Origin of eukaryotes from within archaea, archaeal eukaryome and bursts of gene gain: Eukaryogenesis just made easier?

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 370, Issue 1678, 2015, Pages

  Koonin, Eugene V ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Archaea; Cytoskeleton; Endosymbiosis; Horizontal gene transfer; Phagocytosis

Indexed keywords

CELLS AND CELL COMPONENTS; COMMON ANCESTRY; ENDOSYMBIONT; EUKARYOTE; EVOLUTIONARY BIOLOGY; GENE FLOW; GENETIC ANALYSIS; GENOME; KARYOLOGY; MOLECULAR ANALYSIS; ORIGIN OF LIFE;

ARCHAEA; BACTERIA (MICROORGANISMS); EUKARYOTA;

ARCHAEAL GENOME; ARCHAEON; EUKARYOTE; EUKARYOTIC CELL; EVOLUTION; GENETICS;

ARCHAEA; BIOLOGICAL EVOLUTION; EUKARYOTA; EUKARYOTIC CELLS; GENOME, ARCHAEAL;

EID: 84940704092     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2014.0333     Document Type: Review

References (162)

1. Lane N, Martin W. 2010 The energetics of genome complexity. Nature 467, 929–934. (doi:10.1038/nature09486)
2. Lane N. 2011 Energetics and genetics across the prokaryote–eukaryote divide. Biol. Direct 6, 35. (doi:10.1186/1745-6150-6-35)
3. Lane N. 2015 The vital question: energy, evolution, and the origins of complex life. London, UK: W.W. Norton & Company.
4. Hudder A, Nathanson L, Deutscher MP. 2003 Organization of mammalian cytoplasm. Mol. Cell Biol. 23, 9318–9326. (doi:10.1128/MCB.23.24.9318-9326.2003)
5. Guigas G, Kalla C, Weiss M. 2007 The degree of macromolecular crowding in the cytoplasm and nucleoplasm of mammalian cells is conserved. FEBS Lett. 581, 5094–5098. (doi:10.1016/j.febslet.2007.09.054)
6. 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, 1612–1637. (doi:10.4161/cc.3.12.1345)
7. Collins L, Penny D. 2005 Complex spliceosomal organization ancestral to extant eukaryotes. Mol. Biol. Evol. 22, 1053–1066. (doi:10.1093/molbev/msi091)
8. Bapteste E, Charlebois RL, MacLeod D, Brochier C. 2005 The two tempos of nuclear pore complex evolution: highly adapting proteins in an ancient frozen structure. Genome Biol. 6, R85. (doi:10.1186/gb-2005-6-10-r85)
9. Makarova KS, Wolf YI, Mekhedov SL, Mirkin BG, Koonin EV. 2005 Ancestral paralogs and pseudoparalogs and their role in the emergence of the eukaryotic cell. Nucleic Acids Res. 33, 4626–4638. (doi:10.1093/nar/gki775)
10. Schlacht A, Herman EK, Klute MJ, Field MC, Dacks JB. 2014 Missing pieces of an ancient puzzle: evolution of the eukaryotic membrane-trafficking system. Cold Spring Harb. Perspect. Biol. 6, a016048. (doi:10.1101/cshperspect.a016048)
11. Kurland CG, Collins LJ, Penny D. 2006 Genomics and the irreducible nature of eukaryote cells. Science 312, 1011–1014. (doi:10.1126/science.1121674)
12. Martin W, Dagan T, Koonin EV, Dipippo JL, Gogarten JP, Lake JA. 2007 The evolution of eukaryotes. Science 316, 542–543; author reply 542–543. (doi:10.1126/science.316.5824.542c)
13. 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, 4576–4579. (doi:10.1073/pnas.87.12.4576)
14. Pace NR. 1997 A molecular view of microbial diversity and the biosphere. Science 276, 734–740. (doi:10.1126/science.276.5313.734)
15. Pace NR. 2006 Time for a change. Nature 441, 289. (doi:10.1038/441289a)
16. Pace NR. 2009 Mapping the tree of life: progress and prospects. Microbiol. Mol. Biol. Rev. 73, 565–576. (doi:10.1128/MMBR.00033-09)
17. Cavalier-Smith T. 1993 Kingdom protozoa and its 18 phyla. Microbiol. Rev. 57, 953–994.
18. Patterson DJ. 1999 The diversity of eukaryotes. Am. Nat. 154, S96–S124. (doi:10.1086/303287)
19. Roger AJ. 1999 Reconstructing early events in eukaryotic evolution. Am. Nat. 154, S146–S163. (doi:10.1086/303290)
20. Cavalier-Smith T. 2002 The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int. J. Syst. Evol. Microbiol. 52, 297–354.
