Sequence and structure analysis of Distantly-related viruses reveals extensive gene transfer between viruses and hosts and among viruses

Viruses

Volumn 7, Issue 10, 2015, Pages 5388-5409

  Caprari, Silvia ^a   Metzler, Saskia ^a,b   Lengauer, Thomas ^a   Kalinina, Olga V ^a  

^a MAX PLANCK INSTITUTE FOR INFORMATICS   (Germany)

^b SAARLAND UNIVERSITY   (Germany)

Author keywords

Hemagglutinin esterase; Horizontal gene transfer; Structure comparison; Viral evolution; Viral hallmark genes

Indexed keywords

HEAT SHOCK PROTEIN 70; HEMAGGLUTININ; METHYLTRANSFERASE; PROTEINASE; RNA DIRECTED RNA POLYMERASE; VIRUS ENVELOPE PROTEIN;

ADENOVIRIDAE; AMINO ACID SEQUENCE; ARTICLE; BETAHERPESVIRINAE; BUNYAVIRIDAE; CORONAVIRIDAE; FLAVIVIRIDAE; HORIZONTAL GENE TRANSFER; HUMAN; NONHUMAN; ORTHOMYXOVIRIDAE; PHYLOGENY; SEQUENCE ALIGNMNET; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS; VIRUS CELL INTERACTION; VIRUS GENE; VIRUS GENOME; ANIMAL; BIOLOGY; DNA SEQUENCE; GENETIC RECOMBINATION; GENETICS; HOST PATHOGEN INTERACTION; MOLECULAR EVOLUTION; RNA VIRUS;

ANIMALS; COMPUTATIONAL BIOLOGY; EVOLUTION, MOLECULAR; GENE TRANSFER, HORIZONTAL; GENES, VIRAL; HOST-PATHOGEN INTERACTIONS; HUMANS; RECOMBINATION, GENETIC; RNA VIRUSES; SEQUENCE ANALYSIS, DNA;

EID: 84944810155     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v7102882     Document Type: Article

References (83)

