The Tree of Life

  • Morgan Gaia
  • Violette Da Cunha
  • Patrick ForterreEmail author
Part of the Grand Challenges in Biology and Biotechnology book series (GCBB)


The tree of life, representing the evolution and the relationships between all life-forms, has challenged scientists as soon as Darwin’s work became accepted. A fuel for imagination for a long time, it became more concrete after the molecular biology revolution and the application of mathematical tools to quantify sequence evolution. Despite tremendous advances fueled by the continuous progress in DNA sequencing, from PCR to metagenomics, and in algorithms for phylogenetic reconstruction, many fundamental questions remain still open in the tree of life topology. The biggest of them all would currently be the relationship between Archaea and Eukarya: while some authors argue that they are sister groups (the Woese tree), others state that the latter emerged from the former (the eocyte tree). The tree of life and its subsequent questions are definitely complex objects to comprehend. Evolution states that in order to fully understand life, one has to first know its history, and this mantra should apply here as well. We thus decided to focus in this chapter on the recent history of the tree of life, from its entry into phylogenetics in the 1970s to the recent identification of Asgard archaea and the controversies they have brought. We also briefly discuss the position of the viruses in the tree of life and how their analysis is helpful to understand their host evolution.



MG, VDC, and PF are supported by an ERC grant from the European Union’s Seventh Framework Program (FP/2007–2013)/Project EVOMOBIL-ERC Grant Agreement no. 340440. We thank Pabulo Henrique Rampelotto for the opportunity to write this chapter.


  1. Adam PS, Borrel G, Brochier-Armanet C, Gribaldo S (2017) The growing tree of Archaea: new perspectives on their diversity, evolution and ecology. ISME J 11(11):2407–2425PubMedCrossRefPubMedCentralGoogle Scholar
  2. Albers SV, Forterre P, Prangishvili D, Schleper C (2013) The legacy of Carl Woese and Wolfram Zillig: from phylogeny to landmark discoveries. Nat Rev Microbiol 11(10):713–719PubMedCrossRefPubMedCentralGoogle Scholar
  3. Atkinson GC (2015) The evolutionary and functional diversity of classical and lesser-known cytoplasmic and organellar translational GTPases across the tree of life. BMC Genomics 16:78PubMedPubMedCentralCrossRefGoogle Scholar
  4. Baker BJ, Tyson GW, Webb RI et al (2006) Lineages of acidophilic archaea revealed by community genomic analysis. Science 314(5807):1933–1935PubMedCrossRefPubMedCentralGoogle Scholar
  5. Baker BJ, Comolli LR, Dick GJ et al (2010) Enigmatic, ultrasmall, uncultivated Archaea. Proc Natl Acad Sci USA 107(19):8806–8811PubMedCrossRefPubMedCentralGoogle Scholar
  6. Baldauf SL, Palmer JD, Doolittle WF (1996) The root of the universal tree and the origin of eukaryotes based on elongation factor phylogeny. Proc Natl Acad Sci USA 93(15):7749–7754PubMedCrossRefPubMedCentralGoogle Scholar
  7. Baross JA, Martin WF (2015) The ribofilm as a concept for life’s origins. Cell 162(1):15–15CrossRefGoogle Scholar
  8. Bell PJL (2001) Viral eukaryogenesis: was the ancestor of the nucleus a complex DNA virus? J Mol Evol 53:251–256PubMedCrossRefPubMedCentralGoogle Scholar
  9. Booth A, Doolittle WF (2015) Reply to lane and Martin: being and becoming eukaryotes. Proc Natl Acad Sci USA 112(35):E4824PubMedCrossRefPubMedCentralGoogle Scholar
  10. Boyer M, Madoui M-A, Gimenez G et al (2010) Phylogenetic and phyletic studies of informational genes in genomes highlight existence of a 4th domain of life including giant viruses. PLoS One 5(12):e15530PubMedPubMedCentralCrossRefGoogle Scholar
  11. Brochier C, Forterre P, Gribaldo S (2004) Archaeal phylogeny based on proteins of the transcription and translation machineries: tackling the Methanopyrus kandleri paradox. Genome Biol 5(3):R17PubMedPubMedCentralCrossRefGoogle Scholar
  12. Brochier C, Forterre P, Gribaldo S (2005a) An emerging phylogenetic core of Archaea: phylogenies of transcription and translation machineries converge following addition of new genome sequences. BMC Evol Biol 5:36PubMedPubMedCentralCrossRefGoogle Scholar
  13. Brochier C, Gribaldo S, Zivanovic Y et al (2005b) Nanoarchaea: representatives of a novel archaeal phylum or a fast-evolving euryarchaeal lineage related to Thermococcales? Genome Biol 6(5):R42PubMedPubMedCentralCrossRefGoogle Scholar
  14. Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P (2008a) Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 6(3):245–252PubMedCrossRefPubMedCentralGoogle Scholar
  15. Brochier-Armanet C, Gribaldo S, Forterre P (2008b) A DNA topoisomerase IB in Thaumarchaeota testifies for the presence of this enzyme in the last common ancestor of Archaea and Eucarya. Biol Direct 3:54PubMedPubMedCentralCrossRefGoogle Scholar