21. Gray MW, Lang BF, Burger G. 2004 Mitochondria of protists. Annu. Rev. Genet. 38, 477–524. (doi:10.1146/annurev.genet.37.110801.142526)
22. van der Giezen M. 2009 Hydrogenosomes and mitosomes: conservation and evolution of functions. J. Eukaryot. Microbiol. 56, 221–231. (doi:10.1111/j.1550-7408.2009.00407.x)
23. Embley TM, Martin W. 2006 Eukaryotic evolution, changes and challenges. Nature 440, 623–630. (doi:10.1038/nature04546)
24. Shiflett AM, Johnson PJ. 2010 Mitochondrionrelated organelles in eukaryotic protists. Annu. Rev. Microbiol. 64, 409–429. (doi:10.1146/annurev.micro.62.081307.162826)
25. Katz LA. 1998 Changing perspectives on the origin of eukaryotes. Trends Ecol Evol. 13, 493–497. (doi:10.1016/S0169-5347(98)01490-6)
26. Gray MW, Burger G, Lang BF. 1999 Mitochondrial evolution. Science 283, 1476–1481. (doi:10.1126/science.283.5407.1476)
27. Lang BF, Gray MW, Burger G. 1999 Mitochondrial genome evolution and the origin of eukaryotes. Annu. Rev. Genet. 33, 351–397. (doi:10.1146/annurev.genet.33.1.351)
28. Poole A, Penny D. 2007 Eukaryote evolution: engulfed by speculation. Nature 447, 913. (doi:10.1038/447913a)
29. Poole AM, Penny D. 2007 Evaluating hypotheses for the origin of eukaryotes. Bioessays 29, 74–84. (doi:10.1002/bies.20516)
30. Martin W, Muller M. 1998 The hydrogen hypothesis for the first eukaryote. Nature 392, 37–41. (doi:10.1038/32096)
31. Lane N, Martin WF. 2012 The origin of membrane bioenergetics. Cell 151, 1406–1416. (doi:10.1016/j.cell.2012.11.050)
32. Esser C et al. 2004 A genome phylogeny for mitochondria among alpha-proteobacteria and a predominantly eubacterial ancestry of yeast nuclear genes. Mol. Biol. Evol. 21, 1643–1660. (doi:10.1093/molbev/msh160)
33. Rivera MC, Lake JA. 2004 The ring of life provides evidence for a genome fusion origin of eukaryotes. Nature 431, 152–155. (doi:10.1038/nature02848)
34. Pisani D, Cotton JA, McInerney JO. 2007 Supertrees disentangle the chimerical origin of eukaryotic genomes. Mol. Biol. Evol. 24, 1752–1760. (doi:10.1093/molbev/msm095)
35. Thiergart T, Landan G, Schenk M, Dagan T, Martin WF. 2012 An evolutionary network of genes present in the eukaryote common ancestor polls genomes on eukaryotic and mitochondrial origin. Genome Biol. Evol. 4, 466–485. (doi:10.1093/gbe/evs018)
36. Martin W, Koonin EV. 2006 Introns and the origin of nucleus–cytosol compartmentation. Nature 440, 41–45. (doi:10.1038/nature04531)
37. 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, 22. (doi:10.1186/1745-6150-1-22)
38. Cavalier-Smith T. 2009 Predation and eukaryote cell origins: a coevolutionary perspective. Int. J. Biochem. Cell Biol. 41, 307–322. (doi:10.1016/j.biocel.2008.10.002)
39. von Dohlen CD, Kohler S, Alsop ST, McManus WR. 2001 Mealybug beta-proteobacterial endosymbionts contain gamma-proteobacterial symbionts. Nature 412, 433–436. (doi:10.1038/35086563)
40. McCutcheon JP, Moran NA. 2012 Extreme genome reduction in symbiotic bacteria. Nat. Rev. Microbiol. 10, 13–26. (doi:10.1038/nrmicro2670)
41. Lake JA. 1988 Origin of the eukaryotic nucleus determined by rate-invariant analysis of rRNA sequences. Nature 331, 184–186. (doi:10.1038/331184a0)
42. 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, 3786–3790. (doi:10.1073/pnas.81.12.3786)
43. Lake JA. 1998 Optimally recovering rate variation information from genomes and sequences: pattern filtering. Mol. Biol. Evol. 15, 1224–1231. (doi:10.1093/oxfordjournals.molbev.a026030)
