1932

Abstract

Although viruses comprise the most abundant genetic material in the biosphere, to date only several thousand virus species have been formally defined. Such a limited perspective on virus diversity has in part arisen because viruses were traditionally considered only as etiologic agents of overt disease in humans or economically important species and were often difficult to identify using cell culture. This view has dramatically changed with the rise of metagenomics, which is transforming virus discovery and revealing a remarkable diversity of viruses sampled from diverse cellular organisms. These newly discovered viruses help fill major gaps in the evolutionary history of viruses, revealing a near continuum of diversity among genera, families, and even orders of RNA viruses. Herein, we review some of the recent advances in our understanding of the RNA virosphere that have stemmed from metagenomics, note future directions, and highlight some of the remaining challenges to this rapidly developing field.

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2019-09-29
2024-04-19
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Literature Cited

  1. 1. 
    Hendrix RW, Smith MCM, Burns RN, Ford ME, Hatfull GF 1999. Evolutionary relationships among diverse bacteriophages and prophages: All the world's a phage. PNAS 96:2192–97
    [Google Scholar]
  2. 2. 
    Angly FE, Felts B, Breitbart M, Salamon P, Edwards RA et al. 2006. The marine viromes of four oceanic regions. PLOS Biol 4:e368
    [Google Scholar]
  3. 3. 
    Desnues C, Rodriguez-Brito B, Rayhawk S, Kelley S, Tran T et al. 2008. Biodiversity and biogeography of phages in modern stromatolites and thrombolites. Nature 452:340–43
    [Google Scholar]
  4. 4. 
    Edwards RA, Rohwer F. 2005. Viral metagenomics. Nat. Rev. Microbiol. 3:504–10
    [Google Scholar]
  5. 5. 
    Paez-Espino D, Eloe-Fadrosh EA, Pavlopoulos GA, Thomas AD, Huntemann M et al. 2016. Uncovering Earth's virome. Nature 536:425–430
    [Google Scholar]
  6. 6. 
    Koonin EV, Dolja VV. 2018. Metaviromics: a tectonic shift in understanding virus evolution. Virus Res 246:A1–3
    [Google Scholar]
  7. 7. 
    Zhang YZ, Shi M, Holmes EC 2018. Using metagenomics to characterize an expanding virosphere. Cell 172:1168–72
    [Google Scholar]
  8. 8. 
    Zhang YZ, Wu WC, Shi M, Holmes EC 2018. The diversity, evolution and origins of vertebrate RNA viruses. Curr. Opin. Virol. 31:9–16
    [Google Scholar]
  9. 9. 
    Geoghegan JL, Holmes EC. 2017. Predicting virus emergence amidst evolutionary noise. Open Biol 7:170189
    [Google Scholar]
  10. 10. 
    Lecoq H. 2001. Discovery of the first virus, the tobacco mosaic virus: 1892 or 1898. C. R. Acad. Sci. III 324:929–33
    [Google Scholar]
  11. 11. 
    Culley AI, Lang AS, Suttle CA 2003. High diversity of unknown picorna-like viruses in the sea. Nature 424:1054–57
    [Google Scholar]
  12. 12. 
    Culley AI, Lang AS, Suttle CA 2006. Metagenomic analysis of coastal RNA virus communities. Science 312:1795–98
    [Google Scholar]
  13. 13. 
    Suttle CA. 2005. Viruses in the sea. Nature 437:356–61
    [Google Scholar]
  14. 14. 
    Dolja VV, Koonin EV. 2018. Metagenomics reshapes the concepts of RNA virus evolution by revealing extensive horizontal virus transfer. Virus Res 244:36–52
    [Google Scholar]
  15. 15. 
    Li CX, Shi M, Tian JH, Lin XD, Kang YJ et al. 2015. Unprecedented RNA virus diversity in arthropods reveals the ancestry of negative-sense RNA viruses. eLife 4:e05378
    [Google Scholar]
  16. 16. 
    Shi M, Lin XD, Tian JH, Chen LJ, Chen X et al. 2016. Redefining the invertebrate virosphere. Nature 540:539–43
    [Google Scholar]
  17. 17. 
    Shi M, Lin XD, Chen X, Tian JH, Chen LJ et al. 2018. The evolutionary history of vertebrate RNA viruses. Nature 556:197–202
    [Google Scholar]
  18. 18. 
