1932

Abstract

The origin of eukaryotes has been defined as the major evolutionary transition since the origin of life itself. Most hallmark traits of eukaryotes, such as their intricate intracellular organization, can be traced back to a putative common ancestor that predated the broad diversity of extant eukaryotes. However, little is known about the nature and relative order of events that occurred in the path from preexisting prokaryotes to this already sophisticated ancestor. The origin of mitochondria from the endosymbiosis of an alphaproteobacterium is one of the few robustly established events to which most hypotheses on the origin of eukaryotes are anchored, but the debate is still open regarding the time of this acquisition, the nature of the host, and the ecological and metabolic interactions between the symbiotic partners. After the acquisition of mitochondria, eukaryotes underwent a fast radiation into several major clades whose phylogenetic relationships have been largely elusive. Recent progress in the comparative analyses of a growing number of genomes is shedding light on the early events of eukaryotic evolution as well as on the root and branching patterns of the tree of eukaryotes. Here I discuss current knowledge and debates on the origin and early evolution of eukaryotes. I focus particularly on how phylogenomic analyses have challenged some of the early assumptions about eukaryotic evolution, including the widespread idea that mitochondrial symbiosis in an archaeal host was the earliest event in eukaryogenesis.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-090817-062213
2021-10-08
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/75/1/annurev-micro-090817-062213.html?itemId=/content/journals/10.1146/annurev-micro-090817-062213&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Adl SM, Simpson AGB, Lane CE, Lukeš J, Bass D et al. 2012. The revised classification of eukaryotes. J. Eukaryot. Microbiol. 59:5429–514
    [Google Scholar]
  2. 2. 
    Baum DA, Baum B. 2014. An inside-out origin for the eukaryotic cell. BMC Biol 12:76
    [Google Scholar]
  3. 3. 
    Caforio A, Siliakus MF, Exterkate M, Jain S, Jumde VR et al. 2018. Converting Escherichia coli into an archaebacterium with a hybrid heterochiral membrane. PNAS 115:143704–9
    [Google Scholar]
  4. 4. 
    Cavalier-Smith T. 1987. Eukaryotes with no mitochondria. Nature 326:6111332–33
    [Google Scholar]
  5. 5. 
    Cavalier-Smith T. 2006. Origin of mitochondria by intracellular enslavement of a photosynthetic purple bacterium. Proc. R. Soc. B 273: 1596.1943–52
    [Google Scholar]
  6. 6. 
    Chiyomaru K, Takemoto K. 2020. Revisiting the hypothesis of an energetic barrier to genome complexity between eukaryotes and prokaryotes. R. Soc. Open Sci. 7:2191859
    [Google Scholar]
  7. 7. 
    Dacks JB, Field MC, Buick R, Eme L, Gribaldo S et al. 2016. The changing view of eukaryogenesis—fossils, cells, lineages and how they all come together. J. Cell Sci. 129:203695–703
    [Google Scholar]
  8. 8. 
    de Duve C. 1969. Evolution of the peroxisome. Ann. N. Y. Acad. Sci. 168:2369–81
    [Google Scholar]
  9. 9. 
    de Duve C. 2007. The origin of eukaryotes: a reappraisal. Nat. Rev. Genet. 8:5395–403
    [Google Scholar]
  10. 10. 
    Derelle R, Torruella G, Klimeš V, Brinkmann H, Kim E et al. 2015. Bacterial proteins pinpoint a single eukaryotic root. PNAS 112:7E693–99
    [Google Scholar]
  11. 11. 
    Fan L, Wu D, Goremykin V, Xiao J, Xu Y et al. 2020. Phylogenetic analyses with systematic taxon sampling show that mitochondria branch within Alphaproteobacteria. Nat. Ecol. Evol. 4:91213–19
    [Google Scholar]
  12. 12. 
    Fernández R, Gabaldón T. 2020. Gene gain and loss across the metazoan tree of life. Nat. Ecol. Evol. 4:4524–33
    [Google Scholar]
  13. 13. 
    Doolittle WF 2014. How natural a kind is “Eukaryote?. Cold Spring Harb. Perspect. Biol. 6:6a015974
    [Google Scholar]
  14. 14. 
    Gabaldón T. 2010. Peroxisome diversity and evolution. Philos. Trans. R. Soc. London B 365: 1541.765–73
    [Google Scholar]
  15. 15. 