  16. Brochier-Armanet C, Forterre P, Gribaldo S (2011) Phylogeny and evolution of the Archaea: one hundred genomes later. Curr Opin Microbiol 14(3):274–281PubMedCrossRefPubMedCentralGoogle Scholar
  17. Brown JR, Doolittle WF (1997) Archaea and the prokaryote-to-eukaryote transition. Microbiol Mol Biol Rev 61(4):456–502PubMedPubMedCentralGoogle Scholar
  18. Brown JR, Douady CJ, Italia MJ et al (2001) Universal trees based on large combined protein sequence data sets. Nat Genet 28(3):281–285PubMedCrossRefPubMedCentralGoogle Scholar
  19. Brown CT, Hug LA, Thomas BC et al (2015) Unusual biology across a group comprising more than 15% of domain bacteria. Nature 523(7559):208–211PubMedCrossRefPubMedCentralGoogle Scholar
  20. Bruno WJ, Halpern AL (1999) Topological bias and inconsistency of maximum-likelihood using wrong models. Mol Biol Evol 16(4):564–566PubMedCrossRefPubMedCentralGoogle Scholar
  21. Brüssow H (2009) The not so universal tree of life or the place of viruses in the living world. Philos Trans R Soc Lond Ser B Biol Sci 364(1527):2263–2274CrossRefGoogle Scholar
  22. Camin JH, Sokal RR (1965) A method for deducing branching sequences in phylogeny. Evolution 19:311–323CrossRefGoogle Scholar
  23. Cammarano P, Palm P, Creti R et al (1992) Early evolutionary relationships among known life forms inferred from elongation factor EF-2/EF-G sequences: phylogenetic coherence and structure of the archaeal domain. J Mol Evol 34(5):396–405PubMedCrossRefPubMedCentralGoogle Scholar
  24. Cammarano P, Creti R, Sanangelantoni AM, Palm P (1999) The archaea monophyly issue: a phylogeny of translational elongation factor G(2) sequences inferred from an optimized selection of alignment positions. J Mol Evol 49(4):524–537PubMedCrossRefPubMedCentralGoogle Scholar
  25. Castelle CJ, Wrighton KC, Thomas BC et al (2015) Genomic expansion of domain archaea highlights roles for organisms from new phyla in anaerobic carbon cycling. Curr Biol 25(6):690–701PubMedCrossRefPubMedCentralGoogle Scholar
  26. Cavalier-Smith T (1989) Molecular phylogeny. Archaebacteria and Archezoa. Nature 339(6220):100–101CrossRefGoogle Scholar
  27. Chaikeeratisak V, Nguyen K, Khanna K et al (2017) Assembly of a nucleus-like structure during viral replication in bacteria. Science 355(6321):194–197PubMedPubMedCentralCrossRefGoogle Scholar
  28. Ciccarelli FD, Doerks T, von Mering C et al. (2006) Toward automatic reconstruction of a highly resolved tree of life. Science 311 (5765):1283–7. Erratum in: (2006) Science 312 (5774):697PubMedCrossRefPubMedCentralGoogle Scholar
  29. Cobb M (2017) 60 years ago, Francis Crick changed the logic of biology. PLoS Biol 15(9):e2003243PubMedPubMedCentralCrossRefGoogle Scholar
  30. Comolli LR, Baker JB, Downing KH et al (2009) Three-dimensional analysis of the structure and ecology of a novel, ultra-small archaeon. ISME J 3(2):159–167PubMedCrossRefPubMedCentralGoogle Scholar
  31. Cox CJ, Foster PG, Hirt RP et al (2008) The archaebacterial origin of eukaryotes. Proc Natl Acad Sci USA 105(51):20356–20361PubMedCrossRefPubMedCentralGoogle Scholar
  32. Creti R, Ceccarelli E, Bocchetta M et al (1994) Evolution of translational elongation factor (EF) sequences: reliability of global phylogenies inferred from EF-1 alpha(Tu) and EF-2(G) proteins. Proc Natl Acad Sci USA 91(8):3255–3259PubMedCrossRefPubMedCentralGoogle Scholar
  33. Csurös M, Miklós I (2009) Streamlining and large ancestral genomes in Archaea inferred with a phylogenetic birth-and-death model. Mol Biol Evol 26(9):2087–2095PubMedPubMedCentralCrossRefGoogle Scholar
  34. Csurös M, Rogozin IB, Koonin EV (2011) A detailed history of intron-rich eukaryotic ancestors inferred from a global survey of 100 complete genomes. PLoS Comput Biol 7(9):e1002150PubMedPubMedCentralCrossRefGoogle Scholar
  35. Da Cunha V, Gaia M, Gadelle D et al (2017) Lokiarchaea are close relatives of Euryarchaeota, not bridging the gap between prokaryotes and eukaryotes. PLoS Genet 13(6):e1006810PubMedPubMedCentralCrossRefGoogle Scholar
  36. Da Cunha V, Gaia M, Nasir A, Forterre P (2018) Asgard archaea do not close the debate about the universal tree of life topology. PLoS Genet 14(3):e1007215PubMedPubMedCentralCrossRefGoogle Scholar
  37. Dacks JB, Field MC, Buick R et al (2016) The changing view of eukaryogenesis – fossils, cells, lineages and how they all come together. J Cell Sci 129(20):3695–3703PubMedCrossRefPubMedCentralGoogle Scholar
  38. Dagan T, Martin W (2009) Getting a better picture of microbial evolution en route to a network of genomes. Philos Trans R Soc Lond Ser B Biol Sci 364(1527):2187–2196CrossRefGoogle Scholar
  39. de Duve C (2007) The origin of eukaryotes: a reappraisal. Nat Rev Genet 8(5):395–403PubMedCrossRefPubMedCentralGoogle Scholar