    Babayan SA, Orton RJ, Streicker DG 2018. Predicting reservoir hosts and arthropod vectors from evolutionary signatures in RNA virus genomes. Science 362:577–80
    [Google Scholar]
  19. 19. 
    Shi M, Zhang YZ, Holmes EC 2018. Meta-transcriptomics and the evolutionary biology of RNA viruses. Virus Res 243:83–90
    [Google Scholar]
  20. 20. 
    Qin XC, Shi M, Tian JH, Lin XD, Gao DY et al. 2014. A tick-borne segmented RNA virus contains genome segments derived from unsegmented viral ancestors. PNAS 111:6744–49
    [Google Scholar]
  21. 21. 
    Delwart E. 2012. Animal virus discovery: improving animal health, understanding zoonoses, and opportunities for vaccine development. Curr. Opin. Virol. 2:344–52
    [Google Scholar]
  22. 22. 
    Eden J-S, Chisholm R-H, Bull RA, White PA, Holmes EC, Tanaka MM 2017. Persistent infections in immunocompromised hosts are rarely sources of new pathogen variants. Virus Evol 3:vex018
    [Google Scholar]
  23. 23. 
    Kapoor A, Victoria J, Simmonds P, Slikas E, Chieochansin T et al. 2008. A highly prevalent and genetically diversified Picornaviridae genus in South Asian children. PNAS 105:20482–87
    [Google Scholar]
  24. 24. 
    Li L, Victoria J, Kapoor A, Naeem A, Shaukat S et al. 2009. Genomic characterization of novel human parechovirus type. Emerg. Infect. Dis. 15:288–91
    [Google Scholar]
  25. 25. 
    Victoria JG, Kapoor A, Dupuis K, Schnurr DP, Delwart EL 2008. Rapid identification of known and new RNA viruses from animal tissues. PLOS Pathog 4:e1000163
    [Google Scholar]
  26. 26. 
    Wilson MR, Naccache SN, Samayoa E, Biagtan M, Bashir H et al. 2014. Actionable diagnosis of neuroleptospirosis by next-generation sequencing. N. Engl. J. Med. 370:2408–17
    [Google Scholar]
  27. 27. 
    Lipkin WI, Travis GH, Carbone KM, Wilson MC 1990. Isolation and characterization of Borna disease agent cDNA clones. PNAS 87:4184–88
    [Google Scholar]
  28. 28. 
    Mokili JL, Rohwer F, Dutilh BE 2012. Metagenomics and future perspectives in virus discovery. Curr. Opin. Virol. 2:63–77
    [Google Scholar]
  29. 29. 
    Reyes GR, Purdy MA, Kim JP, Luk KC, Young LM et al. 1990. Isolation of a cDNA from the virus responsible for enterically transmitted non-A, non-B hepatitis. Science 247:1335–39
    [Google Scholar]
  30. 30. 
    CDC (Cent. Dis. Control Prev.) 1999. Outbreak of Hendra-like virus—Malaysia and Singapore, 1998–1999. MMWR Morb. Mortal. Wkly. Rep. 48:265–69
    [Google Scholar]
  31. 31. 
    Chua KB, Bellini WJ, Rota PA, Harcourt BH, Tamin A et al. 2000. Nipah virus: a recently emergent deadly paramyxovirus. Science 288:1432–35
    [Google Scholar]
  32. 32. 
    Drosten C, Günther S, Preiser W, van der Werf S, Brodt HR et al. 2003. Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N. Engl. J. Med. 348:1967–76
    [Google Scholar]
  33. 33. 
    Zhang Y-Z, Zhou DJ, Xiong Y, Chen XP, He YW et al. 2011. Hemorrhagic fever caused by a novel tick-borne Bunyavirus in Huaiyangshan, China. Zhonghua Liu Xing Bing Xue Za Zhi 32:209–20
    [Google Scholar]
  34. 34. 
    Woo PC, Lau SK, Lam CS, Lau CC, Tsang AK et al. 2012. Discovery of seven novel mammalian and avian coronaviruses in the genus Deltacoronavirus supports bat coronaviruses as the gene source of Alphacoronavirus and Betacoronavirus and avian coronaviruses as the gene source of Gammacoronavirus and Deltacoronavirus. J. Virol. 86:3995–4008
    [Google Scholar]
  35. 35. 
    Guo WP, Lin XD, Wang W, Tian JH, Cong ML et al. 2013. Phylogeny and origins of hantaviruses harbored by bats, insectivores, and rodents. PLOS Pathog 9:e1003159
    [Google Scholar]
  36. 36. 