44. Rivera MC, Lake JA. 1992 Evidence that eukaryotes and eocyte prokaryotes are immediate relatives. Science 257, 74–76. (doi:10.1126/science.1621096)
45. Vishwanath P, Favaretto P, Hartman H, Mohr SC, Smith TF. 2004 Ribosomal protein-sequence block structure suggests complex prokaryotic evolution with implications for the origin of eukaryotes. Mol. Phylogenet. Evol. 33, 615–625. (doi:10.1016/j.ympev.2004.07.003)
46. Cox CJ, Foster PG, Hirt RP, Harris SR, Embley TM. 2008 The archaebacterial origin of eukaryotes. Proc. Natl Acad. Sci. USA 105, 20 356–20 361. (doi:10.1073/pnas.0810647105)
47. Lopez-Garcia P, Moreira D. 2006 Selective forces for the origin of the eukaryotic nucleus. Bioessays 28, 525–533. (doi:10.1002/bies.20413)
48. Horiike T, Hamada K, Miyata D, Shinozawa T. 2004 The origin of eukaryotes is suggested as the symbiosis of pyrococcus into gamma-proteobacteria by phylogenetic tree based on gene content. J. Mol. Evol. 59, 606–619. (doi:10.1007/s00239-004-2652-5)
49. Moreira D, Lopez-Garcia P. 1998 Symbiosis between methanogenic archaea and delta-proteobacteria as the origin of eukaryotes: the syntrophic hypothesis. J. Mol. Evol. 47, 517–530. (doi:10.1007/PL00006408)
50. Ciccarelli FD, Doerks T, von Mering C, Creevey CJ, Snel B, Bork P. 2006 Toward automatic reconstruction of a highly resolved tree of life. Science 311, 1283–1287. (doi:10.1126/science.1123061)
51. Fukami-Kobayashi K, Minezaki Y, Tateno Y, Nishikawa K. 2007 A tree of life based on protein domain organizations. Mol. Biol. Evol. 24, 1181–1189. (doi:10.1093/molbev/msm034)
52. Hedges SB, Chen H, Kumar S, Wang DY, Thompson AS, Watanabe H. 2001 A genomic timescale for the origin of eukaryotes. BMC Evol. Biol. 1, 4. (doi:10.1186/1471-2148-1-4)
53. Tekaia F, Yeramian E. 2005 Genome trees from conservation profiles. PLoS Comput. Biol. 1, e75. (doi:10.1371/journal.pcbi.0010075)
54. Forterre P. 1995 Thermoreduction, a hypothesis for the origin of prokaryotes. C R. Acad. Sci. 3 318, 415–422.
55. Poole A, Jeffares D, Penny D. 1999 Early evolution: prokaryotes, the new kids on the block. Bioessays 21, 880–889. (doi:10.1002/(SICI)1521-1878(199910)21:10,880::AID-BIES11.3.0.CO;2-P)
56. Collins LJ, Kurland CG, Biggs P, Penny D. 2009 The modern RNP world of eukaryotes. J. Hered. 100, 597–604. (doi:10.1093/jhered/esp064)
57. Hixon WG, Searcy DG. 1993 Cytoskeleton in the archaebacterium Thermoplasma acidophilum? Viscosity increase in soluble extracts. Biosystems 29, 151–160. (doi:10.1016/0303-2647(93)90091-P)
58. Margulis L. 1996 Archaeal–eubacterial mergers in the origin of Eukarya: phylogenetic classification of life. Proc. Natl Acad. Sci. USA 93, 1071–1076. (doi:10.1073/pnas.93.3.1071)
59. Margulis L, Dolan MF, Guerrero R. 2000 The chimeric eukaryote: origin of the nucleus from the karyomastigont in amitochondriate protists. Proc. Natl Acad. Sci. USA 97, 6954–6959. (doi:10.1073/pnas.97.13.6954)
60. Margulis L, Stolz JF. 1984 Cell symbiosis theory: status and implications for the fossil record. Adv. Space Res. 4, 195–201. (doi:10.1016/0273-1177(84)90562-3)
61. Searcy DG, Stein DB, Green GR. 1978 Phylogenetic affinities between eukaryotic cells and a thermophilic mycoplasma. Biosystems 10, 19–28. (doi:10.1016/0303-2647(78)90024-2)
62. Yutin N, Makarova KS, Mekhedov SL, Wolf YI, Koonin EV. 2008 The deep archaeal roots of eukaryotes. Mol. Biol. Evol. 25, 1619–1630. (doi:10.1093/molbev/msn108)
63. 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, 743–752. (doi:10.1038/nrmicro2426)
