Phylogenomic test of the hypotheses for the evolutionary origin of eukaryotes

Molecular Biology and Evolution

Volumn 31, Issue 4, 2014, Pages 832-845

  Rochette, Nicolas C ^a   Brochier Armanet, Céline ^a   Gouy, Manolo ^a  

^a UNIVERSITÉ DE LYON   (France)

Author keywords

Archaea; Eukaryogenesis; Evolution; Horizontal gene transfer; Phylogeny; Tree of life

Indexed keywords

MITOCHONDRIAL PROTEIN; MITOCHONDRIAL RNA; RIBOSOME PROTEIN; SIGNAL RECOGNITION PARTICLE;

ALPHAPROTEOBACTERIA; ARCHAEON; ARTICLE; BACTERIUM; CLADISTICS; CRENARCHAEOTA; DNA REPAIR; ENDOSYMBIOSIS; EUKARYOTE; EUKARYOTE EVOLUTION; EURYARCHAEOTA; EXOSOME; GENE DUPLICATION; GENOME; HORIZONTAL GENE TRANSFER; KORARCHAEOTA; METHANOGEN; MITOCHONDRIAL GENOME; MONOPHYLY; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PHYLOGENOMICS; PHYLOGENY; PROKARYOTE; PROTEIN PROCESSING; SISTER GROUP; TAXONOMY; THAUMARCHAEOTA; THERMOPLASMATALES;

ARCHAEA; EUKARYOGENESIS; EVOLUTION; HORIZONTAL GENE TRANSFER; PHYLOGENY; TREE OF LIFE;

ARCHAEA; BACTERIA; BIOLOGICAL EVOLUTION; EVOLUTION, MOLECULAR; GENE TRANSFER, HORIZONTAL; GENETIC SPECIATION; GENOME, HUMAN; HUMANS; MODELS, GENETIC; PHYLOGENY; SYMBIOSIS; YEASTS;

EID: 84897859298     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/mst272     Document Type: Article

References (100)

