A phylogenomic data-driven exploration of viral origins and evolution

Science Advances

Volumn 1, Issue 8, 2015, Pages

  Nasir, Arshan ^a,b   Caetano Anollés, Gustavo ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b COMSATS Institute of Information Technology ^*  (Pakistan)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; CYTOLOGY; GENES; PROTEINS;

DATA DRIVEN; FUNCTIONAL DATAS; GENETIC INFORMATION; HORIZONTAL TRANSFER; RNA GENOME; STRUCTURAL DOMAINS; STRUCTURAL EVIDENCE; TREE OF LIFE;

VIRUSES;

EID: 84976496712     PISSN: None     EISSN: 23752548     Source Type: Journal    
DOI: 10.1126/sciadv.1500527     Document Type: Article

References (137)

1. E. Domingo, J. J. Holland, RNA virus mutations and fitness for survival. Annu. Rev. Microbiol. 51, 151–178 (1997).
2. A. M. Q. King, M. J. Adams, E. B. Carstens, E. J. Lefkowitz, Virus Taxonomy: Classification and Nomenclature of Viruses: Ninth Report of the International Committee on Taxonomy of Viruses (Elsevier, San Diego, CA, 2012).
3. M. Krupovic, D. H. Bamford, Double-stranded DNA viruses: 20 families and only five different architectural principles for virion assembly. Curr. Opin. Virol. 1, 118–124 (2011).
4. S. Balaji, N. Srinivasan, Comparison of sequence-based and structure-based phylogenetic trees of homologous proteins: Inferences on protein evolution. J. Biosci. 32, 83–96 (2007).
5. A. Abroi, J. Gough, Are viruses a source of new protein folds for organisms? Virosphere structure space and evolution. Bioessays 33, 626–635 (2011).
6. S. Balaji, N. Srinivasan, Use of a database of structural alignments and phylogenetic trees in investigating the relationship between sequence and structural variability among homologous proteins. Protein Eng. 14, 219–226 (2001).
7. T. J. P. Hubbard, T. L. Blundell, Comparison of solvent-inaccessible cores of homologous proteins: Definitions useful for protein modelling. Protein Eng. 1, 159–171 (1987).
8. C. Chothia, A. M. Lesk, The relation between the divergence of sequence and structure in proteins. EMBO J. 5, 823–826 (1986).
9. A. G. Murzin, S. E. Brenner, T. Hubbard, C. Chothia, SCOP: A structural classification of proteins database for the investigation of sequences and structures. J. Mol. Biol. 247, 536–540 (1995).
10. A. E. Todd, C. A. Orengo, J. M. Thornton, Evolution of function in protein superfamilies, from a structural perspective. J. Mol. Biol. 307, 1113–1143 (2001).
11. D. Lundin, A. M. Poole, B.-M. Sjöberg, M. Högbom, Use of structural phylogenetic networks for classification of the ferritin-like superfamily. J. Biol. Chem. 287, 20565–20575 (2012).
12. D. Caetano-Anollés, K. M. Kim, J. E. Mittenthal, G. Caetano-Anollés, Proteome evolution and the metabolic origins of translation and cellular life. J. Mol. Evol. 72, 14–33 (2011).
13. C. O’Donovan, M. J. Martin, A. Gattiker, E. Gasteiger, A. Bairoch, R. Apweiler, High-quality protein knowledge resource: SWISS-PROT and TrEMBL. Brief. Bioinform. 3, 275–284 (2002).
14. K. Illergård, D. H. Ardell, A. Elofsson, Structure is three to ten times more conserved than sequence—A study of structural response in protein cores. Proteins 77, 499–508 (2009).
15. J. Gough, Convergent evolution of domain architectures (is rare). Bioinformatics 21, 1464–1471 (2005).
16. G. Caetano-Anollés, A. Nasir, Benefits of using molecular structure and abundance in phylogenomic analysis. Front. Genet. 3, 172 (2012).
17. A. Harish, A. Tunlid, C. G. Kurland, Rooted phylogeny of the three superkingdoms. Biochimie 95, 1593–1604 (2013).
18. M. Wang, L. S. Yafremava, D. Caetano-Anollés, J. E. Mittenthal, G. Caetano-Anollés, Reductive evolution of architectural repertoires in proteomes and the birth of the tripartite world. Genome Res. 17, 1572–1585 (2007).