    Gabaldón T. 2012. Mitochondrial origins. Organelle Genetics: Evolution of Organelle Genomes and Gene Expression CE Bullerwell 3–18 Berlin: Springer-Verlag
    [Google Scholar]
  16. 16. 
    Gabaldón T. 2014. Evolutionary considerations on the origin of peroxisomes from the endoplasmic reticulum, and their relationships with mitochondria. Cell. Mol. Life Sci. 71:132379–82
    [Google Scholar]
  17. 17. 
    Gabaldón T. 2014. A metabolic scenario for the evolutionary origin of peroxisomes from the endomembranous system. Cell. Mol. Life Sci. 71:132373–76
    [Google Scholar]
  18. 18. 
    Gabaldón T. 2018. Relative timing of mitochondrial endosymbiosis and the “pre-mitochondrial symbioses” hypothesis. IUBMB Life 70:121188–96
    [Google Scholar]
  19. 19. 
    Gabaldón T. 2020. Patterns and impacts of nonvertical evolution in eukaryotes: a paradigm shift. Ann. N. Y. Acad. Sci. 1476:178–92
    [Google Scholar]
  20. 20. 
    Gabaldón T, Huynen MA. 2003. Reconstruction of the proto-mitochondrial metabolism. Science 301:5633609
    [Google Scholar]
  21. 21. 
    Gabaldón T, Huynen MA. 2004. Shaping the mitochondrial proteome. Biochim. Biophys. Acta Bioenerg. 1659:2–3212–20
    [Google Scholar]
  22. 22. 
    Gabaldón T, Huynen MA. 2007. From endosymbiont to host-controlled organelle: the hijacking of mitochondrial protein synthesis and metabolism. PLOS Comput. Biol. 3:112209–18
    [Google Scholar]
  23. 23. 
    Gabaldón T, Huynen MA. 2008. Reconstruction of ancestral proteomes. Ancestral Sequence Reconstruction D Liberles 128–38 Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  24. 24. 
    Gabaldón T, Pittis AA. 2015. Origin and evolution of metabolic sub-cellular compartmentalization in eukaryotes. Biochimie 119:262–68
    [Google Scholar]
  25. 25. 
    Gabaldón T, Snel B, van Zimmeren F, Hemrika W, Tabak H, Huynen MA. 2006. Origin and evolution of the peroxisomal proteome. Biol. Direct. 1:8
    [Google Scholar]
  26. 26. 
    Garza DR, Dutilh BE. 2015. From cultured to uncultured genome sequences: metagenomics and modeling microbial ecosystems. Cell. Mol. Life Sci. 72:224287–308
    [Google Scholar]
  27. 27. 
    Goodenough U, Heitman J. 2014. Origins of eukaryotic sexual reproduction. Cold Spring Harb. Perspect. Biol. 6:3a016154
    [Google Scholar]
  28. 28. 
    Gould SB, Garg SG, Martin WF. 2016. Bacterial vesicle secretion and the evolutionary origin of the eukaryotic endomembrane system. Trends Microbiol 24:7525–34
    [Google Scholar]
  29. 29. 
    Gray MW. 2017. Lynn Margulis and the endosymbiont hypothesis: 50 years later. Mol. Biol. Cell 28:101285–87
    [Google Scholar]
  30. 30. 
    Gray MW, Burger G, Lang BF. 1999. Mitochondrial evolution. Science 283:54071476–81
    [Google Scholar]
  31. 31. 
    Hampl V, Čepička I, Eliáš M. 2019. Was the mitochondrion necessary to start eukaryogenesis?. Trends Microbiol 27:296–104
    [Google Scholar]
  32. 32. 
    He D, Fiz-Palacios O, Fu CJ, Tsai CC, Baldauf SL. 2014. An alternative root for the eukaryote tree of life. Curr. Biol. 24:4465–70
    [Google Scholar]
  33. 33. 
    Husnik F, Keeling PJ. 2019. The fate of obligate endosymbionts: reduction, integration, or extinction. Curr. Opin. Genet. Dev 58–59:1–8
    [Google Scholar]
  34. 34. 
    Imachi H, Nobu MK, Nakahara N, Morono Y, Ogawara M et al. 2020. Isolation of an archaeon at the prokaryote-eukaryote interface. Nature 577:7791519–25
    [Google Scholar]
  35. 35. 
    Karnkowska A, Vacek V, Zubáčová Z, Treitli SC, Petrželková R et al. 2016. A eukaryote without a mitochondrial organelle. Curr. Biol. 26:101274–84
    [Google Scholar]
  36. 36. 