64. Elkins JG et al. 2008 A korarchaeal genome reveals insights into the evolution of the Archaea. Proc. Natl Acad. Sci. USA 105, 8102–8107. (doi:10.1073/pnas.0801980105)
65. Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P. 2008 Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat. Rev. Microbiol. 6, 245–252. (doi:10.1038/nrmicro1852)
66. Pester M, Schleper C, Wagner M. 2011 The Thaumarchaeota: an emerging view of their phylogeny and ecophysiology. Curr. Opin. Microbiol. 14, 300–306. (doi:10.1016/j.mib.2011.04.007)
67. Lloyd KG et al. 2013 Predominant archaea in marine sediments degrade detrital proteins. Nature 496, 215–218. (doi:10.1038/nature12033)
68. Brochier-Armanet C, Gribaldo S, Forterre P. 2012 Spotlight on the Thaumarchaeota. ISME J. 6, 227–230. (doi:10.1038/ismej.2011.145)
69. Reigstad LJ, Jorgensen SL, Schleper C. 2010 Diversity and abundance of Korarchaeota in terrestrial hot springs of Iceland and Kamchatka. ISME J. 4, 346–356. (doi:10.1038/ismej.2009.126)
70. Miller-Coleman RL, Dodsworth JA, Ross CA, Shock EL, Williams AJ, Hartnett HE, McDonald AI, Havig JR, Hedlund BP. 2012 Korarchaeota diversity, biogeography, and abundance in Yellowstone and Great Basin hot springs and ecological niche modeling based on machine learning. PLoS ONE 7, e35964. (doi:10.1371/journal.pone.0035964)
71. Nunoura T et al. 2011 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. (doi:10.1093/nar/gkq1228)
72. Rinke C et al. 2013 Insights into the phylogeny and coding potential of microbial dark matter. Nature 499, 431–437. (doi:10.1038/nature12352)
73. Castelle CJ et al. 2015 Genomic expansion of domain archaea highlights roles for organisms from new phyla in anaerobic carbon cycling. Curr. Biol. 25, 690–701. (doi:10.1016/j.cub.2015.01.014)
74. Eme L, Doolittle WF. 2015 Microbial diversity: a bonanza of phyla. Curr. Biol. 25, R227–R230. (doi:10.1016/j.cub.2014.12.044)
75. Petitjean C, Deschamps P, Lopez-Garcia P, Moreira D. 2015 Rooting the domain archaea by phylogenomic analysis supports the foundation of the new kingdom Proteoarchaeota. Genome Biol. Evol. 7, 191–204. (doi:10.1093/gbe/evu274)
76. Petitjean C, Deschamps P, Lopez-Garcia P, Moreira D, Brochier-Armanet C. 2015 Extending the conserved phylogenetic core of archaea disentangles the evolution of the third domain of life. Mol. Biol. Evol. 32, 1242–1254. (doi:10.1093/molbev/msv015)
77. Podar M, Makarova KS, Graham DE, Wolf YI, Koonin EV, Reysenbach AL. 2013 Insights into archaeal evolution and symbiosis from the genomes of a nanoarchaeon and its inferred crenarchaeal host from Obsidian Pool, Yellowstone National Park. Biol. Direct 8, 9. (doi:10.1186/1745-6150-8-9)
78. Koonin EV, Yutin N. 2014 The dispersed archaeal eukaryome and the complex archaeal ancestor of eukaryotes. Cold Spring Harb. Perspect. Biol. 6, a016188. (doi:10.1101/cshperspect.a016188)
79. Nelson-Sathi S et al. 2014 Origins of major archaeal clades correspond to gene acquisitions from bacteria. Nature 517, 77–80. (doi:10.1038/nature13805)
80. Guy L, Ettema TJ. 2011 The archaeal ’TACK’ superphylum and the origin of eukaryotes. Trends Microbiol. 19, 580–587. (doi:10.1016/j.tim.2011.09.002)
81. Williams TA, Foster PG, Nye TM, Cox CJ, Embley TM. 2012 A congruent phylogenomic signal places eukaryotes within the Archaea. Proc. R. Soc. B 279, 4870–4879. (doi:10.1098/rspb.2012.1795)
