1932

Abstract

Virology has largely focused on viruses that are pathogenic to humans or to the other species that we care most about. There is no doubt that this has been a worthwhile investment. But many transformative advances have been made through the in-depth study of relatively obscure viruses that do not appear on lists of prioritized pathogens. In this review, I highlight the benefits that can accrue from the study of viruses and hosts off the beaten track. I take stock of viral sequence diversity across host taxa as an estimate of the bias that exists in our understanding of host-virus interactions. I describe the gains that have been made through the metagenomic discovery of thousands of new viruses in previously unsampled hosts as well as the limitations of metagenomic surveys. I conclude by suggesting that the study of viruses that naturally infect existing and emerging model organisms represents an opportunity to push virology forward in useful and hard to predict ways.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-100220-112915
2022-09-29
2024-06-15
Loading full text...

Full text loading...

/deliver/fulltext/virology/9/1/annurev-virology-100220-112915.html?itemId=/content/journals/10.1146/annurev-virology-100220-112915&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Imperiale MJ, Casadevall A. 2015. The importance of virology at a time of great need and great jeopardy. mBio 6:2e00236–15
    [Crossref] [Google Scholar]
  2. 2.
    Goodin MM, Hatfull GF, Malik HS. 2016. A diversified portfolio. Annu. Rev. Virol. 3:vi–viii
    [Crossref] [Google Scholar]
  3. 3.
    Thompson JR. 2021. Fundamental virology: same objectives, changing tools. Front. Virol. 1:6
    [Crossref] [Google Scholar]
  4. 4.
    Stenglein MD, Harris RS. 2006. APOBEC3B and APOBEC3F inhibit L1 retrotransposition by a DNA deamination-independent mechanism. J. Biol. Chem. 281:2516837–41
    [Crossref] [Google Scholar]
  5. 5.
    Chen H, Lilley CE, Yu Q, Lee DV, Chou J et al. 2006. APOBEC3A is a potent inhibitor of adeno-associated virus and retrotransposons. Curr. Biol. 16:5480–85
    [Crossref] [Google Scholar]
  6. 6.
    Bogerd HP, Wiegand HL, Hulme AE, Garcia-Perez JL, O'Shea KS et al. 2006. Cellular inhibitors of long interspersed element 1 and Alu retrotransposition. PNAS 103:238780–85
    [Crossref] [Google Scholar]
  7. 7.
    Muckenfuss H, Hamdorf M, Held U, Perković M, Löwer J et al. 2006. APOBEC3 proteins inhibit human LINE-1 retrotransposition. J. Biol. Chem. 281:3122161–72
    [Crossref] [Google Scholar]
  8. 8.
    Weiss RA, Vogt PK. 2011. 100 years of Rous sarcoma virus. J. Exp. Med. 208:122351–55
    [Crossref] [Google Scholar]
  9. 9.
    Rous P. 1911. A sarcoma of the fowl transmissible by an agent separable from the tumor cells. J. Exp. Med. 13:4397–411
    [Crossref] [Google Scholar]
  10. 10.
    Baltimore D. 1970. Viral RNA-dependent DNA polymerase: RNA-dependent DNA polymerase in virions of RNA tumour viruses. Nature 226:52521209–11
    [Crossref] [Google Scholar]
  11. 11.
    Temin HM, Mizutani S. 1970. Viral RNA-dependent DNA polymerase: RNA-dependent DNA polymerase in virions of Rous sarcoma virus. Nature 226:52521211–13
    [Crossref] [Google Scholar]
  12. 12.
    Stehelin D, Varmus HE, Bishop JM, Vogt PK. 1976. DNA related to the transforming gene(s) of avian sarcoma viruses is present in normal avian DNA. Nature 260:5547170–73
    [Crossref] [Google Scholar]
  13. 13.
    Hershey AD, Chase M. 1952. Independent functions of viral protein and nucleic acid in growth of bacteriophage. J. Gen. Physiol. 36:139–56
    [Crossref] [Google Scholar]
  14. 14.
    Crick FH, Barnett L, Brenner S, Watts-Tobin RJ. 1961. General nature of the genetic code for proteins. Nature 192:1227–32
    [Crossref] [Google Scholar]
  15. 15.
    Ofir G, Sorek R. 2018. Contemporary phage biology: from classic models to new insights. Cell 172:61260–70
    [Crossref] [Google Scholar]
  16. 16.
    Furuichi Y, Morgan M, Muthukrishnan S, Shatkin AJ. 1975. Reovirus messenger RNA contains a methylated, blocked 5′-terminal structure: m7G(5′)ppp(5′)GmpCp-. PNAS 72:1362–66
    [Crossref] [Google Scholar]
  17. 17.
    Nevins JR, Wilson MC. 1981. Regulation of adenovirus-2 gene expression at the level of transcriptional termination and RNA processing. Nature 290:5802113–18
    [Crossref] [Google Scholar]
  18. 18.