    Keeling PJ, Burki F. 2019. Progress towards the tree of eukaryotes. Curr. Biol. 29:16R808–17
    [Google Scholar]
  37. 37. 
    Khan S, Scholey JM. 2018. Assembly, functions and evolution of archaella, flagella and cilia. Curr. Biol. 28:6R278–92
    [Google Scholar]
  38. 38. 
    Koonin EV. 2010. The origin and early evolution of eukaryotes in the light of phylogenomics. Genome Biol 11:5209
    [Google Scholar]
  39. 39. 
    Koonin EV. 2015. Origin of eukaryotes from within archaea, archaeal eukaryome and bursts of gene gain: eukaryogenesis just made easier?. Philos. Trans. R. Soc. B 370: 1678.20140333
    [Google Scholar]
  40. 40. 
    Koumandou VL, Wickstead B, Ginger ML, van der Giezen M, Dacks JB, Field MC. 2013. Molecular paleontology and complexity in the last eukaryotic common ancestor. Crit. Rev. Biochem. Mol. Biol. 48:4373–96
    [Google Scholar]
  41. 41. 
    Kurland C, Andersson S. 2000. Origin and evolution of the mitochondrial proteome. Microbiol. Mol. Biol. Rev. 64:4786–820
    [Google Scholar]
  42. 42. 
    Lane N, Martin W 2010. The energetics of genome complexity. Nature 467:7318929–34
    [Google Scholar]
  43. 43. 
    Lara E, Moreira D, López-García P. 2010. The environmental clade LKM11 and Rozella form the deepest branching clade of fungi. Protist 161:1116–21
    [Google Scholar]
  44. 44. 
    Lombard J, López-García P, Moreira D. 2012. The early evolution of lipid membranes and the three domains of life. Nat. Rev. Microbiol. 10:7507–15
    [Google Scholar]
  45. 45. 
    López-García P, Moreira D. 2020. The Syntrophy hypothesis for the origin of eukaryotes revisited. Nat. Microbiol. 5:5655–67
    [Google Scholar]
  46. 46. 
    Lynch M, Marinov GK 2015. The bioenergetic costs of a gene. PNAS 112:5115690–95
    [Google Scholar]
  47. 47. 
    Martijn J, Vosseberg J, Guy L, Offre P, Ettema TJG. 2018. Deep mitochondrial origin outside the sampled alphaproteobacteria. Nature 557:7703101–5
    [Google Scholar]
  48. 48. 
    Martin W, Koonin EV. 2006. Introns and the origin of nucleus-cytosol compartmentalization. Nature 440:708041–45
    [Google Scholar]
  49. 49. 
    Martin W, Müller M. 1998. The hydrogen hypothesis for the first eukaryote. Nature 392:667137–41
    [Google Scholar]
  50. 50. 
    Martin WF, Tielens AGM, Mentel M, Garg SG, Gould SB. 2017. The physiology of phagocytosis in the context of mitochondrial origin. Microbiol. Mol. Biol. Rev. 81:3e00008-17
    [Google Scholar]
  51. 51. 
    Mast FD, Barlow LD, Rachubinski RA, Dacks JB. 2014. Evolutionary mechanisms for establishing eukaryotic cellular complexity. Trends Cell Biol 24:7435–42
    [Google Scholar]
  52. 52. 
    Mitchell DR. 2007. The evolution of eukaryotic cilia and flagella as motile and sensory organelles. Adv. Exp. Med. Biol. 607:130–40
    [Google Scholar]
  53. 53. 
    Moreira D, López-García P. 1998. Symbiosis between methanogenic archaea and δ-proteobacteria as the origin of eukaryotes: the syntrophic hypothesis. J. Mol. Evol. 47:5517–30
    [Google Scholar]
  54. 54. 
    Mukherjee S, Stamatis D, Bertsch J, Ovchinnikova G, Katta HY et al. 2019. Genomes OnLine database (GOLD) v.7: updates and new features. Nucleic Acids Res 47:D1D649–59
    [Google Scholar]
  55. 55. 
    O'Malley MA, Leger MM, Wideman JG, Ruiz-Trillo I. 2019. Concepts of the last eukaryotic common ancestor. Nat. Ecol. Evol. 3:3338–44
    [Google Scholar]
  56. 56. 
    Pittis AA, Gabaldón T. 2016. Late acquisition of mitochondria by a host with chimaeric prokaryotic ancestry. Nature 531:7592101–4
    [Google Scholar]
  57. 57. 