  40. Degli Esposti M (2016) Late mitochondrial acquisition, really? Genome Biol Evol 8(6):2031–2035PubMedPubMedCentralCrossRefGoogle Scholar
  41. Doolittle WF (2009) The practice of classification and the theory of evolution, and what the demise of Charles Darwin’s tree of life hypothesis means for both of them. Philos Trans R Soc Lond Ser B Biol Sci 364(1527):2221–2228CrossRefGoogle Scholar
  42. Edlind TD, Li J, Visvesvara GS et al (1996) Phylogenetic analysis of beta-tubulin sequences from amitochondrial protozoa. Mol Phylogenet Evol 5(2):359–367PubMedCrossRefPubMedCentralGoogle Scholar
  43. Edwards AWF, Cavalli-Sforza LL (1963) The reconstruction of evolution. Heredity 18:553Google Scholar
  44. Embley TM, Hirt RP (1998) Early branching eukaryotes? Curr Opin Genet Dev 8(6):624–629PubMedCrossRefPubMedCentralGoogle Scholar
  45. Embley TM, Williams TA (2015) Evolution: steps on the road to eukaryotes. Nature 521(7551):169–170PubMedCrossRefPubMedCentralGoogle Scholar
  46. Eme L, Spang A, Lombard J et al (2017) Archaea and the origin of eukaryotes. Nat Rev Microbiol 15(12):711–723PubMedCrossRefPubMedCentralGoogle Scholar
  47. Eren AM, Esen ÖC, Quince C et al (2015) Anvi’o: an advanced analysis and visualization platform for ‘omics data. PeerJ 3:e1319PubMedPubMedCentralCrossRefGoogle Scholar
  48. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 16(6):368–376CrossRefGoogle Scholar
  49. Fitch WM, Margoliash E (1967) Construction of phylogenetic trees. Science 155(3760):279–284PubMedCrossRefPubMedCentralGoogle Scholar
  50. Forterre P (1995) Thermoreduction, a hypothesis for the origin of prokaryotes. C R Acad Sci III 318(4):415–422PubMedPubMedCentralGoogle Scholar
  51. Forterre P (2006) Three RNA cells for ribosomal lineages and three DNA viruses to replicate their genomes: a hypothesis for the origin of cellular domain. Proc Natl Acad Sci USA 103(10):3669–3674PubMedCrossRefPubMedCentralGoogle Scholar
  52. Forterre P (2010) Defining life: the virus viewpoint. Orig Life Evol Biosph 40(2):151–160PubMedPubMedCentralCrossRefGoogle Scholar
  53. Forterre P (2011) A new fusion hypothesis for the origin of Eukarya: better that previous ones, but probably also wrong. Res Microbiol 62(1):77–91CrossRefGoogle Scholar
  54. Forterre P (2012) Darwin’s goldmine is still open: variation and selection run the world. Front Cell Infect Microbiol 2:106PubMedPubMedCentralCrossRefGoogle Scholar
  55. Forterre P (2013) The common ancestor of Archaea and Eukarya was not an archaeon. Archaea 2013:372396PubMedPubMedCentralCrossRefGoogle Scholar
  56. Forterre P (2015) The universal tree of life: an update. Front Microbiol 6:717PubMedPubMedCentralCrossRefGoogle Scholar
  57. Forterre P (2016a) Microbes from Hell. Chicago University Press, ChicagoCrossRefGoogle Scholar
  58. Forterre P (2016b) To be or not to be alive: how recent discoveries challenge the traditional definitions of viruses and life. Stud Hist Phil Biol Biomed Sci 59:100–108CrossRefGoogle Scholar
  59. Forterre P, Gadelle D (2009) Phylogenomics of DNA topoisomerases: their origin and putative roles in the emergence of modern organisms. Nucleic Acids Res 37(3):679–692PubMedPubMedCentralCrossRefGoogle Scholar
  60. Forterre P, Gaia M (2016) Giant viruses and the origin of modern eukaryotes. Curr Opin Microbiol 31:44–49PubMedCrossRefPubMedCentralGoogle Scholar
  61. Forterre P, Philippe H (1999) Where is the root of the universal tree of life? BioEssays 21(10):871–879CrossRefGoogle Scholar
  62. Forterre P, Gribaldo S, Brochier-Armanet C (2009) Happy together: genomic insights into the unique Nanoarchaeum/Ignicoccus association. J Biol 8(1):7. CrossRefPubMedPubMedCentralGoogle Scholar
  63. Forterre P, Prangishvili D (2013) The major role of viruses in cellular evolution: facts and hypotheses. Curr Opin Virol 3(5):558–565PubMedCrossRefPubMedCentralGoogle Scholar
  64. Forterre P, Krupovic M, Prangishvili D (2014) Cellular domains and viral lineages. Trends Microbiol 22(10):554–558PubMedCrossRefPubMedCentralGoogle Scholar
  65. Foster PG, Cox CJ, Embley TM (2009) The primary divisions of life: a phylogenomic approach employing composition-heterogeneous methods. Philos Trans R Soc Lond Ser B Biol Sci 364(1527):2197–2207CrossRefGoogle Scholar
  66. Furukawa R, Nakagawa M, Kuroyanagi T et al (2017) Quest for ancestors of eukaryal cells based on phylogenetic analyses of aminoacyl-tRNA synthetases. J Mol Evol 84(1):51–66PubMedCrossRefPubMedCentralGoogle Scholar
  67. Glansdorff N, Xu Y, Labedan B (2008) The last universal common ancestor: emergence, constitution and genetic legacy of an elusive forerunner. Biol Direct 3:29PubMedPubMedCentralCrossRefGoogle Scholar
  68. Gogarten JP, Kibak H, Dittrich P et al (1989) Evolution of the vacuolar H+-ATPase: implications for the origin of eukaryotes. Proc Natl Acad Sci USA 86(17):6661–6665PubMedCrossRefPubMedCentralGoogle Scholar