19. A. Nasir, K. M. Kim, G. Caetano-Anolles, Giant viruses coexisted with the cellular ancestors and represent a distinct supergroup along with superkingdoms Archaea, Bacteria and Eukarya. BMC Evol. Biol. 12, 156 (2012).
20. J. Gough, K. Karplus, R. Hughey, C. Chothia, Assignment of homology to genome sequences using a library of hidden Markov models that represent all proteins of known structure. J. Mol. Biol. 313, 903–919 (2001).
21. P. Forterre, The virocell concept, in: eLS (Wiley, Chichester, UK, 2012).
22. P. Forterre, Manipulation of cellular syntheses and the nature of viruses: The virocell concept. C. R. Chim. 14, 392–399 (2011).
23. D. Baltimore, Expression of animal virus genomes. Bacteriol. Rev. 35, 235–241 (1971).
24. V. A. Kostyuchenko, G. A. Navruzbekov, L. P. Kurochkina, S. V. Strelkov, V. V. Mesyanzhinov, M. G. Rossmann, The structure of bacteriophage T4 gene product 9: The trigger for tail contraction. Structure 7, 1213–1222 (1999).
25. J. Liu, G. Glazko, A. Mushegian, Protein repertoire of double-stranded DNA bacteriophages. Virus Res. 117, 68–80 (2006).
26. J. Grimes, A. K. Basak, P. Roy, D. Stuart, The crystal structure of bluetongue virus VP7. Nature 373, 167–170 (1995).
27. M. Mathieu, I. Petitpas, J. Navaza, J. Lepault, E. Kohli, P. Pothier, B. V. Venkataram Prasad, J. Cohen, F. A. Rey, Atomic structure of the major capsid protein of rotavirus: Implications for the architecture of the virion. EMBO J. 20, 1485–1497 (2001).
28. P. B. Rosenthal, X. Zhang, F. Formanowski, W. Fitz, C.-H. Wong, H. Meier-Ewert, J. J. Skehel, D. C. Wiley, Structure of the haemagglutinin-esterase-fusion glycoprotein of influenza C virus. Nature 396, 92–96 (1998).
29. Y. Ha, D. J. Stevens, J. J. Skehel, D. C. Wiley, H5 avian and H9 swine influenza virus haemag-glutinin structures: Possible origin of influenza subtypes. EMBO J. 21, 865–875 (2002).
30. N. Yutin, Y. I. Wolf, E. V. Koonin, Origin of giant viruses from smaller DNA viruses not from a fourth domain of cellular life. Virology 466–467, 38–52 (2014).
31. R. W. Hendrix, J. G. Lawrence, G. F. Hatfull, S. Casjens, The origins and ongoing evolution of viruses. Trends Microbiol. 8, 504–508 (2000).
32. J. Filée, P. Forterre, Viral proteins functioning in organelles: A cryptic origin? Trends Microbiol. 13, 510–513 (2005).
33. H. Brüssow, C. Canchaya, W.-D. Hardt, Phages and the evolution of bacterial pathogens: From genomic rearrangements to lysogenic conversion. Microbiol. Mol. Biol. Rev. 68, 560–602 (2004).
34. P. Forterre, D. Prangishvili, The major role of viruses in cellular evolution: Facts and hypotheses. Curr. Opin. Virol. 3, 558–565 (2013).
35. E. V. Koonin, V. V. Dolja, A virocentric perspective on the evolution of life. Curr. Opin. Virol. 3, 546–557 (2013).
36. M. Wang, C. G. Kurland, G. Caetano-Anollés, Reductive evolution of proteomes and protein structures. Proc. Natl. Acad. Sci. U.S.A. 108, 11954–11958 (2011).
37. J. P. McCutcheon, N. A. Moran, Extreme genome reduction in symbiotic bacteria. Nat. Rev. Microbiol. 10, 13–26 (2011).
38. A. Nasir, A. Naeem, M. J. Khan, H. D. L. Nicora, G. Caetano-Anollés, Annotation of protein domains reveals remarkable conservation in the functional make up of proteomes across superkingdoms. Genes 2, 869–911 (2011).