82. Martijn J, Ettema TJ. 2013 From archaeon to eukaryote: the evolutionary dark ages of the eukaryotic cell. Biochem. Soc. Trans. 41, 451–457. (doi:10.1042/BST20120292)
83. Yutin N, Puigbo P, Koonin EV, Wolf YI. 2012 Phylogenomics of prokaryotic ribosomal proteins. PLoS ONE 7, e36972. (doi:10.1371/journal.pone.0036972)
84. 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, 46. (doi:10.1186/1745-6150-7-46)
85. Williams TA, Embley TM. 2014 Archaeal ‘dark matter’ and the origin of eukaryotes. Genome Biol. Evol. 6, 474–481. (doi:10.1093/gbe/evu031)
86. Guy L, Saw JH, Ettema TJ. 2014 The archaeal legacy of eukaryotes: a phylogenomic perspective. Cold Spring Harb. Perspect. Biol. 6, a016022. (doi:10.1101/cshperspect.a016022)
87. 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, 6670–6675. (doi:10.1073/pnas.1420858112)
88. Makarova KS, Sorokin AV, Novichkov PS, Wolf YI, Koonin EV. 2007 Clusters of orthologous genes for 41 archaeal genomes and implications for evolutionary genomics of archaea. Biol. Direct 2, 33. (doi:10.1186/1745-6150-2-33)
89. Csuros M, Miklos I. 2009 Streamlining and large ancestral genomes in Archaea inferred with a phylogenetic birth-and-death model. Mol. Biol. Evol. 26, 2087–2095. (doi:10.1093/molbev/msp123)
90. Wolf YI, Koonin EV. 2013 Genome reduction as the dominant mode of evolution. BioEssays 35, 829–837. (doi:10.1002/bies.201300037)
91. Boussau B, Blanquart S, Necsulea A, Lartillot N, Gouy M. 2008 Parallel adaptations to high temperatures in the Archaean eon. Nature 456, 942–945. (doi:10.1038/nature07393)
92. Lasek-Nesselquist E, Gogarten JP. 2013 The effects of model choice and mitigating bias on the ribosomal tree of life. Mol. Phylogenet. Evol. 69, 17–38. (doi:10.1016/j.ympev.2013.05.006)
93. Williams TA, Foster PG, Cox CJ, Embley TM. 2013 An archaeal origin of eukaryotes supports only two primary domains of life. Nature 504, 231–236. (doi:10.1038/nature12779)
94. Kelly S, Wickstead B, Gull K. 2011 Archaeal phylogenomics provides evidence in support of a methanogenic origin of the Archaea and a thaumarchaeal origin for the eukaryotes. Proc. R. Soc. B 278, 1009–1018. (doi:10.1098/rspb.2010.1427)
95. Koonin EV, Makarova KS, Elkins JG. 2007 Orthologs of the small RPB8 subunit of the eukaryotic RNA polymerases are conserved in hyperthermophilic Crenarchaeota and ‘Korarchaeota’. Biol. Direct 2, 38. (doi:10.1186/1745-6150-2-38)
96. Blombach F, Makarova KS, Marrero J, Siebers B, Koonin EV, van der Oost J. 2009 Identification of an ortholog of the eukaryotic RNA polymerase III subunit RPC34 in Crenarchaeota and Thaumarchaeota suggests specialization of RNA polymerases for coding and non-coding RNAs in Archaea. Biol. Direct 4, 39. (doi:10.1186/1745-6150-4-39)
97. Daniels JP, Kelly S, Wickstead B, Gull K. 2009 Identification of a crenarchaeal orthologue of Elf1: implications for chromatin and transcription in Archaea. Biol. Direct 4, 24. (doi:10.1186/1745-6150-4-24)
98. Koonin EV, Makarova KS, Aravind L. 2001 Horizontal gene transfer in prokaryotes—quantification and classification. Annu. Rev. Microbiol. 55, 709–742.
99. Kennedy SP, Ng WV, Salzberg SL, Hood L, DasSarma S. 2001 Understanding the adaptation of Halobacterium species NRC-1 to its extreme environment through computational analysis of its genome sequence. Genome Res. 11, 1641–1650. (doi:10.1101/gr.190201)
100. Deppenmeier U et al. 2002 The genome of Methanosarcina mazei: evidence for lateral gene transfer between bacteria and archaea. J. Mol. Microbiol. Biotechnol. 4, 453–461.