  69. Golyshina OV, Toshchakov SV, Makarova KS et al (2017) ‘ARMAN’ archaea depend on association with euryarchaeal host in culture and in situ. Nat Commun 8(1):60PubMedPubMedCentralCrossRefGoogle Scholar
  70. Gould SB, Garg SG, Martin WF (2016) Bacterial vesicles secretion and the evolutionary origin of the eukaryotic endomembrane system. Trends Microbiol 24(7):525–534PubMedCrossRefPubMedCentralGoogle Scholar
  71. Gouy M, Li WH (1989) Phylogenetic analysis based on rRNA sequences supports the archaebacterial rather than the eocyte tree. Nature 339(6220):145–147PubMedCrossRefPubMedCentralGoogle Scholar
  72. Gouy M, Baurain D, Philippe H (2015) Rooting the tree of life: the phylogenetic jury is still out. Philos Trans R Soc Lond Ser B Biol Sci 370(1678):20140329CrossRefGoogle Scholar
  73. Gray MW, Doolittle WF (1982) Has the endosymbiont hypothesis been proven? Microbiol Rev 46(1):1–42PubMedPubMedCentralGoogle Scholar
  74. Gribaldo S, Cammarano P (1998) The root of the universal tree of life inferred from anciently duplicated genes encoding components of the protein-targeting machinery. J Mol Evol 47(5):508–516PubMedCrossRefPubMedCentralGoogle Scholar
  75. Gribaldo S, Philippe H (2002) Ancient phylogenetic relationships. Theor Popul Biol 61(4):391–408PubMedCrossRefPubMedCentralGoogle Scholar
  76. Gribaldo S, Poole AM, Daubin V et al (2010) The origin of eukaryotes and their relationship with the Archaea: are we at a phylogenomic impasse? Nat Rev Microbiol 8(10):743–752PubMedCrossRefPubMedCentralGoogle Scholar
  77. Grosjean H, Marck C, de Crécy-Lagard V (2007) The various strategies of codon decoding in organisms of the three domains of life: evolutionary implications. Nucleic Acids Symp Ser (Oxf) 51:15–16CrossRefGoogle Scholar
  78. Guy L, Ettema TJG (2011) The archaeal ‘TACK’ superphylum and the origin of eukaryotes. Trends Microbiol 19(12):580–587PubMedCrossRefPubMedCentralGoogle Scholar
  79. Harris JK, Kelley ST, Spiegelman GB, Pace NR (2003) The genetic core of the universal ancestor. Genome Res 13(3):407–412PubMedPubMedCentralCrossRefGoogle Scholar
  80. Hennig W (1966) Phylogenetic systematics. University of Illinois Press, Urbana, ILGoogle Scholar
  81. Hirt RP, Logsdon JM Jr, Healy B et al (1999) Microsporidia are related to Fungi: evidence from the largest subunit of RNA polymerase II and other proteins. Proc Natl Acad Sci USA 96(2):580–585PubMedCrossRefPubMedCentralGoogle Scholar
  82. House CH, Fitz-Gibbon ST (2002) Using homolog groups to create a whole-genomic tree of free-living organisms: an update. J Mol Evol 54(4):539–547PubMedCrossRefPubMedCentralGoogle Scholar
  83. Huelsenbeck JP, Larget B, Miller RE, Ronquist F (2002) Potential applications and pitfalls of Bayesian inference of phylogeny. Syst Biol 51(5):673–688CrossRefGoogle Scholar
  84. Huet J, Schnabel R, Sentenac A, Zillig W (1983) Archaebacteria and eukaryotes possess DNA-dependent RNA polymerases of a common type. EMBO J 2(8):1291–1294PubMedPubMedCentralCrossRefGoogle Scholar
  85. Hug LA, Baker BJ, Anantharaman K et al (2016) A new view of the tree of life. Nat Microbiol 1:16048PubMedCrossRefPubMedCentralGoogle Scholar
  86. Inagaki Y, Susko E, Fast NM et al (2004) Covarion shifts cause a long-branch attraction artifact that unites microsporidia and archaeabacteria in EF-1alpha phylogenies. Mol Biol Evol 21(7):1340–1349PubMedCrossRefPubMedCentralGoogle Scholar
  87. Iwabe N, Kuma K, Hasegawa M et al (1989) Evolutionary relationship of archaebacteria, eubacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes. Proc Natl Acad Sci USA 86(23):9355–9359PubMedCrossRefPubMedCentralGoogle Scholar
  88. Iwabe N, Kuma K, Kishino H et al (1991) Evolution of RNA polymerases and branching patterns of the three major groups of Archaeabacteria. J Mol Evol 32(1):70–78PubMedCrossRefPubMedCentralGoogle Scholar
  89. Kamaichi T, Hashimoto T, Nakamura Y et al (1996) Complete nucleotide sequences of the genes encoding translation elongation factors 1alpha and 2 from a microsporidian parasite, Glugea plecoglossi: implications for the deepest branching of eukaryotes. J Biochem 20(6):1095–1103CrossRefGoogle Scholar
  90. Keeling PJ, Doolittle WF (1996) Alpha-tubulin from early-diverging eukaryotic lineages and the evolution of the tubulin family. Mol Biol Evol 13(10):1297–1305PubMedCrossRefPubMedCentralGoogle Scholar
  91. Klenk HP, Zillig W (1994) DNA-dependent RNA polymerase subunit B as a tool for phylogenetic reconstructions: branching topology of the archaeal domain. J Mol Evol 38(4):420–432PubMedCrossRefPubMedCentralGoogle Scholar
  92. Klenk HP, Palm P, Zillig W (1991) A monophyletic holophyletic archaeal domain versus the ‘eocyte tree’. Trends Biochem Sci 16(8):288–290PubMedCrossRefPubMedCentralGoogle Scholar