39. N. A. Moran, Microbial minimalism: Genome reduction in bacterial pathogens. Cell 108, 583–586 (2002).
40. C. I. Bandea, A new theory on the origin and the nature of viruses. J. Theor. Biol. 105, 591–602 (1983).
41. C. I. Bandea, The origin and evolution of viruses as molecular organisms. Nat. Preceedings 10101/npre.2009.3886.1 (2009).
42. J.-M. Claverie, C. Abergel, Open questions about giant viruses. Adv. Virus Res. 85, 25–56 (2013).
43. A. Nasir, F.-J. Sun, K. M. Kim, G. Caetano-Anollés, Untangling the origin of viruses and their impact on cellular evolution. Ann. N. Y. Acad. Sci. 1341, 61–74 (2015).
44. A. Nasir, P. Forterre, K. M. Kim, G. Caetano-Anollés, The distribution and impact of viral lineages in domains of life. Front. Microbiol. 5, 194 (2014).
45. E. V. Koonin, V. V. Dolja, M. Krupovic, Origins and evolution of viruses of eukaryotes: The ultimate modularity. Virology 479–480, 2–25 (2015).
46. P. Forterre, The common ancestor of Archaea and Eukarya was not an archaeon. Archaea 2013, 372396 (2013).
47. N. G. A. Abrescia, D. H. Bamford, J. M. Grimes, D. I. Stuart, Structure unifies the viral universe. Annu. Rev. Biochem. 81, 795–822 (2012).
48. M. Sutter, D. Boehringer, S. Gutmann, S. Günther, D. Prangishvili, M. J. Loessner, K. O. Stetter, E. Weber-Ban, N. Ban, Structural basis of enzyme encapsulation into a bacterial nanocompartment. Nat. Struct. Mol. Biol. 15, 939–947 (2008).
49. P. Forterre, D. Prangishvili, The origin of viruses. Res. Microbiol. 160, 466–472 (2009).
50. T. O. Yeates, Y. Tsai, S. Tanaka, M. R. Sawaya, C. A. Kerfeld, Self-assembly in the carboxysome: A viral capsid-like protein shell in bacterial cells. Biochem. Soc. Trans. 35, 508–511 (2007).
51. T. O. Yeates, M. C. Thompson, T. A. Bobik, The protein shells of bacterial microcompartment organelles. Curr. Opin. Struct. Biol. 21, 223–231 (2011).
52. S. Dutta, I. V. Akey, C. Dingwall, K. L. Hartman, T. Laue, R. T. Nolte, J. F. Head, C. W. Akey, The crystal structure of nucleoplasmin-core: Implications for histone binding and nucleo-some assembly. Mol. Cell 8, 841–853 (2001).
53. M. Mizuno, K. Yasukawa, K. Inouye, Insight into the mechanism of the stabilization of Moloney murine leukaemia virus reverse transcriptase by eliminating RNase H activity. Biosci. Biotechnol. Biochem. 74, 440–442 (2010).
54. M. S. Chapman, L. Liljas, Structural folds of viral proteins. Adv. Protein Chem. 64, 125–196 (2003).
55. G. S. Diemer, K. M. Stedman, A novel virus genome discovered in an extreme environment suggests recombination between unrelated groups of RNA and DNA viruses. Biol. Direct 7, 13 (2012).
56. M. Wang, Y.-Y. Jiang, K. Mo Kim, G. Qu, H.-F. Ji, J. E. Mittenthal, H.-Y. Zhang, G. Caetano-Anollés, A universal molecular clock of protein folds and its power in tracing the early history of aerobic metabolism and planet oxygenation. Mol. Biol. Evol. 28, 567–582 (2011).
57. K. M. Kim, G. Caetano-Anollés, The proteomic complexity and rise of the primordial ancestor of diversified life. BMC Evol. Biol. 11, 140 (2011).
58. J. P. Gogarten, H. Kibak, P. Dittrich, L. Taiz, E. J. Bowman, B. J. Bowman, M. F. Manolson, R. J. Poole, T. Date, T. Oshima, Evolution of the vacuolar H+-ATPase: Implications for the origin of eukaryotes. Proc. Natl. Acad. Sci. U.S.A. 86, 6661–6665 (1989).