    Fitzgerald M, Shenk T. 1981. The sequence 5′-AAUAAA-3′ forms parts of the recognition site for polyadenylation of late SV40 mRNAs. Cell 24:1251–60
    [Crossref] [Google Scholar]
  19. 19.
    Berget SM, Moore C, Sharp PA. 1977. Spliced segments at the 5′ terminus of adenovirus 2 late mRNA. PNAS 74:83171–75
    [Crossref] [Google Scholar]
  20. 20.
    Pardi N, Hogan MJ, Porter FW, Weissman D. 2018. mRNA vaccines—a new era in vaccinology. Nat. Rev. Drug Discov. 17:4261–79
    [Crossref] [Google Scholar]
  21. 21.
    Martin SA, Paoletti E, Moss B. 1975. Purification of mRNA guanylyltransferase and mRNA (guanine-7-)methyltransferase from vaccinia virions. J. Biol. Chem. 250:249322–29
    [Crossref] [Google Scholar]
  22. 22.
    Davanloo P, Rosenberg AH, Dunn JJ, Studier FW. 1984. Cloning and expression of the gene for bacteriophage T7 RNA polymerase. PNAS 81:72035–39
    [Crossref] [Google Scholar]
  23. 23.
    Melton DA, Krieg PA, Rebagliati MR, Maniatis T, Zinn K, Green MR. 1984. Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res 12:187035–56
    [Crossref] [Google Scholar]
  24. 24.
    Kost TA, Condreay JP, Jarvis DL. 2005. Baculovirus as versatile vectors for protein expression in insect and mammalian cells. Nat. Biotechnol. 23:5567–75
    [Crossref] [Google Scholar]
  25. 25.
    Muyldermans S. 2013. Nanobodies: natural single-domain antibodies. Annu. Rev. Biochem. 82:775–97
    [Crossref] [Google Scholar]
  26. 26.
    Muyldermans S. 2021. Applications of nanobodies. Annu. Rev. Anim. Biosci. 9:401–21
    [Crossref] [Google Scholar]
  27. 27.
    Doudna JA, Charpentier E. 2014. The new frontier of genome engineering with CRISPR-Cas9. Science 346:62131258096
    [Crossref] [Google Scholar]
  28. 28.
    Wright AV, Nuñez JK, Doudna JA. 2016. Biology and applications of CRISPR systems: harnessing nature's toolbox for genome engineering. Cell 164:1–229–44
    [Crossref] [Google Scholar]
  29. 29.
    Glick B, Chang TS, Jaap RG. 1956. The bursa of Fabricius and antibody production. Poult. Sci. 35:1224–25
    [Crossref] [Google Scholar]
  30. 30.
    Cooper MD, Peterson RDA, Good RA. 1965. Delineation of the thymic and bursal lymphoid systems in the chicken. Nature 205:4967143–46
    [Crossref] [Google Scholar]
  31. 31.
    Lemaitre B, Nicolas E, Michaut L, Reichhart JM, Hoffmann JA 1996. The dorsoventral regulatory gene cassette spätzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86:6973–83
    [Crossref] [Google Scholar]
  32. 32.
    Zambon RA, Nandakumar M, Vakharia VN, Wu LP. 2005. The Toll pathway is important for an antiviral response in Drosophila. PNAS 102:207257–62
    [Crossref] [Google Scholar]
  33. 33.
    Hirano M, Das S, Guo P, Cooper MD. 2011. The evolution of adaptive immunity in vertebrates. Adv. Immunol. 109:125–57
    [Google Scholar]
  34. 34.
    Kamm K, Schierwater B, DeSalle R. 2019. Innate immunity in the simplest animals—placozoans. BMC Genom 20:5
    [Crossref] [Google Scholar]
  35. 35.
    Woznica A, Kumar A, Sturge CR, Xing C, King N, Pfeiffer JK. 2021. STING mediates immune responses in the closest living relatives of animals. eLife 10:e70436
    [Crossref] [Google Scholar]
  36. 36.
    Fauci AS, Lane HC. 2020. Four decades of HIV/AIDS—much accomplished, much to do. N. Engl. J. Med. 383:11–4
    [Crossref] [Google Scholar]
  37. 37.
    Weiss SR. 2020. Forty years with coronaviruses. J. Exp. Med. 217:5e20200537
    [Crossref] [Google Scholar]
  38. 38.
    Almazán F, González JM, Pénzes Z, Izeta A, Calvo E et al. 2000. Engineering the largest RNA virus genome as an infectious bacterial artificial chromosome. PNAS 97:105516–21
    [Crossref] [Google Scholar]
  39. 39.
    Yount B, Curtis KM, Baric RS. 2000. Strategy for systematic assembly of large RNA and DNA genomes: transmissible gastroenteritis virus model. J. Virol. 74:2210600–11
    [Crossref] [Google Scholar]
  40. 40.
