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Journal of Molecular Evolution

, Volume 79, Issue 5–6, pp 228–239 | Cite as

The Relative Ages of Eukaryotes and Akaryotes

  • David Penny
  • Lesley J. Collins
  • Toni K. Daly
  • Simon J. Cox
Original Article

Abstract

The Last Eukaryote Common Ancestor (LECA) appears to have the genetics required for meiosis, mitosis, nucleus and nuclear substructures, an exon/intron gene structure, spliceosomes, many centres of DNA replication, etc. (and including mitochondria). Most of these features are not generally explained by models for the origin of the Eukaryotic cell based on the fusion of an Archeon and a Bacterium. We find that the term ‘prokaryote’ is ambiguous and the non-phylogenetic term akaryote should be used in its place because we do not yet know the direction of evolution between eukaryotes and akaryotes. We use the term ‘protoeukaryote’ for the hypothetical stem group ancestral eukaryote that took up a bacterium as an endosymbiont that formed the mitochondrion. It is easier to make detailed models with a eukaryote to an akaryote transition, rather than vice versa. So we really are at a phylogenetic impasse in not being confident about the direction of change between eukaryotes and akaryotes.

Keywords

Akaryotes (prokaryotes) Eukaryotes older Exon/intron old Multiple centres of replication Nucleus 

Notes

Acknowledgments

This work was started for the Les Treilles foundation workshop on ‘The origins of sex and of modern eukaryotes’ held in the south of France in July 2012.