59. J. P. Gogarten, L. Olendzenski, Orthologs, paralogs and genome comparisons. Curr. Opin. Genet. Dev. 9, 630–636 (1999).
60. C. R. Woese, O. Kandler, M. L. Wheelis, Towards a natural system of organisms: Proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl. Acad. Sci. U.S.A. 87, 4576–4579 (1990).
61. J. T.-F. Wong, J. Chen, W.-K. Mat, S.-K. Ng, H. Xue, Polyphasic evidence delineating the root of life and roots of biological domains. Gene 403, 39–52 (2007).
62. H. Xue, K.-L. Tong, C. Marck, H. Grosjean, J. T.-F. Wong, Transfer RNA paralogs: Evidence for genetic code–amino acid biosynthesis coevolution and an archaeal root of life. Gene 310, 59–66 (2003).
63. H. Xue, S.-K. Ng, K.-L. Tong, J. T.-F. Wong, Congruence of evidence for a Methanopyrus-proximal root of life based on transfer RNA and aminoacyl-tRNA synthetase genes. Gene 360, 120–130 (2005).
64. K. M. Kim, G. Caetano-Anollés, The evolutionary history of protein fold families and proteomes confirms that the archaeal ancestor is more ancient than the ancestors of other superkingdoms. BMC Evol. Biol. 12, 13 (2012).
65. K. M. Kim, A. Nasir, K. Hwang, G. Caetano-Anollés, A tree of cellular life inferred from a genomic census of molecular functions. J. Mol. Evol. 79, 240–262 (2014).
66. P. Forterre, The two ages of the RNA world, and the transition to the DNA world: A story of viruses and cells. Biochimie 87, 793–803 (2005).
67. G. R. Burke, M. R. Strand, Polydnaviruses of parasitic wasps: Domestication of viruses to act as gene delivery vectors. Insects 3, 91–119 (2012).
68. D. Prangishvili, M. Krupovic, A new proposed taxon for double-stranded DNA viruses, the order “Ligamenvirales”. Arch. Virol. 157, 791–795 (2012).
69. N. Philippe, M. Legendre, G. Doutre, Y. Couté, O. Poirot, M. Lescot, D. Arslan, V. Seltzer, L. Bertaux, C. Bruley, J. Garin, J. M. Claverie, C. Abergel, Pandoraviruses: Amoeba viruses with genomes up to 2.5 Mb reaching that of parasitic eukaryotes. Science 341, 281–286 (2013).
70. M. Legendre, J. Bartoli, L. Shmakova, S. Jeudy, K. Labadie, A. Adrait, M. Lescot, O. Poirot, L. Bertaux, C. Bruley, Y. Couté, E. Rivkina, C. Abergel, J.-M. Claverie, Thirty-thousand-year-old distant relative of giant icosahedral DNA viruses with a pandoravirus morphology. Proc. Natl. Acad. Sci. U.S.A. 111, 4274–4279 (2014).
71. P. Colson, X. De Lamballerie, N. Yutin, S. Asgari, Y. Bigot, D. K. Bideshi, X.-W. Cheng, B. A. Federici, J. L. Van Etten, E. V. Koonin, B. La Scola, D. Raoult, “Megavirales”, a proposed new order for eukaryotic nucleocytoplasmic large DNA viruses. Arch. Virol. 158, 2517–2521 (2013).
72. M. L. Baker, W. Jiang, F. J. Rixon, W. Chiu, Common ancestry of herpesviruses and tailed DNA bacteriophages. J. Virol. 79, 14967–14970 (2005).
73. A. Nasir, K. M. Kim, G. Caetano-Anollés, Viral evolution: Primordial cellular origins and late adaptation to parasitism. Mob. Genet. Elements 2, 247–252 (2012).
74. D. Wu, M. Wu, A. Halpern, D. B. Rusch, S. Yooseph, M. Frazier, J. C. Venter, J. A. Eisen, Stalking the fourth domain in metagenomic data: Searching for, discovering, and interpreting novel, deep branches in marker gene phylogenetic trees. PLOS One 6, e18011 (2011).