1. Dimmock, N.; Easton, A.; Leppard, K. Introduction to Modern Virology, 6th ed.;Wiley-Blackwell: Hoboken, NJ, USA, 2009.
2. Raoult, D.; Audic, S.; Robert, C.; Abergel, C.; Renesto, P.; Ogata, H.; la Scola, B.; Suzan, M.; Claverie, J. The 1.2-megabase genome sequence of Mimivirus. Science 2004, 306, 1344-1350.
3. Philippe, N.; Legendre, M.; Doutre, G.; Couté, Y.; Poirot, O.; Lescot, M.; Arslan, D.; Seltzer, V.; Bertaux, L.; Bruley, C.; et al. Pandoraviruses: Amoeba viruses with genomes up to 2.5 Mb reaching that of parasitic eukaryotes. Science 2013, 341, 281-286.
4. Nasir, A.; Kim, K.; Caetano-Anolles, G. Giant viruses coexisted with the cellular ancestors and represent a distinct supergroup along with superkingdoms Archaea, Bacteria and Eukarya. BMC Evol. Biol. 2012, 12, doi:10.1186/1471-2148-12-156.
5. King, A.; Adams, M.; Carstens, E.; Lefkowitz, E. Virus Taxonomy: Classification and Nomenclature of Viruses. Ninth Report of the International Committee on Taxonomy of Viruses; Elsevier: San Diego, CA, USA, 2012.
6. Baltimore, D. Expression of animal virus genomes. Bacteriol. Rev. 1971, 35, 235-241.
7. Koonin, E.; Senkevich, T.; Dolja, V. The ancient Virus World and evolution of cells. Biol. Direct. 2006, 1, doi:10.1186/1745-6150-1-29.
8. Krupovic, M.; Bamford, D. Protein Conservation in Virus Evolution; eLS: Chicago, IL, USA, 2011.
9. Forterre, P. Defining life: The virus viewpoint. Orig. Life Evol. Biosph. 2010, 40, 151-160.
10. Rossmann, M.; Johnson, J. Icosahedral RNA virus structure. Annu. Rev. Biochem. 1989, 58, 533-573.
11. Krupovic, M.; Ravantti, J.; Bamford, D. Geminiviruses: A tale of a plasmid becoming a virus. BMC Evol. Biol. 2009, 9, doi:10.1186/1471-2148-9-112.
12. Raoult, D.; Forterre, P. Redefining viruses: Lessons from Mimivirus. Nat. Rev. Microbiol. 2008, 6, 315-319.
13. Bamford, D.; Grimes, J.; Stuart, D. What does structure tell us about virus evolution? Curr. Opin. Struct. Biol. 2005, 15, 655-663.
14. Krupovic, M.; Bamford, D. Virus evolution: How far does the double b-barrel viral lineage extend? Nat. Rev. Microbiol. 2008, 6, 941-948.
15. Koonin, E.; Dolya, V. Virus world as an evolutionary network of viruses and capsidless selfish elements. Microbiol. Mol. Biol. Rev. 2014, 78, 278-303.
16. Krupovic, M.; Koonin, E. Polintons: A hotbed of eukaryotic virus, transposon and plasmid evolution. Nat. Rev. Microbiol. 2015, 13, 105-115.
17. Ochman, H.; Lawrence, J.; Groisman, E.A. Lateral gene transfer and the nature of bacterial innovation. Nature 2000, 405, 299-304.
18. De la Cruz, F.; Davies, J. Horizontal gene transfer and the origin of species: Lessons from bacteria. Trends Microbiol. 2000, 8, 128-133.
19. Liu, H.; Fu, Y.; Li, B.; Yu, X.; Xie, J.; Cheng, J.; Ghabrial, S.; Li, G.; Yi, X.; Jiang, D. Widespread horizontal gene transfer from circular single-stranded DNA viruses to eukaryotic genomes. BMC Evol. Biol. 2011, 11, doi:10.1186/1471-2148-11-276.
20. Boto, L. Horizontal gene transfer in the acquisition of novel traits by metazoans. Proc. Biol. Sci. 2014, 281, doi:10.1098/rspb.2013.2450.
21. Filée, J.; Pouget, N.; Chandler, M. Phylogenetic evidence for extensive lateral acquisition of cellular genes by Nucleocytoplasmic large DNA viruses. BMC Evol. Biol. 2008, 8, doi:10.1186/1471-2148-8-320.
22. Monier, A.; Pagarete, A.; de Vargas, C.; Allen, M.; Read, B.; Claverie, J.M.; Ogata, H. Horizontal gene transfer of an entire metabolic pathway between a eukaryotic alga and its DNA virus. Genome Res. 2009, 19, 1441-1449.
23. Odom, M.; Hendrickson, R.; Lefkowitz, E. Poxvirus protein evolution: Family wide assessment of possible horizontal gene transfer events. Virus Res. 2009, 144, 233-249.