101. Nelson-Sathi S, Dagan T, Landan G, Janssen A, Steel M, McInerney JO, Deppenmeier U, Martin WF. 2012 Acquisition of 1,000 eubacterial genes physiologically transformed a methanogen at the origin of Haloarchaea. Proc. Natl Acad. Sci. USA 109, 20 537–20 542. (doi:10.1073/pnas.1209119109)
102. Lowe J, Amos LA. 2009 Evolution of cytomotive filaments: the cytoskeleton from prokaryotes to eukaryotes. Int. J. Biochem. Cell Biol. 41, 323–329. (doi:10.1016/j.biocel.2008.08.010)
103. Aylett CH, Lowe J, Amos LA. 2011 New insights into the mechanisms of cytomotive actin and tubulin filaments. Int. Rev. Cell Mol. Biol. 292, 1–71. (doi:10.1016/B978-0-12-386033-0.00001-3)
104. Cabeen MT, Jacobs-Wagner C. 2010 The bacterial cytoskeleton. Annu. Rev. Genet. 44, 365–392. (doi:10.1146/annurev-genet-102108-134845)
105. Celler K, Koning RI, Koster AJ, van Wezel GP. 2013 Multidimensional view of the bacterial cytoskeleton. J. Bacteriol. 195, 1627–1636. (doi:10.1128/JB.02194-12)
106. Bork P, Sander C, Valencia A. 1992 An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin, and hsp70 heat shock proteins. Proc. Natl Acad. Sci. USA 89, 7290–7294. (doi:10.1073/pnas.89.16.7290)
107. Kabsch W, Holmes KC. 1995 The actin fold. FASEB J. 9, 167–174.
108. Lowe J, Amos LA. 1998 Crystal structure of the bacterial cell-division protein FtsZ. Nature 391, 203–206. (doi:10.1038/34472)
109. Nogales E, Downing KH, Amos LA, Lowe J. 1998 Tubulin and FtsZ form a distinct family of GTPases. Nat. Struct. Biol. 5, 451–458. (doi:10.1038/nsb0698-451)
110. Yutin N, Wolf MY, Wolf YI, Koonin EV. 2009 The origins of phagocytosis and eukaryogenesis. Biol. Direct 4, 9. (doi:10.1186/1745-6150-4-9)
111. Makarova KS, Yutin N, Bell SD, Koonin EV. 2010 Evolution of diverse cell division and vesicle formation systems in Archaea. Nat. Rev. Microbiol. 8, 731–741. (doi:10.1038/nrmicro2406)
112. Ettema TJ, Lindas AC, Bernander R. 2011 An actin-based cytoskeleton in archaea. Mol. Microbiol. 80, 1052–1061. (doi:10.1111/j.1365-2958.2011.07635.x)
113. Bernander R, Lind AE, Ettema TJ. 2011 An archaeal origin for the actin cytoskeleton: implications for eukaryogenesis. Commun. Integr. Biol. 4, 664–667. (doi:10.4161/cib.16974)
114. Lindas AC, Bernander R. 2013 The cell cycle of archaea. Nat. Rev. Microbiol. 11, 627–638. (doi:10.1038/nrmicro3077)
115. Lindas AC, Chruszcz M, Bernander R, Valegard K. 2014 Structure of crenactin, an archaeal actin homologue active at 90 degrees C. Acta Crystallogr. D Biol. Crystallogr. 70, 492–500. (doi:10.1107/S1399004714000935)
116. Izore T, Duman R, Kureisaite-Ciziene D, Lowe J. 2014 Crenactin from Pyrobaculum calidifontis is closely related to actin in structure and forms steep helical filaments. FEBS Lett. 588, 776–782. (doi:10.1016/j.febslet.2014.01.029)
117. Goley ED, Welch MD. 2006 The ARP2/3 complex: an actin nucleator comes of age. Nat. Rev. Mol. Cell Biol. 7, 713–726. (doi:10.1038/nrm2026)
118. Yutin N, Koonin EV. 2012 Archaeal origin of tubulin. Biol. Direct 7, 10. (doi:10.1186/1745-6150-7-10)
119. Lebedeva EV et al. 2013 Enrichment and genome sequence of the group I.1a ammonia-oxidizing Archaeon ‘Ca. Nitrosotenuis uzonensis’ representing a clade globally distributed in thermal habitats. PLoS ONE 8, e80835. (doi:10.1371/journal.pone.0080835)
120. Margolin W. 2009 Sculpting the bacterial cell. Curr. Biol. 19, R812–R822. (doi:10.1016/j.cub.2009.06.033)
121. Adams DW, Errington J. 2009 Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nat. Rev. Microbiol. 7, 642–653. (doi:10.1038/nrmicro2198)
122. Samson RY, Obita T, Freund SM, Williams RL, Bell SD. 2008 A role for the ESCRT system in cell division in archaea. Science 322, 1710–1713. (doi:10.1126/science.1165322)
123. Lindas AC, Karlsson EA, Lindgren MT, Ettema TJ, Bernander R. 2008 A unique cell division machinery in the Archaea. Proc. Natl Acad. Sci. USA 105, 18 942–18 946. (doi:10.1073/pnas.0809467105)
124. Samson RY, Bell SD. 2009 Ancient ESCRTs and the evolution of binary fission. Trends Microbiol. 17, 507–513. (doi:10.1016/j.tim.2009.08.003)