75. M. Boyer, M.-A. Madoui, G. Gimenez, B. La Scola, D. Raoult, Phylogenetic and phyletic studies of informational genes in genomes highlight existence of a 4th domain of life including giant viruses. PLOS One 5, e15530 (2010).
76. D. Moreira, P. López-García, Ten reasons to exclude viruses from the tree of life. Nat. Rev. Microbiol. 7, 306–311 (2009).
77. D. Moreira, C. Brochier-Armanet, Giant viruses, giant chimeras: The multiple evolutionary histories of Mimivirus genes. BMC Evol. Biol. 8, 12 (2008).
78. D. Moreira, P. López-García, Comment on “The 1.2-megabase genome sequence of Mimivirus”. Science 308, 1114 (2005).
79. E. V. Koonin, On the origin of cells and viruses: Primordial virus world scenario. Ann. N. Y. Acad. Sci. 1178, 47–64 (2009).
80. E. V. Koonin, T. G. Senkevich, V. V. Dolja, The ancient Virus World and evolution of cells. Biol. Direct 1, 29 (2006).
81. D. Raoult, P. Forterre, Redefining viruses: Lessons from Mimivirus. Nat. Rev. Microbiol. 6, 315–319 (2008).
82. J.-M. Claverie, H. Ogata, Ten good reasons not to exclude giruses from the evolutionary picture. Nat. Rev. Microbiol. 7, 615 (2009).
83. J.-M. Claverie, H. Ogata, S. Audic, C. Abergel, K. Suhre, P.-E. Fournier, Mimivirus and the emerging concept of “giant” virus. Virus Res. 117, 133–144 (2006).
84. P. López-García, The place of viruses in biology in light of the metabolism- versus-replication-first debate. Hist. Philos. Life Sci. 34, 391–406 (2012).
85. R. R. Novoa, G. Calderita, R. Arranz, J. Fontana, H. Granzow, C. Risco, Virus factories: Associations of cell organelles for viral replication and morphogenesis. Biol. Cell 97, 147–172 (2005).
86. J.-M. Claverie, Viruses take center stage in cellular evolution. Genome Biol. 7, 110 (2006).
87. N. R. Hegde, M. S. Maddur, S. V. Kaveri, J. Bayry, Reasons to include viruses in the tree of life. Nat. Rev. Microbiol. 7, 615 (2009).
88. D. Wacey, M. R. Kilburn, M. Saunders, J. Cliff, M. D. Brasier, Microfossils of sulphur-metabolizing cells in 3.4-billion-year-old rocks of Western Australia. Nat. Geosci. 4, 698–702 (2011).
89. E. J. Javaux, C. P. Marshall, A. Bekker, Organic-walled microfossils in 3.2-billion-year-old shallow-marine siliciclastic deposits. Nature 463, 934–938 (2010).
90. P. Forterre, The origin of viruses and their possible roles in major evolutionary transitions. Virus Res. 117, 5–16 (2006).
91. B. La Scola, S. Audic, C. Robert, L. Jungang, X. de Lamballerie, M. Drancourt, R. Birtles, J. M. Claverie, D. Raoult, A giant virus in amoebae. Science 299, 2033 (2003).
92. D. Arslan, M. Legendre, V. Seltzer, C. Abergel, J.-M. Claverie, Distant Mimivirus relative with a larger genome highlights the fundamental features of Megaviridae. Proc. Natl. Acad. Sci. U.S.A. 108, 17486–17491 (2011).
93. D. G. Meckes Jr., N. Raab-Traub, Microvesicles and viral infection. J. Virol. 85, 12844–12854 (2011).
94. M. Jalasvuori, J. K. Bamford, Structural co-evolution of viruses and cells in the primordial world. Orig. Life Evol. Biosph. 38, 165–181 (2008).
95. P. Forterre, M. Krupovic, in Viruses: Essential Agents of Life, G. Witzany, Ed. (Springer, Dordrecht, Netherlands, 2012), pp. 43–60.
96. P. Forterre, The origin of DNA genomes and DNA replication proteins. Curr. Opin. Microbiol. 5, 525–532 (2002).
97. H. Ogata, J.-M. Claverie, Unique genes in giant viruses: Regular substitution pattern and anomalously short size. Genome Res. 17, 1353–1361 (2007).