  93. Knittel K, Lösekman T, Boetus A et al (2005) Diversity and distribution of methanotrophic archaea at cold seeps. Appl Environ Microbiol 71(1):467–479PubMedPubMedCentralCrossRefGoogle Scholar
  94. Koonin EV (2006) The origin of introns and their role in eukaryogenesis: a compromise solution to the introns-early versus introns-late debate? Biol Direct 1:22PubMedPubMedCentralCrossRefGoogle Scholar
  95. Koonin EV (2009) Darwinian evolution in the light of genomics. Nucleic Acids Res 37(4):1011–1034PubMedPubMedCentralCrossRefGoogle Scholar
  96. Koonin EV (2015) Archaeal ancestors of eukaryotes: not so elusive any more. BMC Biol 13:84PubMedPubMedCentralCrossRefGoogle Scholar
  97. Koonin EV, Dolja VV (2013) A virocentric perspective on the evolution of life. Curr Opin Virol 3(5):546–557PubMedPubMedCentralCrossRefGoogle Scholar
  98. Koonin EV, Dolja VV, Krupovic M (2015) Origins and evolution of viruses of eukaryotes: the ultimate modularity. Virology 479–480:2–25PubMedPubMedCentralCrossRefGoogle Scholar
  99. Kurland CG, Collins LJ, Penny D (2006) Genomics and the irreducible nature of eukaryote cells. Science 312(5776):1011–1014PubMedCrossRefPubMedCentralGoogle Scholar
  100. Lake JA (1987) A rate-independent technique for analysis of nucleic acid sequences: evolutionary parsimony. Mol Biol Evol 4(2):167–191PubMedPubMedCentralGoogle Scholar
  101. Lake JA (1988) Origin of the eukaryotic nucleus determined by rate-invariant analysis of rRNA sequences. Nature 331(6152):184–186PubMedCrossRefPubMedCentralGoogle Scholar
  102. Lake JA (1994) Reconstructing evolutionary trees from DNA and protein sequences: paralinear distances. Proc Natl Acad Sci USA 91(4):1455–1459PubMedCrossRefPubMedCentralGoogle Scholar
  103. Lake JA, Henderson E, Oakes M, Clark MW (1984) Eocytes: a new ribosome structure indicates a kingdom with a close relationship to eukaryotes. Proc Natl Acad Sci USA 81(12):3786–3790PubMedCrossRefPubMedCentralGoogle Scholar
  104. Lane N, Martin W (2010) The energetics of genome complexity. Nature 467(7318):929–934PubMedCrossRefPubMedCentralGoogle Scholar
  105. Lane N, Martin WF (2015) Eukaryotes really are special, and mitochondria are why. Proc Natl Acad Sci USA 112(35):E4823PubMedCrossRefPubMedCentralGoogle Scholar
  106. Lartillot N, Philippe H (2004) A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. Mol Biol Evol 21(6):1095–1109PubMedCrossRefPubMedCentralGoogle Scholar
  107. Lartillot N, Brinkmann H, Philippe H (2007) Suppression of long-branch attraction artefacts in the animal phylogeny using a site-heterogeneous model. BMC Evol Biol 7(Suppl 1):S4PubMedPubMedCentralCrossRefGoogle Scholar
  108. Lasek-Nesselquist E, Gogarten JP (2013) The effects of model choice and mitigating bias on the ribosomal tree of life. Mol Phylogenet Evol 69(1):17–38PubMedCrossRefPubMedCentralGoogle Scholar
  109. Lasken RS, Stockwell TB (2007) Mechanism of chimera formation during the multiple displacement amplification reaction. BMC Biotechnol 7:19PubMedPubMedCentralCrossRefGoogle Scholar
  110. Le SQ, Gascuel O (2008) An improved general amino acid replacement matrix. Mol Biol Evol 25(7):1307–1320PubMedCrossRefPubMedCentralGoogle Scholar
  111. Lecompte O, Ripp R, Thierry JC et al (2002) Comparative analysis of ribosomal proteins in complete genomes: an exemple of reductive evolution at the domain scale. Nucleic Acids Res 30(24):5382–5390PubMedPubMedCentralCrossRefGoogle Scholar
  112. Leipe DD, Araving L, Koonin EV (1999) Did DNA replication evolve twice independently? Nucleic Acids Res 27(17):3389–3401PubMedPubMedCentralCrossRefGoogle Scholar
  113. Li S (1996) Phylogenetic tree construction using Markov chain Monte Carlo. PhD dissertation, Ohio State UniversityGoogle Scholar
  114. Linkkila TP, Gogarten JP (1991) Tracing origins with molecular sequences: rooting the universal tree of life. Trends Biochem Sci 16(8):287–288PubMedCrossRefPubMedCentralGoogle Scholar
  115. López-García P, Moreira D (2006) Selective forces for the origin of the eukaryotic nucleus. BioEssays 28(5):525–533PubMedCrossRefPubMedCentralGoogle Scholar
  116. López-García P, Moreira D (2015) Open questions on the origin of Eukaryotes. Trends Ecol Evol 30(11):697–708PubMedPubMedCentralCrossRefGoogle Scholar
  117. López-García P, Eme L, Moreira D (2017) Symbiosis in eukaryotic evolution. J Theor Biol 434:20–33PubMedCrossRefPubMedCentralGoogle Scholar
  118. Martijn J, Ettema TJ (2013) From archeon to eukaryote: the evolutionary dark ages of the eukaryotic cell. Biochem Soc Trans 41(1):451–457PubMedCrossRefPubMedCentralGoogle Scholar
  119. Martin W, Kowallik KV (1999) Annotated English translation of Mereschkowsky’s 1905 paper “Über Natur und Ursprung der Chromatophoren im Pflanzenreiche”. Eur J Phycol 34:287–295Google Scholar