1. Allers T, Mevarech M. 2005. Archaeal genetics-the third way. Nat Rev Genet. 6:58-73.
2. Alsmark C, Foster PG, Sicheritz-Ponten T, Nakjang S, Embley TM, Hirt RP. 2013. Patterns of prokaryotic lateral gene transfers affecting parasitic microbial eukaryotes. Genome Biol. 14:R19.
3. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389.
4. Atteia A, Adrait A, Brugiere S, Tardif M, van Lis R, Deusch O, Dagan T, Kuhn L, Gontero B, Martin W, et al. 2009. A proteomic survey of Chlamydomonas reinhardtii mitochondria sheds new light on the metabolic plasticity of the organelle and on the nature of the a-proteobacterial mitochondrial ancestor. Mol Biol Evol. 26: 1533-1548.
5. 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.
6. Brindefalk B, Ettema TJG, Viklund J, Thollesson M, Andersson SGE. 2011. A phylometagenomic exploration of oceanic alphaproteobacteria reveals mitochondrial relatives unrelated to the SAR11 clade. PLoS One 6:e24457.
7. Brown JR, Douady CJ, Italia MJ, Marshall WE, Stanhope MJ. 2001. Universal trees based on large combined protein sequence data sets. Nat Genet. 28:281-285.
8. Burger G, Gray MW, Forget L, Lang BF. 2013. Strikingly bacteria-like and gene-rich mitochondrial genomes throughout jakobid protists. Genome Biol Evol. 5:418-438.
9. Burki F, Flegontov P, Obornik M, Cihlar J, Pain A, Lukes J, Keeling PJ. 2012. Re-evaluating the green versus red signal in eukaryotes with secondary plastid of red algal origin. Genome Biol Evol. 4:626-635.
10. Canback B, Andersson SGE, Kurland CG. 2002. The global phylogeny of glycolytic enzymes. Proc Natl Acad Sci U S A. 99:6097-6102.
11. Cavalier-Smith T. 2002. The phagotrophic origin of eukaryotes and phylogenetic classification of protozoa. Int J Syst Evol Microbiol. 52(Pt 2): 297-354.
12. Cavalier-Smith T. 2010a. Kingdoms protozoa and chromista and the eozoan root of the eukaryotic tree. Biol Lett. 6:342-345.
13. Cavalier-Smith T. 2010b. Origin of the cell nucleus, mitosis and sex: roles of intracellular coevolution. Biol Direct. 5:7.
14. Ciccarelli FD, Tobias D, von Mering C, Creevey CJ, Snel B, Bork P. 2006. Toward automatic reconstruction of a highly resolved tree of life. Science 311:1283-1287.
15. Collins L, Penny D. 2005. Complex spliceosomal organization ancestral to extant eukaryotes. Mol Biol Evol. 22:1053-1066.
16. Cotton JA, McInerney JO. 2010. Eukaryotic genes of archaebacterial origin are more important than the more numerous eubacterial genes, irrespective of function. Proc Natl Acad Sci U S A. 107: 17252-17255.
17. Criscuolo A, Gribaldo S. 2010. BMGE (block mapping and gathering with entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol Biol. 10:210.
18. Dacks JB, Peden AA, Field MC. 2009. Evolution of specificity in the eukaryotic endomembrane system. Int J Biochem Cell Biol. 41: 330-340.
19. De Craene J-O, Ripp R, Lecompte O, Thompson J, Poch O, Friant S. 2012. Evolutionary analysis of the ENTH/ANTH/VHS protein superfamily reveals a coevolution between membrane trafficking and metabolism. BMC Genomics 13:297.
20. de Duve C. 2007. The origin of eukaryotes: a reappraisal. Nat Rev Genet. 8:395-403.
21. Derelle R, Lang BF. 2012. Rooting the eukaryotic tree with mitochondrial and bacterial proteins. Mol Biol Evol. 29:1277-1289.
22. Devos DP, Reynaud EG. 2010. Intermediate steps. Science 330: 1187-1188.
23. Do CB, Mahabhashyam MSP, Brudno M, Batzoglou S. 2005. ProbCons: probabilistic consistency-based multiple sequence alignment. Genome Res. 15:330-340.
24. Doolittle WF. 1978. Genes in pieces: were they ever together?. Nature 272:581-582.
25. Doolittle WF. 1998. You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet. 4:307-311.
26. Dutheil J, Gaillard S, Bazin E, Glé min S, Ranwez V, Galtier N, Belkhir K. 2006. Bio++: a set of c++ libraries for sequence analysis, phylogenetics, molecular evolution and population genetics. BMC Bioinformatics 7:188.
27. Eddy SR. 2011. Accelerated Profile HMM Searches. PLoS Comput Biol. 7: e1002195.
28. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
29. Embley TM, Martin W. 2006. Eukaryotic evolution, changes and challenges. Nature 440:623-630.
30. Eme L, TrillesA,Moreira D, Brochier-Armanet C. 2011. The phylogenomic analysis of the anaphase promoting complex and its targets points to complex and modern-like control of the cell cycle in the last common ancestor of eukaryotes. BMC Evol Biol. 11:265.
31. Esser C, Ahmadinejad N, Wiegand C, Rotte C, Sebastiani F, Gelius- Dietrich G, Henze K, Kretschmann E, Richly E, Leister D, et al. 2004. A genome phylogeny for mitochondria among alphaproteobacteria and a predominantly eubacterial ancestry of yeast nuclear genes. Mol Biol Evol. 21:1643-1660.
32. Esser C, MartinW, Dagan T. 2007. The origin of mitochondria in light of a fluid prokaryotic chromosome model. Biol Lett. 3:180-184.