    Drexler JF, Corman VM, Müller MA, Lukashev AN, Gmyl A et al. 2013. Evidence for novel hepaciviruses in rodents. PLOS Pathog 9:e1003438
    [Google Scholar]
  37. 37. 
    Tong S, Zhu X, Li Y, Shi M, Bourgeois M et al. 2013. New World bats harbor diverse influenza A viruses. PLOS Pathog 9:e1003657
    [Google Scholar]
  38. 38. 
    Drexler JF, Corman VM, Müller MA, Maganga GD, Vallo P et al. 2012. Bats host major mammalian paramyxoviruses. Nat. Commun. 3:796
    [Google Scholar]
  39. 39. 
    Firth C, Lipkin WI. 2013. The genomics of emerging pathogens. Annu. Rev. Genom. Hum. Genet. 14:281–300
    [Google Scholar]
  40. 40. 
    Greningera AL. 2018. A decade of RNA virus metagenomics is (not) enough. Virus Res 244:218–29
    [Google Scholar]
  41. 41. 
    Conceicao-Neto N, Zeller M, Lefrere H, De Bruyn P, Beller L et al. 2015. Modular approach to customise sample preparation procedures for viral metagenomics: a reproducible protocol for virome analysis. Sci. Rep. 5:16532
    [Google Scholar]
  42. 42. 
    Djikeng A, Halpin R, Kuzmickas R, DePasse J, Feldblyum J et al. 2008. Viral genome sequencing by random priming methods. BMC Genom 9:5
    [Google Scholar]
  43. 43. 
    Lim YW, Schmieder R, Haynes M, Willner D, Furlan M et al. 2013. Metagenomics and metatranscriptomics: windows on CF-associated viral and microbial communities. J. Cyst. Fibros. 12:154–64
    [Google Scholar]
  44. 44. 
    Koonin EV. 1991. The phylogeny of RNA-dependent RNA polymerases of positive-strand RNA viruses. J. Gen. Virol. 72:2197–206
    [Google Scholar]
  45. 45. 
    Geoghegan JL, Di Giallonardo F, Cousins K, Shi M, Williamson JE, Holmes EC 2018. Hidden diversity and evolution of viruses in market fish. Virus Evol 4:vey031
    [Google Scholar]
  46. 46. 
    Wilson MR, O'Donovan BD, Gelfand JM, Sample HA, Chow FC et al. 2018. Chronic meningitis investigated via metagenomic next-generation sequencing. JAMA Neurol 75:947–55
    [Google Scholar]
  47. 47. 
    Naccache SN, Greninger AL, Lee D, Coffey LL, Phan T et al. 2013. The perils of pathogen discovery: origin of a novel parvovirus-like hybrid genome traced to nucleic acid extraction spin columns. J. Virol. 87:11966–77
    [Google Scholar]
  48. 48. 
    Bolduc B, Shaughnessy DP, Wolf YI, Koonin EV, Roberto FF, Young M 2012. Identification of novel positive-strand RNA viruses by metagenomic analysis of archaea-dominated Yellowstone hot springs. J. Virol. 86:5562–73
    [Google Scholar]
  49. 49. 
    Bamford DH, Grimes JM, Stuart DI 2005. What does structure tell us about viral evolution. Curr. Opin. Struct. Biol. 15:655–63
    [Google Scholar]
  50. 50. 
    Fédry J, Liu Y, Péhau-Arnaudet G, Pei J, Li W et al. 2017. The ancient gamete fusogen HAP2 is a eukaryotic class II fusion protein. Cell 168:904–15
    [Google Scholar]
  51. 51. 
    Colmant AMG, Hobson-Peters J, Bielefeldt-Ohmann H, van den Hurk AF, Hall-Mendelin S et al. 2017. A new clade of insect-specific flaviviruses from Australian Anopheles mosquitoes displays species-specific host restriction. mSphere 2:e00262–17
    [Google Scholar]
  52. 52. 
    Junglen S, Drosten C. 2013. Virus discovery and recent insights into virus diversity in arthropods. Curr. Opin. Microbiol. 16:507–13
    [Google Scholar]
  53. 53. 
    Marklewitz M, Zirkel F, Kurth A, Drosten C, Junglen S 2015. Evolutionary and phenotypic analysis of live virus isolates suggests arthropod origin of a pathogenic RNA virus family. PNAS 112:7536–41
    [Google Scholar]
  54. 54. 