  120. Matte-Taillez O, Brochier C, Forterre P, Philippe H (2002) Archaeal phylogeny based on ribosomal proteins. Mol Biol Evol 19(5):631–639CrossRefGoogle Scholar
  121. Mereschkowski C (1905) Über Natur und Ursprung der Chromatophoren im Pflanzenreiche. Biol Centralbl 25:593–604Google Scholar
  122. Mereschkowski K (1910) Theorie der zwei Plasmaarten als Grundlage der Symbiogenesis, einer neuen Lehre von der Ent-stehung der Organismen. Biol Centralbl 30:353–367Google Scholar
  123. Michener CD, Sokal RR (1957) A quantitative approach to a problem in classification. Evolution 11(2):130–162CrossRefGoogle Scholar
  124. Moreira D, López-García P (2009) Ten reasons to exclude viruses from the tree of life. Nat Rev Microbiol 7(4):306–311PubMedCrossRefPubMedCentralGoogle Scholar
  125. Moreira D, López-García P (2015) Evolution of viruses and cells: do we need a fourth domain of life to explain the origin of eukaryotes? Philos Trans R Soc Lond Ser B Biol Sci 370(1678):20140327CrossRefGoogle Scholar
  126. Mulkidjanian AY, Makarova KS, Galperin MY, Koonin EV (2007) Inventing the dynamo machine: the evolution of the F-type and V-type ATPases. Nat Rev Microbiol 5(11):892–899PubMedCrossRefPubMedCentralGoogle Scholar
  127. Nasir A, Kim KM, Caetano-Anollés G (2015) Lokiarchaeota: eukaryote-like missing links from microbial dark matter? Trends Microbiol 23(8):448–450PubMedCrossRefPubMedCentralGoogle Scholar
  128. Nasir A, Kim KM, Da Cunha V, Caetano-Anollés G (2016) Arguments reinforcing the three-domain view of diversified cellular life. Archaea 2016:1851865PubMedPubMedCentralCrossRefGoogle Scholar
  129. Nurk S, Bankevich A, Antipov D et al (2013) Assembling single-cell genomes and mini-metagenomes from chimeric MDA products. J Comput Biol 20(10):714–737PubMedPubMedCentralCrossRefGoogle Scholar
  130. Olsen GJ, Woese CR (1989) A brief note concerning archaebacterial phylogeny. Can J Microbiol 35(1):119–123PubMedCrossRefPubMedCentralGoogle Scholar
  131. Olsen GJ, Woese CR (1997) Archaeal genomics: an overview. Cell 89(7):991–994CrossRefGoogle Scholar
  132. Pace NR, Olsen GJ, Woese CR (1986) Ribosomal RNA phylogeny and the primary lines of evolutionary descent. Cell 45(3):325–326PubMedCrossRefPubMedCentralGoogle Scholar
  133. Parks DH, Imelfort M, Skennerton CT et al (2015) CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 25(7):1043–1055PubMedPubMedCentralCrossRefGoogle Scholar
  134. Parks DH, Rinke C, Chuvochina M et al (2017) Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life. Nat Microbiol 2(11):1533–1542PubMedCrossRefPubMedCentralGoogle Scholar
  135. Penny D, Hoeppner MP, Poole AM, Jeffares DC (2009) An overview of the introns-first theory. J Mol Evol 69(5):527–540PubMedCrossRefGoogle Scholar
  136. Petitjean C, Deschamps P, López-García P, Moreira D (2014) Rooting the domain archaea by phylogenomic analysis supports the foundation of the new kingdom Proteoarchaeota. Genome Biol Evol 7(1):191–204PubMedPubMedCentralCrossRefGoogle Scholar
  137. Philippe H, Forterre P (1999) The rooting of the universal tree of life is not reliable. J Mol Evol 49(4):509–523PubMedCrossRefPubMedCentralGoogle Scholar
  138. Philippe H, Germot A (2000) Phylogeny of eukaryotes based on ribosomal RNA: long-branch attraction and models of sequence evolution. Mol Biol Evol 17(5):830–834PubMedCrossRefGoogle Scholar
  139. Philippe H, Germot A, Moreira A (2000a) The new phylogeny of eukaryotes. Curr Opin Genet Dev 10(6):596–601PubMedCrossRefGoogle Scholar
  140. Philippe H, Lopez P, Brinkmann H et al (2000b) Early-branching or fast-evolving eukaryotes? An answer based on slowly evolving positions. Proc Biol Sci 267(1449):1213–1221PubMedPubMedCentralCrossRefGoogle Scholar
  141. Pisani D, Cotton JA, McInerney JO (2007) Supertrees disentangle the chimerical origin of eukaryotic genomes. Mol Biol Evol 24(8):1752–1760PubMedCrossRefPubMedCentralGoogle Scholar
  142. Pittis AA, Gabaldón T (2016) Late acquisition of mitochondria by a host with chimaeric prokaryotic ancestry. Nature 531(7592):101–104PubMedPubMedCentralCrossRefGoogle Scholar
  143. Poole AM (2009) Horizontal gene transfer and the earliest stages of the evolution of life. Res Microbiol 160(7):473–480PubMedCrossRefPubMedCentralGoogle Scholar
  144. Poole A, Penny D (2001) Does endo-symbiosis explain the origin of the nucleus? Nat Cell Biol 3(8):E173–E174PubMedCrossRefPubMedCentralGoogle Scholar
  145. Prangishvili D (2013) The wonderful world of archaeal viruses. Annu Rev Microbiol 67:565–585PubMedCrossRefPubMedCentralGoogle Scholar
  146. Pühler G, Leffers H, Gropp G et al (1989) Archaeabacterial DNA-dependent RNA polymerases testify to the evolution of the eukaryotic nuclear genome. Proc Natl Acad Sci USA 86(12):4569–4573PubMedCrossRefPubMedCentralGoogle Scholar
  147. Raoult D (2010) The post-Darwinian rhizome of life. Lancet 375(9709):104–105PubMedCrossRefPubMedCentralGoogle Scholar
