Discussion detailing the phylogenetic analysis of the Lokiarchaeota-Eukarya affiliation as well as the simplified ‘eukaryotic ribosome’ of Lokiarchaeum. It also includes Supplementary Tables 1-10 and Supplementary Figures 1-24, which provide more details into annotations, applied methods and phylogenetic analyses.

Additional data