33. Forterre P. 2011. A new fusion hypothesis for the origin of eukarya: better than previous ones, but probably also wrong. Res Microbiol. 162:77-91.
34. Gabaldón T, Huynen MA. 2007. From endosymbiont to host-controlled organelle: the hijacking of mitochondrial protein synthesis and metabolism. PLoS Comput Biol. 3:e219.
35. Godde JS. 2012. Breaking through a phylogenetic impasse: a pair of associated archaea might have played host in the endosymbiotic origin of eukaryotes. Cell Biosci. 2:29.
36. Grabowski B, Kelman Z. 2003. Archeal DNA replication: eukaryal proteins in a bacterial context. Annu Rev Microbiol. 57:487-516.
37. Gribaldo S, Brochier-Armanet C. 2006. The origin and evolution of archaea: a state of the art. Philos Trans R Soc Lond B Biol Sci. 361: 1007-1022.
38. 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.
39. Guldan H, Matysik F-M, Bocola M, Sterner R, Babinger P. 2011. Functional assignment of an enzyme that catalyzes the synthesis of an archaea-type ether lipid in bacteria. Angew Chem Int Ed Engl. 50:8188-8191.
40. Gupta RS, Golding GB. 1996. The origin of the eukaryotic cell. Trends Biochem Sci. 21:166-171.
41. Guy L, Ettema TJG. 2011. The archaeal 'TACK' superphylum and the origin of eukaryotes. Trends Microbiol. 19:580-587.
42. Hammesfahr B, Kollmar M. 2012. Evolution of the eukaryotic dynactin complex, the activator of cytoplasmic dynein. BMC Evol Biol. 12:95.
43. Hampl V, Hug L, Leigh JW, Dacks JB, Lang BF, Simpson AGB, Roger AJ. 2009. Phylogenomic analyses support the monophyly of excavata and resolve relationships among eukaryotic "supergroups". Proc Natl Acad Sci U S A. 106:3859-3864.
44. Hampl V, Stairs CW, Roger AJ. 2011. The tangled past of eukaryotic enzymes involved in anaerobic metabolism. Mob Genet Elements. 1: 71-74.
45. Horiike T, Hamada K, Kanaya S, Shinozawa T. 2001. Origin of eukaryotic cell nuclei by symbiosis of archaea in bacteria is revealed by homology- hit analysis. Nat Cell Biol. 3:210-214.
46. Horiike T, Hamada K, Miyata D, Shinozawa T. 2004. The origin of eukaryotes is suggested as the symbiosis of Pyrococcus into g-proteobacteria by phylogenetic tree based on gene content. J Mol Evol. 59:606-619.
47. Iyer LM, Anantharaman V, Wolf MY, Aravind L. 2008. Comparative genomics of transcription factors and chromatin proteins in parasitic protists and other eukaryotes. Int J Parasitol. 38:1-31.
48. Jékely G. 2003. Small GTPases and the evolution of the eukaryotic cell. Bioessays 25:1129-1138.
49. Kandler O, König H. 1998. Cell wall polymers in archaea (archaebacteria). Cell Mol Life Sci. 54:305-308.
50. Katoh K, Toh H. 2008. Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform. 9:286-298.
51. Keeling PJ, Palmer JD. 2008. Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet. 9:605-618.
52. 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 Biol Sci. 278: 1009-1018.
53. Koonin EV. 2010. The origin and early evolution of eukaryotes in the light of phylogenomics. Genome Biol. 11:209.
54. Küper U, Meyer C, Müller V, Rachel R, Huber H. 2010. Energized outer membrane and spatial separation of metabolic processes in the hyperthermophilic archaeon ignicoccus hospitalis. Proc Natl Acad Sci U S A. 107:3152-3156.
55. Lake JA, Rivera MC. 1994. Was the nucleus the first endosymbiont?. Proc Natl Acad Sci U S A. 91:2880-2881.
56. 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.
57. Le SQ, Gascuel O, Lartillot N. 2008. Empirical profile mixture models for phylogenetic reconstruction. Bioinformatics 24:2317-2323.
58. Le SQ, Lartillot N, Gascuel O. 2008. Phylogenetic mixture models for proteins. Philos Trans R Soc Lond B Biol Sci. 363:3965-3976.
59. Lester L, Meade A, Pagel M. 2006. The slow road to the eukaryotic genome. Bioessays 28:57-64.
60. Lopez-Garcia P, Moreira D. 2006. Selective forces for the origin of the eukaryotic nucleus. Bioessays 28:525-533.
61. Makarova KS. 2005. Ancestral paralogs and pseudoparalogs and their role in the emergence of the eukaryotic cell. Nucleic Acids Res. 33: 4626-4638.
62. 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.
63. Marcet-Houben M, Gabaldón T. 2010. Acquisition of prokaryotic genes by fungal genomes. Trends Genet. 26:5-8.
64. Margulis L, Dolan MF, Guerrero R. 2000. The chimeric eukaryote: origin of the nucleus from the karyomastigont in amitochondriate protists. Proc Natl Acad Sci U S A. 97:6954-6959.
65. Martijn J, Ettema TJG. 2013. From archaeon to eukaryote: the evolutionary dark ages of the eukaryotic cell. Biochem Soc Trans. 41: 451-457.
66. Martin W. 1999. Mosaic bacterial chromosomes: a challenge en route to a tree of genomes. Bioessays 21:99-104.
67. Martin W, Müller M. 1998. The hydrogen hypothesis for the first eukaryote. Nature 392:37-41.