  148. Raoult D, Forterre P (2008) Redefining viruses: lessons from Mimivirus. Nat Rev Microbiol 6(4):315–319PubMedCrossRefPubMedCentralGoogle Scholar
  149. Raymann K, Brochier-Armanet C, Gribaldo S (2015) The two-domain tree of life is linked to a new root for the Archaea. Proc Natl Acad Sci USA 112(21):6670–6675PubMedCrossRefPubMedCentralGoogle Scholar
  150. Rinke C, Schwientek P, Sczyrba A et al (2013) Insights into the phylogeny and coding potential of microbial dark matter. Nature 499(7459):431–437PubMedCrossRefPubMedCentralGoogle Scholar
  151. Rivera MC, Lake JA (2004) The ring of life provides evidence for a genome fusion origin of eukaryotes. Nature 431(7005):152–155PubMedCrossRefPubMedCentralGoogle Scholar
  152. Rochette NC, Brochier-Armanet C, Gouy M (2014) Phylogenomic test of the hypotheses for the evolutionary origin of eukaryotes. Mol Biol Evol 31(4):832–845PubMedPubMedCentralCrossRefGoogle Scholar
  153. Sagan L (1967) On the origin of mitosing cells. J Theor Biol 14(3):255–274PubMedCrossRefPubMedCentralGoogle Scholar
  154. Sanger F, Brownlee GG, Barrell BG (1965) A two-dimensional fractionation procedure for radioactive nucleotides. J Mol Biol 13(2):373–398PubMedCrossRefPubMedCentralGoogle Scholar
  155. Sapp J, Fox GE (2013) The singular quest for a universal tree of life. Microbiol Mol Biol Rev 77(4):541–550PubMedPubMedCentralCrossRefGoogle Scholar
  156. Schulz F, Eloe-Fadrosh EA, Bowers RM et al (2017) Towards a balanced view of the bacterial tree of life. Microbiome 5(1):140PubMedPubMedCentralCrossRefGoogle Scholar
  157. Seitz KW, Lazar CS, Hinrichs KU et al (2016) Genomic reconstruction of a novel, deeply branched sediment archaeal phylum with pathways for acetogenesis and sulfur reduction. ISME J 10(7):1696–1705PubMedPubMedCentralCrossRefGoogle Scholar
  158. Sharma V, Colson P, Giorgi R et al (2014) DNA-dependent RNA polymerase detects hidden giant viruses in published databanks. Genome Biol Evol 6(7):1603–1610PubMedPubMedCentralCrossRefGoogle Scholar
  159. Sharma V, Colson P, Chabrol O et al (2015a) Welcome to pandoraviruses at the ‘Fourth TRUC’ club. Front Microbiol 6:423PubMedPubMedCentralGoogle Scholar
  160. Sharma V, Colson P, Chabrol O et al (2015b) Pithovirus sibericus, a new bona fide member of the ‘Fourth TRUC’ club. Front Microbiol 6:722PubMedPubMedCentralGoogle Scholar
  161. Sousa FL, Neukirchen S, Allen JF et al (2016) Lokiarchaeon is hydrogen dependent. Nat Microbiol 1:16034PubMedCrossRefGoogle Scholar
  162. Spang A, Hatzenpichler R, Brochier-Armanet C et al (2010) Distinct gene set in two different lineages of ammonia-oxidizing archaea supports the phylum Thaumarchaeota. Trends Microbiol 18(8):331–340PubMedCrossRefGoogle Scholar
  163. Spang A, Saw JH, Jørgensen S et al (2015) Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521(7551):173–179PubMedPubMedCentralCrossRefGoogle Scholar
  164. Spang A, Caceres EF, Ettema TJG (2017) Genomic exploration of the diversity, ecology, and evolution of the archaeal domain of life. Science 357(6351):eaaf3883PubMedCrossRefPubMedCentralGoogle Scholar
  165. Spang A, Eme L, Saw JH et al (2018) Asgard archaea are the closest prokaryotic relatives of eukaryotes. PLoS Genet 14(3):e1007080PubMedPubMedCentralCrossRefGoogle Scholar
  166. Stanier RY, Van Niel CB (1962) The concept of a Bacterium. Arch Mikrobiol 42:17–35PubMedCrossRefGoogle Scholar
  167. Stetter KO (1989) Extremely thermophilic chemolithoautotrophic archaebacteria. In: Schlegel HG, Brown B (eds) Autotrophic bacteria. Science Tech Publishers and Springer, Berlin, pp 167–171Google Scholar
  168. Stetter KO (2013) A brief history of the discovery of hyperthermophilic life. Biochem Soc Trans 41(1):416–420PubMedCrossRefPubMedCentralGoogle Scholar
  169. Stöffler-Meilicke M, Böhme C, Strobel O et al (1986) Structure of ribosomal subunits of M. vannielii: ribosomal morphology as a phylogenetic marker. Science 231(4743):1306–1308PubMedCrossRefPubMedCentralGoogle Scholar
  170. Swofford DL, Waddell PJ, Huelsenbeck JP et al (2001) Bias in phylogenetic estimation and its relevance to the choice between parsimony and likelihood methods. Syst Biol 50(4):525–539PubMedCrossRefGoogle Scholar
  171. Takemura M (2001) Poxviruses and the origin of the eukaryotic nucleus. J Mol Evol 52:419–425PubMedCrossRefPubMedCentralGoogle Scholar
  172. Tavare S (1986) Some probabilistic and statistical problems on the analysis of DNA sequences? Lect Math Life Sci 17(2):57–86Google Scholar
  173. Tornabene TG, Langworthy TA (1979) Diphytanyl and dibiphytanyl glycerol ether lipids of methanogenic archaeabacteria. Science 203(4375):51–53PubMedCrossRefGoogle Scholar
  174. Urbonavicius J, Auxilien S, Walbott H et al (2008) Acquisition of a bacterial RumA-type tRNA(uracil-54,C5)-methyltransferase by Archaea through an ancient horizontal gene transfer. Mol Microbiol 67(2):323–335PubMedCrossRefGoogle Scholar