24. La Scola, B.; Desnues, C.; Pagnier, I.; Robert, C.; Barrassi, L.; Fournous, G.; Merchat, M.; Suzan-Monti, M.; Forterre, P.; Koonin, E.; et al. The virophage as a unique parasite of the giant mimivirus. Nature 2008, 455, 100-104.
25. The UniProt Consortium. Activities at the Universal Protein Resource (UniProt). Nucleic Acids Res. 2014, 42, D191-D198.
26. Altschul, S.; Gish, W.; Miller, W.; Myers, E.; Lipman, D. Basic local alignment search tool. J. Mol. Biol. 1990, 215, 403-410.
27. Punta, M.; Coggill, P.; Eberhardt, R.; Mistry, J.; Tate, J.; Boursnell, C.; Pang, N.; Forslund, K.; Ceric, G.; Clements, J.; et al. The Pfam protein families database. Nucleic Acids Res. 2012, 40, D290-D301.
28. Finn, R.; Clements, J.; Eddy, S. HMMER web server: Interactive sequence similarity searching. Nucleic Acids Res. 2011, 39, W29-W37.
29. Stamatakis, A. RAxML Version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014, 30, 1312-1313.
30. Huson, D.; Scornavacca, C. Dendroscope 3: An interactive tool for rooted phylogenetic trees and networks. Syst. Biol. 2012, 61, 1061-1067.
31. Leinonen, R.; Akhtar, R.; Birney, E.; Bower, L.; Cerdeno-Tárraga, A.; Cheng, Y.; Cleland, I.; Faruque, N.; Goodgame, N.; Gibson, R.; et al. The European nucleotide archive. Nucleic Acids Res. 2011, 39, D28-D31.
32. Peden, J. CodonW. Available online: http://codonw.sourceforge.net/ (accessed on 1 April 2013).
33. Bernstein, F.; Koetzle, T.; Williams, G.; Meyer, E., Jr.; Brice, M.; Rogers, J.; Kennard, O.; Shimanouchi, T.; Tasumi, M. The Protein Data Bank: A computer-based archival file for macromolecular structures. J. Mol. Biol. 1977, 112, 535-542.
34. Li,W.; Godzik, A. CD-HIT: A fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 2006, 22, 1658-1659.
35. Zhang, Y.; Skolnick, J. TM-align: A protein structure alignment algorithm based on TM-score. Nucleic Acids Res. 2005, 33, 2302-2309.
36. Zhang, Y.; Skolnick, J. Scoring function for automated assessment of protein structure template quality. Proteins 2004, 57, 702-710.
37. Xu, J.; Zhang, Y. How significant is a protein structure similarity with TM-score = 0.5? Bioinformatics 2010, 26, 889-895.
38. Holm, L.; Rosenström, P. Dali server: Conservation mapping in 3D. Nucleic Acids Res. 2010, 38, W545-W549.
39. Pettersen, E.; Goddard, T.; Huang, C.; Couch, G.; Greenblatt, D.; Meng, E.; Ferrin, T. UCSF Chimera- A visualization system for exploratory research and analysis. J. Comput. Chem. 2004, 25, 1605-1612.
40. Walker, J.; Saraste, M.; Runswick, M.; Gay, N. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP requiring enzymes and a common nucleotide binding fold. EMBO J. 1982, 1, 945-951.
41. Sharma, D.; Say, A.; Ledford, L.; Hughes, A.; Sehorn, H.; Dwyer, D.; Sehorn, M. Role of the conserved lysine within the Walker A motif of human DMC1. DNA Repair 2013, 12, 53-62.
42. Ferrer-Orta, C.; Arias, A.; Perez-Luque, R.; Escarmís, C.; Domingo, E.; Verdaguer, N. Structure of foot-and-mouth disease virus RNA-dependent RNA polymerase and its complex with a template-primer RNA. J. Biol. Chem. 2004, 279, 47212-47221.
43. Gibbs, M.;Weiller, G. Evidence that a plant virus switched hosts to infect a vertebrate and then recombined with a vertebrate-infecting virus. Proc. Natl. Acad. Sci. USA 1999, 96, 8022-8027.
44. Saraste, M.; Sibbald, P.;Wittinghofer, A. The P-loop-A common motif in ATP- and GTP-binding proteins. Trends Biochem. Sci. 1990, 15, 430-434.
45. Caruthers, J.; Johnson, E.; McKay, D. Crystal structure of yeast initiation factor 4A, a DEAD-box RNA helicase. Proc. Natl. Acad. Sci. USA 2000, 97, 13080-13085.
46. Vértessy, B.; Tóth, J. Keeping uracil out of DNA: Physiological role, structure and catalytic mechanism of dUTPases. Acc. Chem. Res. 2009, 42, 97-106.