References

  1. Attwater J, Wochner A, Holliger P (2013) In-ice evolution of RNA polymerase ribozyme activity. Nat Chem 5:1011–1018PubMedCentralPubMedCrossRefGoogle Scholar
  2. Blake CCF (1983) Exons—present from the beginning? Nature 306:535–537PubMedCrossRefGoogle Scholar
  3. Bolcun-Filas E, Rinaldi VD, White ME, Schimenti JC (2014) Reversal of female infertility by Chk2 ablation reveals the oocyte DNA damage checkpoint pathway. Science 343:533–536PubMedCentralPubMedCrossRefGoogle Scholar
  4. Boussau B, Blanquart S, Necsulea A, Lartillot N, Gouy M (2008) Parallel adaptations to high temperatures in the Archaean eon. Nature 456:942–945PubMedCrossRefGoogle Scholar
  5. Bracht JR, Perlman DH, landweber LF (2012) Cytosine methylation and hydroxymethylation mark DNA for elimination in Oxytricha trifallax. Genome Biol 13:R99PubMedCentralPubMedCrossRefGoogle Scholar
  6. Brawerman G (1974) Eukaryotic messenger RNA. Annu Rev Biochem 43:621–642PubMedCrossRefGoogle Scholar
  7. Brinkmann H, Philippe H (1999) Archaea sister group of bacteria? Indications from tree reconstruction artifacts in ancient phylogenies. Mol Biol Evol 16:817–825PubMedCrossRefGoogle Scholar
  8. Caetano-Anollés G (2002) Evolved RNA secondary structure and the rooting of the universal tree of life. J Mol Evol 54:333–345PubMedCrossRefGoogle Scholar
  9. Carlile M (1982) Prokaryotes and eukaryotes: strategies and successes. Trends Bioch Sci 7:128–130CrossRefGoogle Scholar
  10. Cavalier-Smith T (2010) Origin of the cell nucleus, mitosis and sex: roles of intracellular coevolution. Biol Dir 5:7CrossRefGoogle Scholar
  11. Chatton E (1925) Pansporella perplexa: amœbien à spores protégées parasite des daphnies: réflexions sur la biologie et la phylogénie des protozoaires. Masson, ParisGoogle Scholar
  12. Collins LJ, Penny D (2005) Complex spliceosomal organization ancestral to extant eukaryotes. Mol Biol Evol 22:1053–1066PubMedCrossRefGoogle Scholar
  13. Collins LJ, Kurland CG, Biggs P, Penny D (2009) The modern RNP world of eukaryotes. J Hered 100:597–604PubMedCrossRefGoogle Scholar
  14. Collins LJ, Chen XS, Schonfeld B (2010) The epigenetics of non-coding RNA. In: Tollefsbol T (ed) Handbook of epigenetics. Academic Press, Oxford, pp 49–61Google Scholar
  15. Crest J, Oxnard N, Ji J-Y, Schubiger G (2007) Onset of the DNA replication checkpoint in the early drosophila embryo. Genetics 175:567–584PubMedCentralPubMedCrossRefGoogle Scholar
  16. Daly TK, Sutherland-Smith AJ, Penny D (2013) In silico resurrection of the Major Vault Protein suggests it is ancestral in modern eukaryotes. Gen Biol Evol 5:1567–1583CrossRefGoogle Scholar
  17. de Duve C (2007) The origin of eukaryotes: a reappraisal. Nat Rev Gen 8:395–403CrossRefGoogle Scholar
  18. de Nooijer S, Holland B, Penny D (2009) Eukaryote origins: there was no Garden of Eden? PLoS ONE 4:e5507PubMedCentralPubMedCrossRefGoogle Scholar
  19. del Campo J, Sieracki ME, Molestina R, Keeling P, Massana R, Ruiz-Trillo I (2014) The others: our biased perspective of eukaryotic genomes. Trends Ecol Evol 29:252–259PubMedCentralPubMedCrossRefGoogle Scholar
  20. Desmond E, Brochier-Armanet C, Forterre P, Gribaldo S (2011) On the last common ancestor and early evolution of eukaryotes: reconstructing the history of mitochondrial ribosomes. Res Microbiol 162:53–70PubMedCrossRefGoogle Scholar
  21. Di Giulio M (2011) The last universal common ancestor (LUCA) and the ancestors of Archaea and Bacteria were progenote. J Mol Evol 72:119–126PubMedCrossRefGoogle Scholar
  22. Diekmann Y, Pereira-Leal JB (2013) Evolution of intracellular compartmentalization. Biochem J 449:319–331PubMedCrossRefGoogle Scholar
  23. Doolittle WF (2014) The trouble with (group II) introns. Proc Natl Acad Sci USA 111:6536–6537PubMedCentralPubMedCrossRefGoogle Scholar
  24. Drinnenberg IA, Fink GR, Bartel DP (2011) Compatibility with killer explains the rise of RNAi-deficient fungi. Science 333:1592PubMedCentralPubMedCrossRefGoogle Scholar
  25. Egel R, Penny D (2007) On the origin of meiosis in eukaryotic evolution: coevolution of meiosis and mitosis from feeble beginnings. In: Egel R, Lankenau D-H (eds) Recombination and meiosis: models, means and evolution. Springer, Berlin, pp 249–288Google Scholar