  175. Vossbrinck CR, Maddox JV, Friedman S et al (1987) Ribosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes. Nature 326(6111):411–414PubMedCrossRefGoogle Scholar
  176. Wallace DC, Morowitz HJ (1973) Genome size and evolution. Chromosoma 40:121–122PubMedCrossRefGoogle Scholar
  177. Werner F, Grohmann D (2011) Evolution of multisubunit RNA polymerases in the three domains of life. Nat Rev Microbiol 9(2):85–98CrossRefGoogle Scholar
  178. Williams TA, Embley TM, Heinz E (2011) Informational gene phylogenies do not support a fourth domain of life for nucleocytoplasmic large DNA viruses. PLoS One 6(6):e21080PubMedPubMedCentralCrossRefGoogle Scholar
  179. Williams TA, Foster PG, Nye TM et al (2012) A congruent phylogenomic signal places eukaryotes within the Archaea. Proc Biol Sci 279(1749):4870–4879PubMedPubMedCentralCrossRefGoogle Scholar
  180. Williams TA, Foster PG, Cox CJ, Embley TM (2013) An archaeal origin of eukaryotes supports only two primary domains of life. Nature 504(7479):231–236PubMedCrossRefPubMedCentralGoogle Scholar
  181. Williams TA, Szöllősi GJ, Spang A et al (2017) Integrative modeling of gene and genome evolution roots the archaeal tree of life. Proc Natl Acad Sci USA 114(23):E4602–E4611PubMedCrossRefPubMedCentralGoogle Scholar
  182. Woese CR (1979) A proposal concerning the origin of life on the planet earth. J Mol Evol 13(2):95–101PubMedCrossRefPubMedCentralGoogle Scholar
  183. Woese CR (1987) Bacterial evolution. Microbiol Rev 51(2):221–271PubMedPubMedCentralGoogle Scholar
  184. Woese CR (1998) The universal ancestor. Proc Natl Acad Sci USA 95(12):6854–6859PubMedCrossRefPubMedCentralGoogle Scholar
  185. Woese CR (2000) Interpreting the universal phylogenetic tree. Proc Natl Acad Sci USA 97(15):8392–8396PubMedCrossRefPubMedCentralGoogle Scholar
  186. Woese CR (2002) On the evolution of cells. Proc Natl Acad Sci USA 99(13):8742–8747PubMedCrossRefPubMedCentralGoogle Scholar
  187. Woese CR, Fox GE (1977a) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci USA 74(11):5088–5090PubMedCrossRefPubMedCentralGoogle Scholar
  188. Woese CR, Fox GE (1977b) The concept of cellular evolution. J Mol Evol 10(1):1–6PubMedCrossRefPubMedCentralGoogle Scholar
  189. Woese CR, Maniloff J, Zablen LB (1980) Phylogenetic analysis of the mycoplasmas. Proc Natl Acad Sci USA 77(1):494–498PubMedCrossRefPubMedCentralGoogle Scholar
  190. Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA 87(12):4576–4579PubMedCrossRefPubMedCentralGoogle Scholar
  191. Wolf YI, Rogozin IB, Grishin NV, Koonin EV (2002) Genome trees and the tree of life. Trends Genet 18(9):472–479PubMedCrossRefPubMedCentralGoogle Scholar
  192. Wolf YI, Makarova KS, Yutin N, Koonin EV (2012) Updated clusters of orthologous genes for Archaea: a complex ancestor of the Archaea and the byways of horizontal gene transfer. Biol Direct 7:46PubMedPubMedCentralCrossRefGoogle Scholar
  193. Yang Z, Rannala B (2012) Molecular phylogenetics: principles and practice. Nat Rev Microbiol 13(5):303–314CrossRefGoogle Scholar
  194. Yang D, Oyaizu Y, Oyaizu H et al (1985) Mitochondrial origins. Proc Natl Acad Sci USA 82(13):4443–4447PubMedCrossRefPubMedCentralGoogle Scholar
  195. Yutin N, Makarova KS, Mekhedov SL et al (2008) The deep archaeal roots of eukaryotes. Mol Biol Evol 25(8):1619–1630PubMedPubMedCentralCrossRefGoogle Scholar
  196. Zablen LB, Kissil MS, Woese CR, Buetow DE (1975) Phylogenetic origin of the chloroplast and prokaryotic nature of its ribosomal RNA. Proc Natl Acad Sci USA 72(6):2418–2422PubMedCrossRefPubMedCentralGoogle Scholar
  197. Zaremba-Niedzwiedzka K, Caceres EF, Saw JH et al (2017) Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature 541(7637):353–358PubMedCrossRefPubMedCentralGoogle Scholar
  198. Zillig W, Stetter KO, Janeković D (1979) DNA-dependent RNA polymerase from the archaebacterium Sulfolobus acidocaldarius. Eur J Biochem 96(3):596–604CrossRefGoogle Scholar
  199. Zillig W, Prangishvili D, Schleper C et al (1996) Viruses, plasmids and other genetic elements of thermophilic and hyperthermophilic Archaea. FEMS Microbiol Rev 18(2–3):225–236PubMedCrossRefPubMedCentralGoogle Scholar
  200. Zuckerkandl E, Pauling L (1965) Molecules as documents of evolutionary history. J Theor Biol 8(2):357–366PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Morgan Gaia
    • 1
  • Violette Da Cunha
    • 1
    • 2
  • Patrick Forterre
    • 1
    • 2
    Email author
  1. 1.Département de MicrobiologieInstitut Pasteur, Unité de Biologie Moléculaire du Gène chez les Extrêmophiles (BMGE)ParisFrance
  2. 2.Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Univ. Paris-Sud, Univ. Paris-SaclayGif-sur-YvetteFrance

Personalised recommendations