The hybrid nature of the Eukaryota and a consilient view of life on Earth

Journal name:
Nature Reviews Microbiology
Volume:
12,
Pages:
449–455
Year published:
DOI:
doi:10.1038/nrmicro3271
Published online

Abstract

The origin of the eukaryotic cell, which is known as eukaryogenesis, has puzzled scientists for more than 100 years, and many hypotheses have been proposed. Recent analyses of new data enable the safe elimination of some of these hypotheses, whereas support for other hypotheses has increased. In this Opinion article, we evaluate the available theories for their compatibility with empirical observations and conclude that cellular life consists of two primary, paraphyletic prokaryotic groups and one secondary, monophyletic group that has symbiogenic origins — the eukaryotes.

At a glance

Figures

  1. Competing scenarios for the origin of the eukaryotes and the highest-level structure for describing the diversity of cellular life.
    Figure 1: Competing scenarios for the origin of the eukaryotes and the highest-level structure for describing the diversity of cellular life.

    a | The 'three-domains' phylogenetic tree, which is also known as the three-domains tree of life. b | The 'eukaryotes-early' hypothesis implies that prokaryotes are derived from a eukaryotic ancestor. c | The Eocyte hypothesis postulates that eukaryotes are derived from a lineage of the Archaebacteria that post-dates the diversification of the Archaebacteria. d | The 'ring of life' hypothesis postulates that eukaryotes arose from two lineages of prokaryotes, one of which was archaebacterial and one of which was eubacterial, and consequently, it is the only monophyletic group, although with symbiogenic origins. The ring of life hypothesis also implies that eukaryotes are late to arise and are a secondary grouping of life, whereas the two prokaryote groups are primary groupings.

  2. The ring of life hypothesis.
    Figure 2: The ring of life hypothesis.

    Schematic representation of the flow of genetic material from the two major prokaryotic groups into the base of the eukaryotes and the separate flow of genetic material from cyanobacteria into plastid-containing eukaryotes.