    Pollard TD, Goldman RD. 2018. Overview of the cytoskeleton from an evolutionary perspective. Cold Spring Harb. Perspect. Biol. 10:7a030288
    [Google Scholar]
  58. 58. 
    Roger AJ, Muñoz-Gómez SA, Kamikawa R 2017. The origin and diversification of mitochondria. Curr. Biol. 27:21R1177–92
    [Google Scholar]
  59. 59. 
    Sagan L. 1967. On the origin of mitosing cells. J. Theor. Biol. 14:3255–74
    [Google Scholar]
  60. 60. 
    Schlüter A, Fourcade S, Ripp R, Mandel JL, Poch O, Pujol A. 2006. The evolutionary origin of peroxisomes: an ER-peroxisome connection. Mol. Biol. Evol. 23:4838–45
    [Google Scholar]
  61. 61. 
    Shen XX, Opulente DA, Kominek J, Zhou X, Steenwyk JL et al. 2018. Tempo and mode of genome evolution in the budding yeast subphylum. Cell 175:61533–45.e20
    [Google Scholar]
  62. 62. 
    Sousa FL, Neukirchen S, Allen JF, Lane N, Martin WF. 2016. Lokiarchaeon is hydrogen dependent. Nat. Microbiol. 1:16034
    [Google Scholar]
  63. 63. 
    Spang A, Saw JH, Jørgensen SL, Zaremba-Niedzwiedzka K, Martijn J et al. 2015. Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521:7551173–79
    [Google Scholar]
  64. 64. 
    Spang A, Stairs CW, Dombrowski N, Eme L, Lombard J et al. 2019. Proposal of the reverse flow model for the origin of the eukaryotic cell based on comparative analyses of Asgard archaeal metabolism. Nat. Microbiol. 4:71138–48
    [Google Scholar]
  65. 65. 
    Speijer D. 2011. Oxygen radicals shaping evolution: why fatty acid catabolism leads to peroxisomes while neurons do without it. BioEssays 33:288–94
    [Google Scholar]
  66. 66. 
    Speijer D. 2014. Reconsidering ideas regarding the evolution of peroxisomes: the case for a mitochondrial connection. Cell. Mol. Life Sci. 71:132377–78
    [Google Scholar]
  67. 67. 
    Speijer D. 2017. Alternating terminal electron-acceptors at the basis of symbiogenesis: how oxygen ignited eukaryotic evolution. BioEssays 39:21600174
    [Google Scholar]
  68. 68. 
    Stanier R, Doudoroff M, Adelberg E. 1963. The Microbial World Englewood Cliffs, NJ: Prentice Hall, 2nd ed..
  69. 69. 
    Von Dohlen CD, Kohler S, Alsop ST, McManus WR. 2001. Mealybug β-proteobacterial endosymbionts contain γ-proteobacterial symbionts. Nature 412:6845433–36
    [Google Scholar]
  70. 70. 
    Vosseberg J, van Hooff JJE, Marcet-Houben M, van Vlimmeren A, van Wijk LM et al. 2021. Timing the origin of eukaryotic cellular complexity with ancient duplications. Nat. Ecol. Evol. 5:92–100
    [Google Scholar]
  71. 71. 
    Wickstead B, Gull K. 2011. The evolution of the cytoskeleton. J. Cell Biol. 194:4513–25
    [Google Scholar]
  72. 72. 
    Williams TA, Cox CJ, Foster PG, Szöllősi GJ, Embley TM. 2020. Phylogenomics provides robust support for a two-domains tree of life. Nat. Ecol. Evol. 4:1138–47
    [Google Scholar]
  73. 73. 
    Williams TA, Foster PG, Nye TMW, Cox CJ, Embley TM. 2012. A congruent phylogenomic signal places eukaryotes within the Archaea. Proc. R. Soc. B 279: 1749.4870–79
    [Google Scholar]
  74. 74. 
    Yu FB, Blainey PC, Schulz F, Woyke T, Horowitz MA, Quake SR 2017. Microfluidic-based mini-metagenomics enables discovery of novel microbial lineages from complex environmental samples. eLife 6:e26580
    [Google Scholar]
  75. 75. 
    Zaremba-Niedzwiedzka K, Caceres EF, Saw JH, Bäckström D, Juzokaite L et al. 2017. Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature 541:7637353–58
    [Google Scholar]
/content/journals/10.1146/annurev-micro-090817-062213
Loading
/content/journals/10.1146/annurev-micro-090817-062213
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error