47. Barabás, O.; Nemeth-Pongracz, V.; Magyar, A.; Hudecz, F.; Vértessy, B. Role of the C-terminal conserved sequence motif in the function of dUTPase from Mason-Pfizer monkey retrovirus. J. Pept. Sci. 2006, 12, 206.
48. Leonard, C.; Aravind, L.; Koonin, E. Novel families of putative protein kinases in bacteria and Archaea: evolution of the "eukaryotic" protein kinase superfamily. Genome Res. 1998, 8, 1038-1047.
49. Hickman, A.; Waninger, S.; Scocca, J.; Dyda, F. Molecular organization in site-specific recombination: The catalytic domain of bacteriophage HP1 integrase at 2.7 Å resolution. Cell 1997, 89, 227-237.
50. De Groot, R. Structure, function and evolution of the hemagglutininesterase proteins of corona- and toroviruses. Glycoconj. J. 2006, 23, 59-72.
51. Acha-Orbea, H.; MacDonald, H. Superantigens of mouse mammary tumor virus. Annu. Rev. Immunol. 1995, 13, 459-486.
52. Knappe, A.; Hiller, C.; Thurau, M.; Wittmann, S.; Hofmann, H.; Fleckenstein, B.; Fickenscher, H. The superantigen-homologous viral immediateearly gene ie14/vsag in herpesvirus saimiri-transformed human T cells. J. Virol. 1997, 71, 9124-9133.
53. Peremyslov, V.; Andreev, I.; Prokhnevsky, A.; Duncan, G.; Taliansky, M.; Dolja, V. Complex molecular architecture of beet yellow virus particles. Proc. Natl. Acad. Sci. USA 2004, 101, 5030-5035.
54. Lange, M.; Lehle, J. The genome of Cryptophlebia leucotreta granulovirus. Virology 2003, 317, 220-236.
55. Morse, M.; Marriott, A.; Nuttall, P. The glycoprotein of Thogoto virus (a tick-borne othomyxo-like virus) is related to the baculovirus glycoprotein GP64. Virology 1992, 186, 640-646.
56. Van Beurden, S.; Leroy, B.;Wattiez, R.; Haenen, O.; Boeren, S.; Vervoort, J.; Peeters, B.; Rottier, P.; Engelsma, M.; Vanderplasschen, A. Identification and localization of the structural proteins of anguillid herpesvirus 1 Vet. Res. 2011, 42, doi:10.1186/1297-9716-42-105.
57. Mushegian, A.; Elena, S. Evolution of plant virus movement proteins from the 30K superfamily and their homologs integrated in plant genomes. Virology 2015, 476, 304-315.
58. Rost, B. Twilight zone of protein sequence alignments. Protein Eng. 1999, 12, 85-94.
59. Irigoyen, N.; Garriga, D.; Navarro, A.; Verdaguer, N.; Rodriguez, J.; Caston, J. Autoproteolytic activity derived from the infectious bursal disease virus capsid protein. J. Biol. Chem. 2009, 284, 8064-8072.
60. Zhang, X.; Sun, S.; Xiang, Y.; Wong, J.; Klose, T.; Raoult, D.; Rossmann, M. Structure of Sputnik, a virophage, at 3.5 Å resolution. Proc. Natl. Acad. Sci. USA 2012, 109, 18431-18436.
61. Benson, S.; Bamford, J.; Bamford, D.; Burnett, R. The X-ray crystal structure of P3, the major coat protein of the lipid-containing bacteriophage PRD1,at 1.65 Å resolution. Acta Crystallogr. Sect. D 2002, D58, 39-59.
62. Khayat, R.; Tang, L.; Larson, E.; Lawrence, M.; Young, M.; Johnson, J. Structure of an Archaeal virus capsid protein reveals a common ancestry to eukaryotic and bacterial viruses. Proc. Natl. Acad. Sci. USA 2005, 102, 18944-18949.
63. Abrescia, N.; Grimes, J.; Kivela, H.; Assenberg, R.; Sutton, G.; Butcher, S.; Bamford, J.K.H.; Bamford, D.H.; Stuart, D.I. Insights into virus evolution and membrane biogenesis from the structure of the marine lipid-containing bacteriophage PM2. Mol. Cell 2008, 31, 749-761.
64. Nandhagopal, N.; Simpson, A.; Gurnon, J.; Yan, X.; Baker, T.; Graves, M.; van Etten, J.; Rossmann, M. The structure and evolution of the major capsid protein of a large, lipid-containing DNA virus. Proc. Natl. Acad. Sci. USA 2002, 99, 14758-14763.
65. Dessau, M.; Modis, Y. Crystal structure of glycoprotein C from Rift Valley fever virus. Proc. Natl. Acad. Sci. USA 2013, 110, 1696-1701.