References

  1. Martin, W. & Kowallik, K. Annotated English translation of Mereschkowsky's 1905 paper 'Über Natur und Ursprung der Chromatophoren imvPflanzenreiche'. Eur. J. Phycol. 34, 287295 (1999).
  2. Wallin, I. E. The mitochondria problem. Am. Naturalist 57, 255261 (1923).
  3. Alvarez-Ponce, D., Bapteste, E., Lopez, P. & McInerney, J. O. Gene similarity networks provide new tools for understanding eukaryote origins and evolution. Proc. Natl Acad. Sci. USA 110, E1594E1603 (2013).
  4. Esser, C. et al. A genome phylogeny for mitochondria among α-proteobacteria and a predominantly eubacterial ancestry of yeast nuclear genes. Mol. Biol. Evol. 21, 16431660 (2004).
  5. Kurland, C. G., Collins, L. J. & Penny, D. Genomics and the irreducible nature of eukaryote cells. Science 312, 10111014 (2006).
  6. Lane, N. & Martin, W. The energetics of genome complexity. Nature 467, 929934 (2010).
  7. López-García, P. & Moreira, D. Selective forces for the origin of the eukaryotic nucleus. Bioessays 28, 525533 (2006).
  8. Pisani, D., Cotton, J. A. & McInerney, J. O. Supertrees disentangle the chimerical origin of eukaryotic genomes. Mol. Biol. Evol. 24, 17521760 (2007).
  9. Rivera, M. C. & Lake, J. A. The ring of life provides evidence for a genome fusion origin of eukaryotes. Nature 431, 152155 (2004).
  10. Stechmann, A. & Cavalier-Smith, T. The root of the eukaryote tree pinpointed. Curr. Biol. 13, 665666 (2003).
  11. Popper, K. R. The Logic of Scientific Discovery (Routledge, 1959).
  12. Whewell, W. The Philosophy Of Inductive Sciences, Founded Upon Their History (John W. Parker, 1840).
  13. 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, 231236 (2013).
  14. Fitzpatrick, D. A., Creevey, C. J. & McInerney, J. O. Genome phylogenies indicate a meaningful α-proteobacterial phylogeny and support a grouping of the mitochondria with the Rickettsiales. Mol. Biol. Evol. 23, 7485 (2006).
  15. Margulis, L. Archaeal–eubacterial mergers in the origin of Eukarya: phylogenetic classification of life. Proc. Natl Acad. Sci. USA 93, 10711076 (1996).
  16. Rinke, C., Schwientek, P., Sczyrba, A. & Ivanova, N. N. Insights into the phylogeny and coding potential of microbial dark matter. Nature 499, 431437 (2013).
  17. 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, 466485 (2012).
  18. Cavalier-Smith, T. The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int. J. Syst. Evol. Microbiol. 52, 297354 (2002).
  19. Devos, D. P. & Reynaud, E. G. Evolution. Intermediate steps. Science 330, 11871188 (2010).
  20. Martin, W. & Müller, M. The hydrogen hypothesis for the first eukaryote. Nature 392, 3741 (1998).
  21. Searcy, D. G. Metabolic integration during the evolutionary origin of mitochondria. Cell Res. 13, 229238 (2003).
  22. Yang, D., Oyaizu, Y., Oyaizu, H., Olsen, G. J. & Woese, C. R. Mitochondrial origins. Proc. Natl Acad. Sci. USA 82, 44434447 (1985).
  23. McInerney, J. O. et al. Planctomycetes and eukaryotes: a case of analogy not homology. Bioessays 33, 810817 (2011).
  24. Hirt, R. P. et al. Microsporidia are related to Fungi: evidence from the largest subunit of RNA polymerase II and other proteins. Proc. Natl Acad. Sci. USA 96, 580585 (1999).
  25. Roger, A. J. et al. A mitochondrial-like chaperonin 60 gene in Giardia lamblia: evidence that diplomonads once harbored an endosymbiont related to the progenitor of mitochondria. Proc. Natl Acad. Sci. USA 95, 229234 (1998).
  26. Rodriguez-Ezpeleta, N. & Embley, T. M. The SAR11 group of α-proteobacteria is not related to the origin of mitochondria. PLOS ONE 7, e30520 (2012).
  27. Woese, C. R. Bacterial evolution. Microbiol. Rev. 51, 221 (1987).
  28. Bapteste, E. et al. Evolutionary analyses of non-genealogical bonds produced by introgressive descent. Proc. Natl Acad. Sci. USA 109, 1826618272 (2012).
  29. Gogarten, J. P. et al. Evolution of the vacuolar H+-ATPase: implications for the origin of eukaryotes. Proc. Natl Acad. Sci. USA 86, 66616665 (1989).
  30. Brinkmann, H. & Philippe, H. Archaea sister group of Bacteria? Indications from tree reconstruction artifacts in ancient phylogenies. Mol. Biol. Evol. 16, 817825 (1999).
  31. Forterre, P. The origin of DNA genomes and DNA replication proteins. Curr. Opin. Microbiol. 5, 525532 (2002).
  32. Van Valen, L. M. & Maiorana, V. C. The archaebacteria and eukaryotic origins. Nature 287, 248250 (1980).
  33. de Duve, C. The origin of eukaryotes: a reappraisal. Nature Rev. Genet. 8, 395403 (2007).
  34. Cotton, J. A. & McInerney, J. O. Eukaryotic genes of archaebacterial origin are more important than the more numerous eubacterial genes, irrespective of function. Proc. Natl Acad. Sci. USA 107, 1725217255 (2010).
  35. Margulis, L., Bermudes, D. & Obar, R. Symbiosis in evolution: status of the hypothesis of the spirochete origin of undulipodia. Orig. Life Evol. Biosph. 16, 319 (1986).
  36. Lake, J. A., Henderson, E., Oakes, M. & Clark, M. W. Eocytes: a new ribosome structure indicates a kingdom with a close relationship to eukaryotes. Proc. Natl Acad. Sci. USA 81, 37863790 (1984).
  37. Williams, T. A., Foster, P. G., Nye, T. M. W., Cox, C. J. & Embley, T. M. A congruent phylogenomic signal places eukaryotes within the Archaea. Proc. Biol. Sci. 279, 48704879 (2012).
  38. Lake, J. A., Servin, J. A., Herbold, C. W. & Skophammer, R. G. Evidence for a new root of the tree of life. Systemat. Biol. 57, 835843 (2008).
  39. Dagan, T., Roettger, M., Bryant, D. & Martin, W. Genome networks root the tree of life between prokaryotic domains. Genome Biol. Evol. 2, 379392 (2010).
  40. Ciccarelli, F. D. et al. Toward automatic reconstruction of a highly resolved tree of life. Science 311, 12831287 (2006).
  41. Lasek-Nesselquist, E. & Gogarten, J. P. The effects of model choice and mitigating bias on the ribosomal tree of life. Mol. Phylogenet. Evol. 69, 1738 (2013).