125. Ettema TJ, Bernander R. 2009 Cell division and the ESCRT complex: A surprise from the archaea. Commun. Integr. Biol. 2, 86–88. (doi:10.4161/cib.7523)
126. Pelve EA, Lindas AC, Martens-Habbena W, de la Torre JR, Stahl DA, Bernander R. 2011 Cdv-based cell division and cell cycle organization in the thaumarchaeon Nitrosopumilus maritimus. Mol. Microbiol. 82, 555–566. (doi:10.1111/j.1365-2958.2011.07834.x)
127. Dobro MJ, Samson RY, Yu Z, McCullough J, Ding HJ, Chong PL, Bell SD, Jensen GJ. 2013 Electron cryotomography of ESCRT assemblies and dividing Sulfolobus cells suggests that spiraling filaments are involved in membrane scission. Mol. Biol. Cell 24, 2319–2327. (doi:10.1091/mbc.E12-11-0785)
128. Burroughs AM, Iyer LM, Aravind L. 2012 Structure and evolution of ubiquitin and ubiquitin-related domains. Methods Mol. Biol. 832, 15–63. (doi:10.1007/978-1-61779-474-2_2)
129. Burroughs AM, Iyer LM, Aravind L. 2012 The natural history of ubiquitin and ubiquitin-related domains. Front. Biosci. 17, 1433–1460. (doi:10.2741/3996)
130. van der Veen AG, Ploegh HL. 2012 Ubiquitin-like proteins. Annu. Rev. Biochem. 81, 323–357. (doi:10.1146/annurev-biochem-093010-153308)
131. Hochstrasser M. 2000 Evolution and function of ubiquitin-like protein-conjugation systems. Nat. Cell Biol. 2, E153–E157. (doi:10.1038/35019643)
132. Maupin-Furlow JA. 2014 Prokaryotic ubiquitin-like protein modification. Annu. Rev. Microbiol. 68, 155–175. (doi:10.1146/annurev-micro-091313-103447)
133. Humbard MA, Miranda HV, Lim JM, Krause DJ, Pritz JR, Zhou G, Chen S, Wells L, Maupin-Furlow JA. 2010 Ubiquitin-like small archaeal modifier proteins (SAMPs) in Haloferax volcanii. Nature 463, 54–60. (doi:10.1038/nature08659)
134. Miranda HV, Nembhard N, Su D, Hepowit N, Krause DJ, Pritz JR, Phillips C, Soll D, Maupin-Furlow JA. 2011 E1- and ubiquitin-like proteins provide a direct link between protein conjugation and sulfur transfer in archaea. Proc. Natl Acad. Sci. USA 108, 4417–4422. (doi:10.1073/pnas.1018151108)
135. Maupin-Furlow JA. 2013 Ubiquitin-like proteins and their roles in archaea. Trends Microbiol. 21, 31–38. (doi:10.1016/j.tim.2012.09.006)
136. Grau-Bove X, Sebe-Pedros A, Ruiz-Trillo I. 2015 The eukaryotic ancestor had a complex ubiquitin signaling system of archaeal origin. Mol. Biol. Evol. 32, 726–739. (doi:10.1093/molbev/msu334)
137. Makarova KS, Koonin EV. 2010 Archaeal ubiquitinlike proteins: functional versatility and putative ancestral involvement in tRNA modification revealed by comparative genomic analysis. Archaea 2010, 710303. (doi:10.1155/2010/710303)
138. Wang F, Liu M, Qiu R, Ji C. 2011 The dual role of ubiquitin-like protein Urm1 as a protein modifier and sulfur carrier. Protein Cell 2, 612–619. (doi:10.1007/s13238-011-1074-6)
139. Van der Veen AG, Schorpp K, Schlieker C, Buti L, Damon JR, Spooner E, Ploegh HL, Jentsch S. 2011 Role of the ubiquitin-like protein Urm1 as a noncanonical lysine-directed protein modifier. Proc. Natl Acad. Sci. USA 108, 1763–1770. (doi:10.1073/pnas.1014402108)
140. Cerutti H, Casas-Mollano JA. 2006 On the origin and functions of RNA-mediated silencing: from protists to man. Curr. Genet. 50, 81–99. (doi:10.1007/s00294-006-0078-x)
141. Shabalina SA, Koonin EV. 2008 Origins and evolution of eukaryotic RNA interference. Trends Ecol. Evol. 23, 578–587. (doi:10.1016/j.tree.2008.06.005)
142. Carthew RW, Sontheimer EJ. 2009 Origins and mechanisms of miRNAs and siRNAs. Cell 136, 642–655. (doi:10.1016/j.cell.2009.01.035)
143. Burroughs AM, Ando Y, Aravind L. 2013 New perspectives on the diversification of the RNA interference system: insights from comparative genomics and small RNA sequencing. Wiley Interdiscip. Rev. RNA 5, 141–182. (doi:10.1002/wrna.1210)
144. Tijsterman M, Plasterk RH. 2004 Dicers at RISC; the mechanism of RNAi. Cell 117, 1–3. (doi:10.1016/S0092-8674(04)00293-4)
145. Jaskiewicz L, Filipowicz W. 2008 Role of Dicer in posttranscriptional RNA silencing. Curr. Top. Microbiol. Immunol. 320, 77–97.