    Remnant EJ, Shi M, Buchmann G, Blacquière T, Holmes EC et al. 2017. A diverse range of novel RNA viruses in geographically distinct honey bee populations. J. Virol. 91:e00158-17
    [Google Scholar]
  55. 55. 
    Shi M, Neville P, Nicholson J, Eden JS, Imrie A, Holmes EC 2017. High-resolution metatranscriptomics reveals the ecological dynamics of mosquito-associated RNA viruses in Western Australia. J. Virol. 91:e00680-17
    [Google Scholar]
  56. 56. 
    Tokarz R, Sameroff S, Tagliafierro T, Jain K, Williams SH et al. 2018. Identification of novel viruses in Amblyomma americanum, Dermacentor variabilis, and Ixodes scapularis ticks. mSphere 3:e00614-17
    [Google Scholar]
  57. 57. 
    Tokarz R, Williams SH, Sameroff S, Sanchez Leon M, Jain K, Lipkin WI 2014. Virome analysis of Amblyomma americanum, Dermacentor variabilis, and Ixodes scapularis ticks reveals novel highly divergent vertebrate and invertebrate viruses. J. Virol. 88:11480–92
    [Google Scholar]
  58. 58. 
    Webster CL, Waldron FM, Robertson S, Crowson D, Ferrari G et al. 2015. The discovery, distribution, and evolution of viruses associated with Drosophila melanogaster. PLOS Biol 13:e1002210
    [Google Scholar]
  59. 59. 
    Colmant AMG, Hall-Mendelin S, Ritchie SA, Bielefeldt-Ohmann H, Harrison JJ et al. 2018. The recently identified flavivirus Bamaga virus is transmitted horizontally by Culex mosquitoes and interferes with West Nile virus replication in vitro and transmission in vivo. PLOS Negl. Trop. Dis 12:e0006886
    [Google Scholar]
  60. 60. 
    Hall-Mendelin S, McLean BJ, Bielefeldt-Ohmann H, Hobson-Peters J, Hall RA et al. 2016. The insect-specific Palm Creek virus modulates West Nile virus infection in and transmission by Australian mosquitoes. Parasit. Vectors 9:414
    [Google Scholar]
  61. 61. 
    Holmes EC. 2011. The evolution of endogenous viral elements. Cell Host Microbe 10:368–77
    [Google Scholar]
  62. 62. 
    Whitfield ZJ, Dolan PT, Kunitomi M, Tassetto M, Seetin MG et al. 2017. The diversity, structure, and function of heritable adaptive immunity sequences in the Aedes aegypti genome. Curr. Biol. 27:3511–19
    [Google Scholar]
  63. 63. 
    Bennett AJ, Bushmaker T, Cameron K, Ondzie A, Niama FR et al. 2018. Diverse RNA viruses of arthropod origin in the blood of fruit bats suggest a link between bat and arthropod viromes. Virology 528:64–72
    [Google Scholar]
  64. 64. 
    Roossinck MJ. 2015. Plants, viruses and the environment: ecology and mutualism. Virology 479:80271–77
    [Google Scholar]
  65. 65. 
    Olival KJ, Hosseini PR, Zambrana-Torrelio C, Ross N, Bogich TL, Daszak P 2017. Host and viral traits predict zoonotic spillover from mammals. Nature 546:646–50
    [Google Scholar]
  66. 66. 
    Dill JA, Camus AC, Leary JH, Di Giallonardo F, Holmes EC, Ng TFF 2016. Distinct viral lineages of hepadnavirus from fish and amphibians reveal the complex evolutionary history of hepadnaviruses. J. Virol. 90:7920–33
    [Google Scholar]
  67. 67. 
    Lauber C, Seitz S, Mattei S, Suh A, Beck J et al. 2017. Deciphering the origin and evolution of hepatitis B viruses by means of a family of non-enveloped fish viruses. Cell Host Microbe 22:387–99
    [Google Scholar]
  68. 68. 
    Suh A, Weber CC, Kehlmaier C, Braun EL, Green RE et al. 2014. Early Mesozoic coexistence of amniotes and Hepadnaviridae. PLOS Genet 10:e1004559
    [Google Scholar]
  69. 69. 
    Allison AB, Ballard JR, Tesh RB, Brown JD, Ruder MG et al. 2015. Cyclic avian mass mortality in the northeastern United States is associated with a novel orthomyxovirus. J. Virol. 89:1389–403
    [Google Scholar]
  70. 70. 