98. D. Prangishvili, R. A. Garrett, E. V. Koonin, Evolutionary genomics of archaeal viruses: Unique viral genomes in the third domain of life. Virus Res. 117, 52–67 (2006).
99. Y. Yin, D. Fischer, Identification and investigation of ORFans in the viral world. BMC Genomics 9, 24 (2008).
100. D. Cortez, P. Forterre, S. Gribaldo, A hidden reservoir of integrative elements is the major source of recently acquired foreign genes and ORFans in archaeal and bacterial genomes. Genome Biol. 10, R65 (2009).
101. P. Forterre, 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. U.S.A. 103, 3669–3674 (2006).
102. P. Forterre, D. Prangishvili, The great billion-year war between ribosome- and capsid-encoding organisms (cells and viruses) as the major source of evolutionary novelties. Ann. N. Y. Acad. Sci. 1178, 65–77 (2009).
103. H. Liu, Y. Fu, D. Jiang, G. Li, J. Xie, J. Cheng, Y. Peng, S. A. Ghabrial, X. Yi, Widespread horizontal gene transfer from double-stranded RNA viruses to eukaryotic nuclear genomes. J. Virol. 84, 11876–11887 (2010).
104. T. E. Shutt, M. W. Gray, Bacteriophage origins of mitochondrial replication and transcription proteins. Trends Genet. 22, 90–95 (2006).
105. A. Katzourakis, R. J. Gifford, Endogenous viral elements in animal genomes. PLOS Genet. 6, e1001191 (2010).
106. S. Mi, X. Lee, X. Li, G. M. Veldman, H. Finnerty, L. Racie, E. LaVallie, X. Y. Tang, P. Edouard, S. Howes, J. C. Keith Jr., J. M. McCoy, Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403, 785–789 (2000).
107. C. R. Woese, Evolution from Molecules to Men (Cambridge Univ. Press, Cambridge, UK, 1983), pp. 209–233.
108. D. Lundin, S. Gribaldo, E. Torrents, B. M. Sjoberg, A. M. Poole, Ribonucleotide reduction—Horizontal transfer of a required function spans all three domains. BMC Evol. Biol. 10, 383 (2010).
109. P. López-García, D. Moreira, Metabolic symbiosis at the origin of eukaryotes. Trends Biochem. Sci. 24, 88–93 (1999).
110. W. Martin, M. Müller, The hydrogen hypothesis for the first eukaryote. Nature 392, 37–41 (1998).
111. C. J. Cox, P. G. Foster, R. P. Hirt, S. R. Harris, T. M. Embley, The archaebacterial origin of eukaryotes. Proc. Natl. Acad. Sci. U.S.A. 105, 20356–20361 (2008).
112. T. A. Williams, P. G. Foster, T. M. W. Nye, C. J. Cox, T. M. Embley, A congruent phylogenomic signal places eukaryotes within the Archaea. Proc. R. Soc. B 279, 4870–4879 (2012).
113. L. Guy, T. J. G. Ettema, The archaeal ‘TACK’ superphylum and the origin of eukaryotes. Trends Microbiol. 19, 580–587 (2011).
114. S. Nelson-Sathi, T. Dagan, G. Landan, A. Janssen, M. Steel, J. O. McInerney, U. Deppenmeier, W. F. Martina, Acquisition of 1,000 eubacterial genes physiologically transformed a methano-gen at the origin of Haloarchaea. Proc. Natl. Acad. Sci. U.S.A. 109, 20537–20542 (2012).
115. A. Goulet, S. Blangy, P. Redder, D. Prangishvili, C. Felisberto-Rodrigues, P. Forterre, V. Campanacci, C. Cambillau, Acidianus filamentous virus 1 coat proteins display a helical fold spanning the filamentous archaeal viruses lineage. Proc. Natl. Acad. Sci. U.S.A. 106, 21155–21160 (2009).
116. B. Bolduc, D. P. Shaughnessy, Y. I. Wolf, E. V. Koonin, F. F. Roberto, M. Young, Identification of novel positive-strand RNA viruses by metagenomic analysis of archaea-dominated Yellowstone hot springs. J. Virol. 86, 5562–5573 (2012).