146. Kidwell MA, Chan JM, Doudna JA. 2014 Evolutionarily conserved roles of the Dicer helicase domain in regulating RNA interference processing. J. Biol. Chem. 289, 28 352–28 362. (doi:10.1074/jbc.M114.589051)
147. Gao Z, Wang M, Blair D, Zheng Y, Dou Y. 2014 Phylogenetic analysis of the endoribonuclease Dicer family. PLoS ONE 9, e95350. (doi:10.1371/journal.pone.0095350)
148. Tolia NH, Joshua-Tor L. 2007 Slicer and the Argonautes. Nat. Chem. Biol. 3, 36–43. (doi:10.1038/nchembio848)
149. Hock J, Meister G. 2008 The Argonaute protein family. Genome Biol. 9, 210. (doi:10.1186/gb-2008-9-2-210)
150. Court DL, Gan J, Liang YH, Shaw GX, Tropea JE, Costantino N, Waugh DS, Ji X. 2013 RNase III: Genetics and function; structure and mechanism. Annu. Rev. Genet. 47, 405–431. (doi:10.1146/annurev-genet-110711-155618)
151. Lestini R, Duan Z, Allers T. 2010 The archaeal Xpf/Mus81/FANCM homolog Hef and the Holliday junction resolvase Hjc define alternative pathways that are essential for cell viability in Haloferax volcanii. DNA Repair (Amst) 9, 994–1002. (doi:10.1016/j.dnarep.2010.06.012)
152. Makarova KS, Wolf YI, van der Oost J, Koonin EV. 2009 Prokaryotic homologs of Argonaute proteins are predicted to function as key components of a novel system of defense against mobile genetic elements. Biol. Direct 4, 29. (doi:10.1186/1745-6150-4-29)
153. Swarts DC, Makarova K, Wang Y, Nakanishi K, Ketting RF, Koonin EV, Patel DJ, van der Oost J. 2014 The evolutionary journey of Argonaute proteins. Nat. Struct. Mol. Biol. 21, 743–753. (doi:10.1038/nsmb.2879)
154. Olovnikov I, Chan K, Sachidanandam R, Newman DK, Aravin AA. 2013 Bacterial Argonaute samples the transcriptome to identify foreign DNA. Mol. Cell 51, 594–605. (doi:10.1016/j.molcel.2013.08.014)
155. Swarts DC et al. 2014 DNA-guided DNA interference by a prokaryotic Argonaute. Nature 507, 258–261. (doi:10.1038/nature12971)
156. Hur JK, Olovnikov I, Aravin AA. 2014 Prokaryotic Argonautes defend genomes against invasive DNA. Trends Biochem. Sci. 39, 257–259. (doi:10.1016/j.tibs.2014.04.006)
157. Iyer LM, Koonin EV, Aravind L. 2003 Evolutionary connection between the catalytic subunits of DNAdependent RNA polymerases and eukaryotic RNAdependent RNA polymerases and the origin of RNA polymerases. BMC Struct. Biol. 3, 1. (doi:10.1186/1472-6807-3-1)
158. Hurley JH. 2010 The ESCRT complexes. Crit. Rev. Biochem. Mol. Biol. 45, 463–487. (doi:10.3109/10409238.2010.502516)
159. Esser C, Martin W, Dagan T. 2007 The origin of mitochondria in light of a fluid prokaryotic chromosome model. Biol. Lett. 3, 180–184. (doi:10.1098/rsbl.2006.0582)
160. Ku C, Nelson-Sathi S, Roettger M, Garg S, Hazkani- Covo E, Martin WF. In press. Endosymbiotic gene transfer from prokaryotic pangenomes: inherited chimerism in eukaryotes. Proc. Natl Acad. Sci. USA. (doi:10.1073/pnas.1421385112)
161. Spang A et al. 2015 Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521, 173–179. (doi:10.1038/nature14447)
162. Embley TM, Williams TA. 2015 Evolution: steps on the road to eukaryotes. Nature 521, 169–170. (doi:10.1038/nature14522)