  26. Eigen M, Schuster P (1978) Part A: Emergence of the hypercycle. Naturwissenschaften 65:7–41CrossRefGoogle Scholar
  27. El Albani A et al (2014) The 2.1 Ga old Francevillian biota: biogenicity, taphonomy and biodiversity. PLoS ONE 9:e99438PubMedCentralPubMedCrossRefGoogle Scholar
  28. Embley TM, Martin W (2006) Eukaryotic evolution, changes and challenges. Nature 440:623–630PubMedCrossRefGoogle Scholar
  29. Epp C, Li F, Howitt CA, Chookajorn T, Deitsch KW (2009) Chromatin associated sense and antisense noncoding RNAs are transcribed from the var gene family of virulence genes of the malaria parasite Plasmodium falciparum. RNA 15:116–127PubMedCentralPubMedCrossRefGoogle Scholar
  30. Fica SM, Tuttle N, Novak T et al (2013) RNA catalyses nuclear pre-mRNA splicing. Nature 503:229–234PubMedPubMedCentralGoogle Scholar
  31. Fisk JC, Read LK (2011) Protein arginine methylation in parasitic protozoa. Eukaryot Cell 10:1013–1022PubMedCentralPubMedCrossRefGoogle Scholar
  32. Flot JF et al (2013) Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga. Nature 500:453–457PubMedCrossRefGoogle Scholar
  33. Forsdyke DR (2013) Introns first. Biol Theory. doi: 10.10007/s13752-013-0090-6 Google Scholar
  34. Forterre P (1995) Thermoreduction, a hypothesis for the origin of prokaryotes. C R Acad Sci Paris 318:415–422PubMedGoogle Scholar
  35. Forterre P (2006) Three RNA cells for ribosomal lineages and three DNA viruses to replicate their genomes: a hypothesis for the origin of the cellular domain. Proc Natl Acad Sci USA 103:3669–3674PubMedCentralPubMedCrossRefGoogle Scholar
  36. Forterre P (2011) A new fusion hypothesis for the origin of Eukarya: better than previous ones, but probably also wrong. Res Microbiol 162:77–91PubMedCrossRefGoogle Scholar
  37. Forterre P (2013) The common ancestor of Archaea and Eukarya was not an Archaeon. Archaea UNSP 372396. doi: 10.1155/2013/372396 Google Scholar
  38. Forterre P, Philippe H (1999) Where is the root of the universal tree of life? BioEssays 21:871–879PubMedCrossRefGoogle Scholar
  39. Fossum S, Crooke E, Skarstad K (2007) Organization of sister origins and replisomes during multifork DNA replication in Escherichia coli. EMBO J 26:4514–4522PubMedCentralPubMedCrossRefGoogle Scholar
  40. Fuerst J (2013) The PVC superphylum: exceptions to the bacterial definition? Antonie Van Leeuwenhoek 104:451–466PubMedCrossRefGoogle Scholar
  41. Gilbert W (1978) Why genes in pieces? Nature 271:501PubMedCrossRefGoogle Scholar
  42. Gilbert W (1985) Genes-in-pieces revisited. Science 228:823–824PubMedCrossRefGoogle Scholar
  43. Glansdorf N (1999) On the origin of operons and their possible role in evolution towards thermophily. J Mol Evol 49:432–438CrossRefGoogle Scholar
  44. Gribaldo S, Poole AM, Daubin V, Forterre P, Brochier-Armanet C (2010) The origin of eukaryotes and their relationship with the Archaea: are we at a phylogenomic impasse? Nat Rev Microbiol 8:743–752PubMedCrossRefGoogle Scholar
  45. Harish A, Tunlid A, Kurland CG (2013) Rooted phylogeny of the three superkingdoms. Biochimie 95:1593–1604PubMedCrossRefGoogle Scholar
  46. Hawkins M, Malla S, Blythe MJ, Nieduszynski CA, Allers T (2013) Accelerated growth in the absence of DNA replication origins. Nature 503:544–547PubMedCentralPubMedCrossRefGoogle Scholar
  47. He D, Fiz-Palacios O, Fu C-J, Fehling J, Tsai C-C, Baldauf SL (2014) An alternative root for the eukaryote tree of life. Curr Biol 24:465–470PubMedCrossRefGoogle Scholar
  48. Heslop-Harrison JS, Schwarzacher T (2013) Nucleosomes and centromeric DNA packaging. Proc Natl Acad Sci USA 110:19974–19975PubMedCentralPubMedCrossRefGoogle Scholar
  49. Javaux EJ, Marshall CP, Bekker A (2010) Organic-walled microfossils in 3.2-billion-year-old shallow-marine siliciclastic deposits. Nature 463:934–938PubMedCrossRefGoogle Scholar
  50. Jeffares DG, Poole AM, Penny D (1998) Relics from the RNA world. J Mol Evol 46:18–36PubMedCrossRefGoogle Scholar
  51. Jeffares DC, Mourier T, Penny D (2006) The biology of intron gain and loss. Trends Gen 22:16–22CrossRefGoogle Scholar
  52. Jeltsch A (2013) Oxygen, epigenetic signaling, and the evolution of early life. Trends Biochem Sci 38:172–176PubMedCrossRefGoogle Scholar