    Geoghegan JL, Duchêne S, Holmes EC 2017. Comparative analysis estimates the relative frequencies of co-divergence and cross-species transmission within viral families. PLOS Pathog 13:e1006215
    [Google Scholar]
  71. 71. 
    Bacharach E, Mishra N, Briese T, Zody MC, Kembou Tsofack JE et al. 2016. Characterization of a novel orthomyxo-like virus causing mass die-offs of tilapia. mBio 7:e00431-16
    [Google Scholar]
  72. 72. 
    Taylor J, Pelchat M. 2010. Origin of hepatitis Delta virus. Future Microbiol 5:393–402
    [Google Scholar]
  73. 73. 
    Wille M, Netter HJ, Littlejohn M, Yuen L, Shi M et al. 2018. A divergent hepatitis D-like virus in birds. Viruses 10:720
    [Google Scholar]
  74. 74. 
    Woolhouse MEJ, Brierley L. 2018. Epidemiological characteristics of human-infective RNA viruses. Sci. Data 5:180017
    [Google Scholar]
  75. 75. 
    Tan SK, Relman DA, Pinsky BA 2017. The human virome: implications for clinical practice in transplantation medicine. J. Clin. Microbiol. 55:2884–93
    [Google Scholar]
  76. 76. 
    Holmes EC, Rambaut A, Andersen KG 2018. Pandemics: spend on surveillance, not prediction. Nature 558:180–82
    [Google Scholar]
  77. 77. 
    Wilson MR, Suan D, Duggins A, Schubert RD, Khan LM et al. 2017. A novel cause of chronic viral meningoencephalitis: Cache Valley virus. Ann. Neurol. 82:105–14
    [Google Scholar]
  78. 78. 
    Shi M, Lin XD, Vasilakis N, Tian JH, Li CX et al. 2016. Divergent viruses discovered in arthropods and vertebrates revise the evolutionary history of the Flaviviridae and related viruses. J. Virol. 90:659–69
    [Google Scholar]
  79. 79. 
    Ladner JT, Wiley MR, Beitzel B, Auguste AJ, Dupuis AP II et al. 2016. A multicomponent animal virus isolated from mosquitoes. Cell Host Microbe 20:357–67
    [Google Scholar]
  80. 80. 
    Gorbalenya AE, Enjuanes L, Ziebuhr J, Snijder EJ 2006. Nidovirales: evolving the largest RNA virus genome. Virus Res 117:17–37
    [Google Scholar]
  81. 81. 
    Saberi A, Gulyaeva AA, Brubacher JL, Newmark PA, Gorbalenya AE 2018. A planarian nidovirus expands the limits of RNA genome size. PLOS Pathog 14:e1007314
    [Google Scholar]
  82. 82. 
    Simon-Loriere E, Holmes EC. 2013. Gene duplication is infrequent in the recent evolutionary history of RNA viruses. Mol. Biol. Evol. 30:1263–69
    [Google Scholar]
  83. 83. 
    Meyers G, Rumenapf T, Thiel HJ 1989. Ubiquitin in a togavirus. Nature 341:491
    [Google Scholar]
  84. 84. 
    Holmes EC. 2009. The Evolution and Emergence of RNA Viruses New York: Oxford Univ. Press
  85. 85. 
    Ochman H, Lawrence JG, Groisman EA 2000. Lateral gene transfer and the nature of bacterial innovation. Nature 405:299–304
    [Google Scholar]
  86. 86. 
    Simmonds P, Adams MJ, Benkő M, Breitbart M, Brister JR et al. 2017. Consensus statement: virus taxonomy in the age of metagenomics. Nat. Rev. Microbiol. 15:161–68
    [Google Scholar]
  87. 87. 
    Bobay LM, Ochman H. 2018. Biological species in the viral world. PNAS 115:6040–45
    [Google Scholar]
  88. 88. 
    Bexfield N, Kellam P. 2011. Metagenomics and the molecular identification of novel viruses. Vet. J. 190:191–98
    [Google Scholar]
  89. 89. 
    Delwart EL. 2007. Viral metagenomics. Rev. Med. Virol. 17:115–31
    [Google Scholar]
  90. 90. 
    Rosario K, Breitbart M. 2011. Exploring the viral world through metagenomics. Curr. Opin. Virol. 1:289–97
    [Google Scholar]
  91. 91. 
    Tang P, Chiu C. 2010. Metagenomics for the discovery of novel human viruses. Future Microbiol 5:177–89
    [Google Scholar]
  92. 92. 