  42. Creevey, C. J., Doerks, T., Fitzpatrick, D. A., Raes, J. & Bork, P. Universally distributed single-copy genes indicate a constant rate of horizontal transfer. PLOS ONE 6, e22099 (2011).
  43. Dagan, T. & Martin, W. The tree of one percent. Genome Biol. 7, 118 (2006).
  44. Gouy, M. & Li, W. H. Phylogenetic analysis based on rRNA sequences supports the archaebacterial rather than the eocyte tree. Nature 339, 145147 (1989).
  45. Tourasse, N. J. & Gouy, M. Accounting for evolutionary rate variation among sequence sites consistently changes universal phylogenies deduced from rRNA and protein-coding genes. Mol. Phylogenet. Evol. 13, 159168 (1999).
  46. 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, 743752 (2010).
  47. Williams, T. A. & Embley, T. M. Archaeal “dark matter” and the origin of eukaryotes. Genome Biol. Evol. 6, 474481 (2014).
  48. 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, 4576 (1990).
  49. Baldauf, S. L., Palmer, J. D. & Doolittle, W. F. The root of the universal tree and the origin of eukaryotes based on elongation factor phylogeny. Proc. Natl Acad. Sci. USA 93, 77497754 (1996).
  50. Keane, T. M., Creevey, C. J., Pentony, M. M., Naughton, T. J. & McLnerney, J. O. Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol. Biol. 6, 29 (2006).
  51. Cox, C., Foster, P., Hirt, R. & Harris, S. The archaebacterial origin of eukaryotes. Proc. Natl Acad. Sci. USA 105, 2035620361 (2008).
  52. 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 Biol. Sci. 364, 21972207 (2009).
  53. Foster, P. G. Modeling compositional heterogeneity. Syst. Biol. 53, 485495 (2004).
  54. Lartillot, N., Lepage, T. & Blanquart, S. PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 25, 22862288 (2009).
  55. Guy, L. & Ettema, T. J. The archaeal 'TACK' superphylum and the origin of eukaryotes. Trends Microbiol. 19, 580587 (2011).
  56. Stamatakis, A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 26882690 (2006).
  57. 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, 731741 (2010).
  58. Mojzsis, S. J. et al. Evidence for life on Earth before 3,800 million years ago. Nature 384, 5559 (1996).
  59. Wacey, D., Kilburn, M. R., Saunders, M., Cliff, J. & Brasier, M. D. Microfossils of sulphur-metabolizing cells in 3.4-billion-year-old rocks of Western Australia. Nature Geosci. 4, 698702 (2011).
  60. Knoll, A. H., Javaux, E. J., Hewitt, D. & Cohen, P. Eukaryotic organisms in Proterozoic oceans. Phil. Trans. R. Soc. Lond. B Biol. Sci. 361, 1023 (2006).
  61. Brocks, J. J., Logan, G. A., Buick, R. & Summons, R. E. Archean molecular fossils and the early rise of eukaryotes. Science 285, 10331036 (1999).
  62. Knoll, A. H. Paleobiological perspectives on early eukaryotic evolution. Cold Spring Harb. Perspect. Biol. 6, a016113.
  63. Rasmussen, B., Fletcher, I. R., Brocks, J. J. & Kilburn, M. R. Reassessing the first appearance of eukaryotes and cyanobacteria. Nature 455, 11011104 (2008).
  64. Brocks, J. J. & Banfield, J. Unravelling ancient microbial history with community proteogenomics and lipid geochemistry. Nature Rev. Microbiol. 7, 601609 (2009).
  65. Parfrey, L. W., Lahr, D. J. G., Knoll, A. H. & Katz, L. A. Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc. Natl Acad. Sci. USA 108, 1362413629 (2011).
  66. Shih, P. M. & Matzke, N. J. Primary endosymbiosis events date to the later Proterozoic with cross-calibrated phylogenetic dating of duplicated ATPase proteins. Proc. Natl Acad. Sci. USA 110, 1235512360 (2013).
  67. Timmis, J. N., Ayliffe, M. A., Huang, C. Y. & Martin, W. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nature Rev. Genet. 5, 123135 (2004).
  68. Lynch, M. & Conery, J. S. The origins of genome complexity. Science 302, 14011404 (2003).
  69. Jain, R., Rivera, M. C. & Lake, J. A. Horizontal gene transfer among genomes: the complexity hypothesis. Proc. Natl Acad. Sci. USA 96, 3801 (1999).
  70. Alvarez-Ponce, D. & McInerney, J. O. The human genome retains relics of its prokaryotic ancestry: human genes of archaebacterial and eubacterial origin exhibit remarkable differences. Genome Biol. Evol. 3, 782790 (2011).
  71. Poole, A. M. & Penny, D. Evaluating hypotheses for the origin of eukaryotes. Bioessays 29, 7484 (2007).
  72. Naor, A. & Gophna, U. Cell fusion and hybrids in Archaea: prospects for genome shuffling and accelerated strain development for biotechnology. Bioengineered 4, 126129 (2013).
  73. Naor, A., Lapierre, P., Mevarech, M., Papke, R. T. & Gophna, U. Low species barriers in halophilic archaea and the formation of recombinant hybrids. Curr. Biol. 22, 14441448 (2012).
  74. Wachtershauser, G. From pre-cells to Eukarya — a tale of two lipids. Mol. Microbiol. 47, 1322 (2003).
  75. Shimada, H. & Yamagishi, A. Stability of heterochiral hybrid membrane made of bacterial sn-G3P lipids and archaeal sn-G1P lipids. Biochemistry 50, 41144120 (2011).
  76. Yutin, N., Wolf, M. Y., Wolf, Y. I. & Koonin, E. V. The origins of phagocytosis and eukaryogenesis. Biol. Direct 4, 9 (2009).
  77. Nelson-Sathi, S. et al. Acquisition of 1,000 eubacterial genes physiologically transformed a methanogen at the origin of Haloarchaea. Proc. Natl Acad. Sci. USA 109, 2053720542 (2012).
  78. Lake, J. A. Evidence for an early prokaryotic endosymbiosis. Nature 460, 967971 (2009).
  79. Beiko, R. G., Harlow, T. J. & Ragan, M. A. Highways of gene sharing in prokaryotes. Proc. Natl Acad. Sci. USA 102, 14332 (2005).
  80. Muller, M. et al. Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol. Mol. Biol. Rev. 76, 444495 (2012).
  81. Moran, N. A. Microbial minimalism: genome reduction in bacterial pathogens. Cell 108, 583586 (2002).
  82. Forterre, P. 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, 36693674 (2006).
  83. Forterre, P. The origin of viruses and their possible roles in major evolutionary transitions. Virus Res. 117, 516 (2006).