68. Miele V, Penel S, Daubin V, Picard F, Kahn D, Duret L. 2012. High-quality sequence clustering guided by network topology andmultiple alignment likelihood. Bioinformatics 28:1078-1085.
69. Neumann N, Lundin D, Poole AM. 2010. Comparative genomic evidence for a complete nuclear pore complex in the last eukaryotic common ancestor. PLoS One 5:e13241.
70. Penel S, Arigon A-M, Dufayard J-F, Sertier A-S, Daubin V, Duret L, Gouy M, Perriére G. 2009. Databases of homologous gene families for comparative genomics. BMC Bioinformatics 10(Suppl 6):S3.
71. Penn O, Privman E, Landan G, Graur D, Pupko T. 2010. An alignment confidence score capturing robustness to guide tree uncertainty. Mol Biol Evol. 27:1759-1767.
72. Pereto J, Lopez-Garcia P, Moreira D. 2004. Ancestral lipid biosynthesis and early membrane evolution. Trends Biochem Sci. 29:469-477.
73. Pisani D, Cotton JA, McInerney JO. 2007. Supertrees disentangle the chimerical origin of eukaryotic genomes.Mol Biol Evol. 24:1752-1760.
74. Poole AM, Neumann N. 2011. Reconciling an archaeal origin of eukaryotes with engulfment: a biologically plausible update of the eocyte hypothesis. Res Microbiol. 162:71-76.
75. Price MN, Dehal PS, Arkin AP. 2010. FastTree 2-approximately maximum- likelihood trees for large alignments. PLoS One 5:e9490.
76. Ramesh MA,Malik S-B, Logsdon JM. 2005. A phylogenomic inventory of meiotic genes; evidence for sex in giardia and an early eukaryotic origin of meiosis. Curr Biol. 15:185-191.
77. Reeve JN. 2003. Archaeal chromatin and transcription. MolMicrobiol. 48: 587-598.
78. Rivera MC, Jain R, Moore JE, Lake JA. 1998. Genomic evidence for two functionally distinct gene classes. Proc Natl Acad Sci U S A. 95: 6239-6244.
79. Rivera MC, Lake JA. 2004. The ring of life provides evidence for a genome fusion origin of eukaryotes. Nature 431:152-155.
80. Robbertse B, Yoder RJ, Boyd A, Reeves J, Spatafora JW. 2011. Hal: an automated pipeline for phylogenetic analyses of genomic data. PLoS Curr. 3:RRN1213.
81. Roger AJ, Simpson AG. 2009. Evolution: revisiting the root of the eukaryote tree. Curr Biol. 19:R165-R167.
82. Rogozin IB, Basu MK, Csuros M, Koonin EV. 2009. Analysis of rare genomic changes does not support the unikont-bikont phylogeny and suggests cyanobacterial symbiosis as the point of primary radiation of eukaryotes. Genome Biol Evol. 1:99-113.
83. Saruhashi S, Hamada K, Miyata D, Horiike T, Shinozawa T. 2008. Comprehensive analysis of the origin of eukaryotic genomes. Genes Genet Syst. 83:285-291.
84. Searcy DG. 2003. Metabolic integration during the evolutionary origin of mitochondria. Cell Res. 13:229-238.
85. Shimada H, Yamagishi A. 2011. Stability of heterochiral hybrid membrane made of bacterial sn-G3P lipids and archaeal sn-G1P lipids. Biochemistry 50:4114-4120.
86. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690.
87. Staub E, Fiziev P, Rosenthal A, Hinzmann B. 2004. Insights into the evolution of the nucleolus by an analysis of its protein domain repertoire. Bioessays 26:567-581.
88. Szklarczyk R, Huynen MA. 2010. Mosaic origin of the mitochondrial proteome. Proteomics 10:4012-4024.
89. Talavera G, Castresana J. 2007. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol. 56:564-577.
90. Tatusov RL. 1997. A genomic perspective on protein families. Science 278:631-637.
91. 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.
92. Thrash JC, Boyd A, HuggettMJ, Grote J, Carini P, Yoder RJ, Robbertse B, Spatafora JW, Rappé MS, Giovannoni SJ. 2011. Phylogenomic evidence for a common ancestor of mitochondria and the SAR11 clade. Sci Rep. 1:13.
93. Van Dongen SM. 2000. Graph clustering by flow simulation [Ph.D. thesis]. [The Netherlands]: University of Utrecht.
94. Vellai T, Takács K, Vida G. 1998. A new aspect to the origin and evolution of eukaryotes. J Mol Evol. 46:499-507.
95. Williams TA, Foster PG, Nye TMW, Cox CJ, Embley TM. 2012. A congruent phylogenomic signal places eukaryotes within the archaea. Proc Biol Sci. 279:4870-4879.
96. Wu D, Hugenholtz P, Mavromatis K, Pukall R, Dalin E, Ivanova NN, Kunin V, Goodwin L, Wu M, Tindall BJ, et al. 2009. A phylogeny-driven genomic encyclopaedia of bacteria and archaea. Nature 462:1056-1060.
97. Yutin N, Makarova KS, Mekhedov SL, Wolf YI, Koonin EV. 2008. The deep archaeal roots of eukaryotes. Mol Biol Evol. 25: 1619-1630.
98. Yutin N,WolfMY, Wolf YI, Koonin EV. 2009. The origins of phagocytosis and eukaryogenesis. Biol Direct. 4:9.
99. Zhao S, Burki F, Bråte J, Keeling PJ, Klaveness D, Shalchian-Tabrizi K. 2012. Collodictyon-an ancient lineage in the tree of eukaryotes. Mol Biol Evol. 29:1557-1568.
100. Zhaxybayeva O, Hamel L, Raymond J, Gogarten JP. 2004. Visualization of the phylogenetic content of five genomes using dekapentagonal maps. Genome Biol. 5:R20.