    Zanotto PM, Gibbs MJ, Gould EA, Holmes EC 1996. A reevaluation of the higher taxonomy of viruses based on RNA polymerases. J. Virol. 70:6083–96
    [Google Scholar]
  93. 93. 
    Wolf YI, Kazlauskas D, Iranzo J, Lucía-Sanz A, Kuhn JH et al. 2018. Origins and evolution of the global RNA virome. mBio 9:e02329-18
    [Google Scholar]
  94. 94. 
    Fredricks DN, Relman DA. 1996. Sequence-based identification of microbial pathogens: a reconsideration of Koch's postulates. Clin. Microbiol. Rev. 9:18–33
    [Google Scholar]
  95. 95. 
    Wille M, Eden J-S, Shi M, Klaassen M, Hurt AC, Holmes EC 2018. Virus–virus interactions and host ecology are associated with RNA virome structure in wild birds. Mol. Ecol. 27:5263–78
    [Google Scholar]
  96. 96. 
    Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu G, Pyke AT et al. 2009. A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell 139:1268–78
    [Google Scholar]
  97. 97. 
    Tan CH, Wong PJ, Li MI, Yang H, Ng LC, O'Neill SL 2017. wMel limits zika and chikungunya virus infection in a Singapore Wolbachia-introgressed Ae. aegypti strain, wMel-Sg. PLOS Negl. Trop. Dis. 11:e0005496
    [Google Scholar]
  98. 98. 
    Shi M, White VL, Schlub T, Eden J-S, Hoffmann AA, Holmes EC 2018. No detectable effect of Wolbachia wMel on the prevalence and abundance of the RNA virome of Drosophila melanogaster. Proc. R. Soc. B 285:20181165
    [Google Scholar]
  99. 99. 
    Nambulli S, Sharp CR, Acciardo AS, Drexler JF, Duprex WP 2016. Mapping the evolutionary trajectories of morbilliviruses: what, where and whither. Curr. Opin. Virol. 16:95–105
    [Google Scholar]
  100. 100. 
    Wang LF, Walker PJ, Poon LL 2011. Mass extinctions, biodiversity and mitochondrial function: Are bats ‘special’ as reservoirs for emerging viruses. Curr. Opin. Virol. 1:649–57
    [Google Scholar]
  101. 101. 
    Drummond AJ, Pybus OG, Rambaut A, Forsberg R, Rodrigo AG 2003. Measurably evolving populations. Trends Ecol. Evol. 18:481–88
    [Google Scholar]
  102. 102. 
    Biek R, Pybus OG, Lloyd-Smith JO, Didelot X 2015. Measurably evolving pathogens in the genomic era. Trends Ecol. Evol. 30:306–13
    [Google Scholar]
  103. 103. 
    Duchêne S, Holmes EC, Ho SYW 2014. Analyses of evolutionary dynamics in viruses are hindered by a time-dependent bias in rate estimates. Proc. R. Soc. B 281:20140732
    [Google Scholar]
  104. 104. 
    Katzourakis A, Gifford RJ. 2010. Endogenous viral elements in animal genomes. PLOS Genet 6:e1001191
    [Google Scholar]
  105. 105. 
    Aiewsakun P, Katzourakis A. 2015. Endogenous viruses: connecting recent and ancient viral evolution. Virology 479:48026–37
    [Google Scholar]
  106. 106. 
    Roossinck MJ, Martin DP, Roumagnac P 2015. Plant virus metagenomics: advances in virus discovery. Phytopathology 105:716–27
    [Google Scholar]
  107. 107. 
    Mushegian A, Shipunov A, Elena SF 2016. Changes in the composition of the RNA virome mark evolutionary transitions in green plants. BMC Biol 14:68
    [Google Scholar]
  108. 108. 
    Miranda JA, Culley AI, Schvarcz CR, Steward GF 2016. RNA viruses as major contributors to Antarctic virioplankton. Environ. Microbiol. 18:3714–27
    [Google Scholar]
  109. 109. 
    Krupovic M, Koonin EV. 2017. Multiple origins of viral capsid proteins from cellular ancestors. PNAS 114:E2401–10
    [Google Scholar]
  110. 110. 
    Gostic KM, Ambrose M, Worobey M, Lloyd-Smith JO 2016. Potent protection against H5N1 and H7N9 influenza via childhood hemagglutinin imprinting. Science 354:722–26
    [Google Scholar]
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