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Author information

Affiliations

  1. Bioinformatics and Molecular Evolution Unit, Department of Biology, National University of Ireland, Maynooth, County Kildare, Ireland.

    • James O. McInerney
  2. Bioinformatics and Molecular Evolution Group, School of Biotechnology, Dublin City University, Glasnevin, Dublin 9, Ireland.

    • Mary J. O'Connell
  3. School of Biological Sciences and School of Earth Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK.

    • Davide Pisani

Competing interests statement

The authors declare no competing interests.

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Author details

  • James O. McInerney

    James O. McInerney is a professor of evolutionary biology at the National University of Ireland Maynooth. He studies a broad range of evolutionary biology topics, including introgressive processes, such as lateral gene transfer, gene and genome remodelling, and symbiogenesis. His research group has developed several computer programs in the area of molecular evolution. James O. McInerney's Homepage.

  • Mary J. O'Connell

    Mary J. O'Connell is a bioinformatics and molecular evolutionary biology faculty member at the School of Biotechnology, Dublin City University, Ireland. She received her Ph.D. in 2005 from the National University of Ireland Maynooth, Ireland. Her laboratory work on the development and application of molecular evolutionary theory for understanding the evolution of mammal genomes and disease and early eukaryotic life. Her research has been funded by Science Foundation Ireland Research Frontiers Program (EOB2673) and the Fulbright Commission. Mary J. O'Connell's Homepage.

  • Davide Pisani

    Davide Pisani obtained his primary degree at the University of Parma, Italy, where he studied Natural Sciences. He than obtained his Ph.D. at the University of Bristol, UK. His work focuses on understanding key evolutionary transitions that happened in deep times, using genomic data. These include: the origin of the eukaryotes, the origin of animals, metazoan phylogenetics, the origin of light-sensitive proteins and vision. He is Reader of Phylogenomics at the School of Earth Sciences and at the School of Biological Sciences of the University of Bristol. He is a member of the NASA Astrobiology Institute (Massachusetts Institute of Technology (MIT) Lead Team). Davide Pisani's Homepage.

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