  53. Joyce GF (2002) The antiquity if RNA-based evolution. Nature 418:214–221PubMedCrossRefGoogle Scholar
  54. Kashtan N et al (2014) Single-cell genomics reveals hundreds of coexisting subpopulations in wild Prochlorococcus. Science 344:416–420PubMedCrossRefGoogle Scholar
  55. Keeling PJ et al (2005) The tree of eukaryotes. Trends Ecol Evol 20:670–676PubMedCrossRefGoogle Scholar
  56. Koonin EV (2010) The incredible expanding ancestor of eukaryotes. Cell 140:606–608PubMedCentralPubMedCrossRefGoogle Scholar
  57. Koonin EV (2014) Carl Woese’s vision of cellular evolution and the domains of life. RNA Biol 11:197–204PubMedCentralPubMedCrossRefGoogle Scholar
  58. Koonin EV, Csuros M, Rogozin IB (2013) Whence genes in pieces: reconstruction of the exon-intron gene structures of the last eukaryotic common ancestor and other ancestral eukaryotes. Wiley Interdis Rev RNA 4:93–105CrossRefGoogle Scholar
  59. Kurland CG, Collins LJ, Penny D (2006) Genomics and the irreducible nature of eukaryote cells. Science 312:1011–1014PubMedCrossRefGoogle Scholar
  60. Lan R, Reeves PR (2000) Intraspecies variation in bacterial genomes: the need for a species genome concept. Trends Microbiol 8:396–401PubMedCrossRefGoogle Scholar
  61. Lane CE, van den Heuvel K, Kozera C, Curtis BA, Parsons BJ, Bowman S, Archibald JM (2007) Nucleomorph genome of Hemiselmis andersenii reveals complete intron loss and compaction as a driver of protein structure and function. Proc Natl Acad Sci USA 104:19908–19913PubMedCentralPubMedCrossRefGoogle Scholar
  62. Lehman N (2003) A case for the extreme antiquity of recombination. J Mol Evol 56:770–777PubMedCrossRefGoogle Scholar
  63. Lindås A-C, Bernander R (2013) The cell cycle of archaea. Nat Rev Microbiol 11:627–638PubMedCrossRefGoogle Scholar
  64. Lopez P, Forterre P, Philippe H (1999) The root of the tree of life in the light of the covarion model. J Mol Evol 49:496–508PubMedCrossRefGoogle Scholar
  65. Lynch M, Abegg A (2010) The rate of establishment of complex adaptations. Mol Biol Evol 27:1404–1414PubMedCentralPubMedCrossRefGoogle Scholar
  66. Mans BJ, Anantharaman V, Aravind L, Koonin EV (2004) Comparative genomics, evolution and origins of the nuclear envelope and nuclear pore complex. Cell Cycle 3:1612–1637PubMedCrossRefGoogle Scholar
  67. Mossel E, Steel M (2004) A phase transition for a random cluster model on phylogenetic trees. Math Biosci 187:189–203PubMedCrossRefGoogle Scholar
  68. Motamedi MR, Verdel A, Colmenares SU, Gerber SA, Gygi SP, Moazed D (2004) Two RNAi complexes, RITS and RDRC, physically interact and localize to noncoding centromeric RNAs. Cell 119:789–802PubMedCrossRefGoogle Scholar
  69. Moulton V, Gardner PP, Pointon RF, Creamer LK, Jameson GB, Penny D (2000) RNA folding argues against a hot-start origin of life. J Mol Evol 51:416–421PubMedGoogle Scholar
  70. Muller HJ (1964) The relation of recombination to mutational advance. Mutat Res 1:2–9CrossRefGoogle Scholar
  71. Nardelli SC, Che F-Y (2013) The histone code of Toxoplasma gondii comprises conserved and unique posttranslational modifications. mBio 4:e00922PubMedCentralPubMedCrossRefGoogle Scholar
  72. Niklas KJ (2014) The evolutionary-developmental origins of multicellularity. Am J Bot 10:6–25CrossRefGoogle Scholar
  73. Orthwein O et al (2014) Mitosis inhibits DNA double-strand break repair to guard against telomere fusions. Science 344:189–193PubMedCrossRefGoogle Scholar
  74. Parfrey LW, Lahr DJG, Knoll AH, Katz LA (2011) Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc Natl Acad Sci USA 108:13624–13629PubMedCentralPubMedCrossRefGoogle Scholar
  75. Penny D (2005) An interpretive review of the origin of life research. Biol Philos 20:633–671CrossRefGoogle Scholar
  76. Penny D, Poole AM (1999) The nature of the universal ancestor. Curr Opin Gen Dev 9:672–677CrossRefGoogle Scholar
  77. Penny D, Poole AM (2003) Lateral gene transfer: some theoretical aspects. N Z BioSci 12:32–35Google Scholar
  78. Philippe N (2013) Pandoraviruses: amoeba viruses with genomes up to 2.5 Mb reaching that of parasitic eukaryotes. Science 341:281–286PubMedCrossRefGoogle Scholar