66. Pérez-Vargas, J.; Krey, T.; Valansi, C.; Avinoam, O.; Haouz, A.; Jamin, M.; Raveh-Barak, H.; Podbilewicz, B.; Rey, F. Structural basis of eukaryotic cell-cell fusion. Cell 2014, 157, 407-419.
67. Gibrat, J.F.; Mariadassou, M.; Boudinot, P.; Delmas, B. Analyses of the radiation of birnaviruses from diverse host phyla and of their evolutionary affinities with other double-stranded RNA and positive strand RNA viruses using robust structure-based multiple sequence alignments and advanced phylogenetic methods. BMC Evol. Biol. 2013, 13, doi:10.1186/1471-2148-13-154.
68. Reich, S.; Guilligay, D.; Pflug, A.; Malet, H.; Berger, I.; Crépin, T.; Hart, D.; Lunardi, T.; Nanao, M.; Ruigrok, R.; et al. Structural insight into cap-snatching and RNA synthesis by influenza polymerase. Nature 2014, 516, 361-366.
69. Salgado, P.S.; Koivunen, M.R.L.; Makeyev, E.V.; Bamford, D.H.; Stuart, D.I.; Grimes, J.M. The structure of an RNAi polymerase links RNA silencing and transcription. PLoS Biol. 2006, 4, e434.
70. He, X.; Byrd, A.; Yun, M.; Pemble, C.; Harrison, D.; Yeruva, L.; Dahl, C.; Kreuzer, K.; Raney, K.; White, S. The T4 phage SF1B helicase Dda is structurally optimized to perform DNA strand separation. Structure 2012, 20, 1189-1200.
71. Gorbalenya, A.; Koonin, E. Helicases: Amino acid sequence comparisons and structure-function relationships. Curr. Opin. Struct. Biol. 1993, 3, 419-429.
72. Zeng, Q.; Langereis, M.; van Viet, A.; Huizinga, E.; de Groot, R. Structure of coronavirus hemagglutinin-esterase offers insight into Corona- and Influenza virus evolution. Proc. Natl. Acad. Sci. USA 2008, 105, 9065-9069.
73. Wang, Q.; Cheng, F.; Lu, M.; Tian, X.; Ma, J. Crystal structure of unliganded influenza B virus hemagglutinin. J. Virol. 2008, 82, 3011-3020.
74. Koonin, E.; Dolja, V. Evolution and taxonomy of positive-strand RNA viruses: Implications of comparative analysis of amino acid sequences. Crit. Rev. Biochem. Mol. Biol. 1993, 28, 375-430.
75. Abrescia, N.G.; Bamford, D.H.; Grimes, J.M.; Stuart, D.I. Structure unifies the viral universe. Ann. Rev. Biochem. 2012, 81, 795-822.
76. Sillitoe, I.; Lewis, T.E.; Cuff, A.; Das, S.; Ashford, P.; Dawson, N.L.; Furnham, N.; Laskowski, R.A.; Lee, D.; Lees, J.G.; et al. CATH: Comprehensive structural and functional annotations for genome sequences. Nucleic Acids Res. 2015, 43, D376-D381.
77. Andreeva, A.; Howorth, D.; Chandonia, J.M.; Brenner, S.E.; Hubbard, T.J.P.; Chothia, C.; Murzin, A.G. Data growth and its impact on the SCOP database: New developments. Nucleic Acids Res. 2007, 36, D419-D425.
78. Moreira, D. Multiple independent horizontal transfers of informational genes from bacteria to plasmids and phages: implications for the origin of bacterial replication machinery. Mol. Microbiol. 2000, 35, 1-5.
79. Koonin, E.; Makarova, K.; Aravind, L. Horizontal gene transfer in prokaryotes: quantification and classification. Ann. Rev. Microbiol. 2001, 55, 709-742.
80. Nicolas, P.; Bize, L.; Muri, F.; Hoebeke, M.; Rodolphe, F.; Ehrlich, S.D.; Prum, B.; Bessiãĺres, P. Mining Bacillus subtilis chromosome heterogeneities using hidden Markov models. Nucleic Acids Res. 2002, 30, 1418-1426.
81. Tsirigos, A.; Rigoutsos, I. A sensitive, support-vector-machine method for the detection of horizontal gene transfers in viral, Archaeal and bacterial genomes. Nucleic Acids Res. 2005, 33, 3699-3707.
82. Metzler, S.; Kalinina, O.V. Detection of atypical genes in virus families using a one-class SVM. BMC Genomics 2014, 15, doi:10.1186/1471-2164-15-913.
83. Koonin, E.V.; Yutin, N. Origin and evolution of eukaryotic large nucleo-cytoplasmic DNA viruses. Intervirology 2010, 53, 284-292.