117. M. Krupovič, P. Forterre, D. H. Bamford, Comparative analysis of the mosaic genomes of tailed archaeal viruses and proviruses suggests common themes for virion architecture and assembly with tailed viruses of bacteria. J. Mol. Biol. 397, 144–160 (2010).
118. D. Prangishvili, The wonderful world of archaeal viruses. Annu. Rev. Microbiol. 67, 565–585 (2013).
119. Y. Bao, S. Federhen, D. Leipe, V. Pham, S. Resenchuk, M. Rozanov, R. Tatusov, T. Tatusova, National Center for Biotechnology Information Viral Genomes Project. J. Virol. 78, 7291–7298 (2004).
120. M. Wang, G. Caetano-Anollés, Global phylogeny determined by the combination of protein domains in proteomes. Mol. Biol. Evol. 23, 2444–2454 (2006).
121. D. L. Swofford, Phylogenomic Analysis Using Parsimony and Other Programs (PAUP∗) Ver 4.0b10 (Sinauer, Sunderland, MA, 2002).
122. J. G. Lundberg, Wagner networks and ancestors. Syst. Biol. 21, 398–413 (1972).
123. B. Kolaczkowski, J. W. Thornton, Performance of maximum parsimony and likelihood phylo-genetics when evolution is heterogeneous. Nature 431, 980–984 (2004).
124. D. H. Huson, D. C. Richter, C. Rausch, T. Dezulian, M. Franz, R. Rupp, Dendroscope: An interactive viewer for large phylogenetic trees. BMC Bioinformatics 8, 460 (2007).
125. T. Fahmy, P. Aubry, XLSTAT-Pro (Version 7.0) (Society Addinsoft, Brooklyn, NY, 2008).
126. D. Bryant, V. Moulton, Neighbor-Net: An agglomerative method for the construction of phylogenetic networks. Mol. Biol. Evol. 21, 255–265 (2004).
127. D. H. Huson, SplitsTree: Analyzing and visualizing evolutionary data. Bioinformatics 14, 68–73 (1998).
128. H. Fang, J. Gough, dcGO: Database of domain-centric ontologies on functions, phenotypes, diseases and more. Nucleic Acids Res. 41, D536–D544 (2013).
129. M. K. Pietilä, E. Roine, L. Paulin, N. Kalkkinen, D. H. Bamford, An ssDNA virus infecting archaea: A new lineage of viruses with a membrane envelope. Mol. Microbiol. 72, 307–319 (2009).
130. T. Mochizuki, M. Krupovic, G. Pehau-Arnaudet, Y. Sako, P. Forterre, D. Prangishvili, Archaeal virus with exceptional virion architecture and the largest single-stranded DNA genome. Proc. Natl. Acad. Sci. U.S.A. 109, 13386–13391 (2012).
131. C. Hulo, E. de Castro, P. Masson, L. Bougueleret, A. Bairoch, I. Xenarios, P. Le Mercier, ViralZone: A knowledge resource to understand virus diversity. Nucleic Acids Res. 39 (Suppl. 1), D576–D582 (2011).
132. A. Nasir, K. M. Kim, G. Caetano-Anollés, Global patterns of protein domain gain and loss in superkingdoms. PLOS Comput. Biol. 10, e1003452 (2014).
133. P. H. Weston, in Ontogeny and Systematics, C. J. Humphries, Ed. (Columbia Univ. Press, New York, 1988), pp. 27–56.
134. P. H. Weston, in Models in Phylogeny Reconstruction, R. W. Scotland, D. J. Siebert, D. M. Williams, Eds. (Clarendon Press, Oxford, UK, 1994), pp. 125–155.
135. G. Caetano-Anollés, M. Wang, D. Caetano-Anollés, J. E. Mittenthal, The origin, evolution and structure of the protein world. Biochem. J. 417, 621–637 (2009).
136. J. P. Huelsenbeck, R. Nielsen, Effect of nonindependent substitution on phylogenetic accuracy. Syst. Biol. 48, 317–328 (1999).
137. G. Caetano-Anollés, A. Nasir, K. Zhou, D. Caetano-Anollés, J. E. Mittenthal, F.-J. Sun, K. M. Kim, Archaea: The first domain of diversified life. Archaea 2014, 590214 (2014).