  79. Philippe H, Brinkmann H et al (2011) Resolving difficult phylogenetic questions: why more sequences are not enough. PLoS Biol 9:e1000602PubMedCentralPubMedCrossRefGoogle Scholar
  80. Poole AM (2006) Did group II intron proliferation in an endosymbiont-bearing archaeon create eukaryotes? Biol Dir 1:6. doi: 10.1186/1745-6150-1-36 CrossRefGoogle Scholar
  81. Poole AM (2010) Eukaryote evolution: the importance of the stem group. In: Caetano-Anolles G (ed) Evolutionary genomics and systems biology. Wiley, New YorkGoogle Scholar
  82. Poole AM, Neumann N (2011) Reconciling an archaeal origin of eukaryotes with engulfment: a biologically plausible update of the Eocyte hypothesis. Res Microbiol 162:71–76PubMedCrossRefGoogle Scholar
  83. Poole AM, Penny D (2007) Evaluating hypotheses for the origin of eukaryotes. BioEssays 29:74–84PubMedCrossRefGoogle Scholar
  84. Poole AM, Phillips MJ, Penny D (2003) Prokaryote and eukaryote evolvability. BioSystems 69:163–185PubMedCrossRefGoogle Scholar
  85. Ramakrishnan G, Gilchrist CA, Musa H, Torok MS, Grant PA, Mann BJ, Petri WA Jr (2004) Histone acetylatransferases and deacetylase in Entamoeba histolytica. Mol Biochem Parasit 138:205–216CrossRefGoogle Scholar
  86. Reanney DC (1974) On the origin of prokaryotes. J Theor Biol 48:243–251PubMedCrossRefGoogle Scholar
  87. Roy SW (2006) Intron-rich ancestors. Trends Genet 22:468–471PubMedCrossRefGoogle Scholar
  88. Simoes-Barbosa A, Hirt RP, Johnson PJ (2010) A metazoan/plant-like capping enzyme and cap modified nucleotides in the unicellular eukaryote Trichomonas vaginalis. PLoS Pathog 6:e1000999PubMedCentralPubMedCrossRefGoogle Scholar
  89. Sonda S et al (2010) Epigenetic mechanisms regulate stage differentiation in the minimized protozoan Giardia lamblia. Mol Microbiol 76:48–67PubMedCrossRefGoogle Scholar
  90. Strobel SA (2013) Metal ghosts in the splicing machine. Nature 503:201–202PubMedGoogle Scholar
  91. Sullivan WJ Jr, Nuguleswaran A, SO Angel (2006) Histones and histone modifications in protozoan parasites. Cell Microbiol 8:1850–1861PubMedCrossRefGoogle Scholar
  92. Trenholme K, Marek L, Duffy S (2014) Lysine acetylation in sexual stage malaria parasites is a target for antimalarial small molecules. Antimicrob Agents Chemother 58:3666–3678PubMedCentralPubMedCrossRefGoogle Scholar
  93. Vesteg M, Sandorova Z, Krajcovic J (2012) Selective forces for the origin of spliceosomes. J Mol Evol 74:226–231PubMedCrossRefGoogle Scholar
  94. White WTJ, Zhong B, Penny D (2013) Beyond reasonable doubt: evolution from DNA sequences. PLoS ONE 8:e69924PubMedCentralPubMedCrossRefGoogle Scholar
  95. Wilkins A, Holliday R (2009) The evolution of meiosis from mitosis. Genetics 181:3–12PubMedCentralPubMedCrossRefGoogle Scholar
  96. Williams TA, Foster PG, Cox CJ, Embley TM (2013) An archaeal origin of eukaryotes supports only two primary domains of life. Nature 504:231–236PubMedCrossRefGoogle Scholar
  97. Woese CR, Fox GE (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci USA 74:5088–5090PubMedCentralPubMedCrossRefGoogle Scholar
  98. Wu XM, Tronholm A et al (2013) Evidence for deep phylogenetic conservation of exonic splice-related constraints: splice-related skews at exonic ends in the brown alga Ectocarpus are common and resemble those seen in humans. Gen Biol Evol 5:1731–1745CrossRefGoogle Scholar
  99. Yi S (2012) Birds do it, bees do it, worms and ciliates do it too: DNA methylation from unexpected corners of the tree of life. Genome Biol 13:174PubMedCentralPubMedCrossRefGoogle Scholar
  100. Zhao L, Saelao P, Jones CD, Begun DJ (2014) Origin and spread of de novo genes in Drosophila melanogaster populations. Science 343:769–772PubMedCentralPubMedCrossRefGoogle Scholar
  101. Zubkov MV, Tarran GA (2008) High bacterivory by the smallest phytoplankton in the North Atlantic ocean. Nature 455:224–226PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • David Penny
    • 1
  • Lesley J. Collins
    • 2
  • Toni K. Daly
    • 1
    • 3
  • Simon J. Cox
    • 1
  1. 1.Institute of Fundamental SciencesMassey UniversityPalmerston NorthNew Zealand
  2. 2.Health SciencesUniversal College of LearningPalmerston NorthNew Zealand
  3. 3.NorthTecWhangareiNew Zealand

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