    Yount B, Curtis KM, Fritz EA, Hensley LE, Jahrling PB et al. 2003. Reverse genetics with a full-length infectious cDNA of severe acute respiratory syndrome coronavirus. PNAS 100:2212995–3000
    [Crossref] [Google Scholar]
  41. 41.
    Kirchdoerfer RN, Cottrell CA, Wang N, Pallesen J, Yassine HM et al. 2016. Pre-fusion structure of a human coronavirus spike protein. Nature 531:7592118–21
    [Crossref] [Google Scholar]
  42. 42.
    Wrapp D, Wang N, Corbett KS, Goldsmith JA, Hsieh C-L et al. 2020. Cryo-EM structure of the 2019-nCoV spike in the prefusion conformation. Science 367:64831260–63
    [Crossref] [Google Scholar]
  43. 43.
    Plowright RK, Parrish CR, McCallum H, Hudson PJ, Ko AI et al. 2017. Pathways to zoonotic spillover. Nat. Rev. Microbiol. 15:8502–10
    [Crossref] [Google Scholar]
  44. 44.
    Grange ZL, Goldstein T, Johnson CK, Anthony S, Gilardi K et al. 2021. Ranking the risk of animal-to-human spillover for newly discovered viruses. PNAS 118:15e2002324118
    [Crossref] [Google Scholar]
  45. 45.
    Woolhouse M, Gaunt E. 2007. Ecological origins of novel human pathogens. Crit. Rev. Microbiol. 33:4231–42
    [Crossref] [Google Scholar]
  46. 46.
    Lednicky JA, Tagliamonte MS, White SK, Elbadry MA, Alam MM et al. 2021. Independent infections of porcine deltacoronavirus among Haitian children. Nature 600:7887133–37
    [Crossref] [Google Scholar]
  47. 47.
    Kolata G, Mueller B. 2022. Halting progress and happy accidents: how mRNA vaccines were made. New York Times Jan. 15, p. A1
    [Google Scholar]
  48. 48.
    Li C-X, Shi M, Tian J-H, Lin X-D, Kang Y-J et al. 2015. Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses. eLife 4:e05378
    [Crossref] [Google Scholar]
  49. 49.
    Shi M, Lin X-D, Tian J-H, Chen L-J, Chen X et al. 2016. Redefining the invertebrate RNA virosphere. Nature 540:7634539–43
    [Crossref] [Google Scholar]
  50. 50.
    Shi M, Lin X-D, Chen X, Tian J-H, Chen L-J et al. 2018. The evolutionary history of vertebrate RNA viruses. Nature 556:7700197–202
    [Crossref] [Google Scholar]
  51. 51.
    Roossinck MJ. 2015. Move over, bacteria! Viruses make their mark as mutualistic microbial symbionts. J. Virol. 89:136532–35
    [Crossref] [Google Scholar]
  52. 52.
    Greninger AL. 2018. A decade of RNA virus metagenomics is (not) enough. Virus Res 244:218–29
    [Crossref] [Google Scholar]
  53. 53.
    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 13:7e1002210
    [Crossref] [Google Scholar]
  54. 54.
    Koonin EV, Dolja VV. 2018. Metaviromics: a tectonic shift in understanding virus evolution. Virus Res 246:A1–3
    [Crossref] [Google Scholar]
  55. 55.
    Sayers EW, Beck J, Bolton EE, Bourexis D, Brister JR et al. 2021. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 49:D1D10–17
    [Crossref] [Google Scholar]
  56. 56.
    Schoch CL, Ciufo S, Domrachev M, Hotton CL, Kannan S et al. 2020. NCBI Taxonomy: a comprehensive update on curation, resources and tools. Database 2020:baaa062
    [Crossref] [Google Scholar]
  57. 57.
    Koonin EV, Dolja VV, Krupovic M, Varsani A, Wolf YI et al. 2020. Global organization and proposed megataxonomy of the virus world. Microbiol. Mol. Biol. Rev. 84:2e00061–19
    [Crossref] [Google Scholar]
  58. 58.
    Racaniello V. 2016. Moving beyond metagenomics to find the next pandemic virus. PNAS 113:112812–14
    [Crossref] [Google Scholar]
  59. 59.
    Oldstone MBA. 2014. History of virology. Encyclopedia Microbiology TM Schmidt 608–12 Cambridge, MA: Academic
    [Google Scholar]
  60. 60.
    De Wachter R, Verhassel JP, Fiers W. 1968. The 5′-terminal tetranucleotide sequence of bacteriophage MS2 ribonucleic acid. Arch. Int. Physiol. Biochim. 76:3580–81
    [Google Scholar]
  61. 61.
    Hatcher EL, Zhdanov SA, Bao Y, Blinkova O, Nawrocki EP et al. 2017. Virus Variation Resource—improved response to emergent viral outbreaks. Nucleic Acids Res 45:D1D482–90
    [Crossref] [Google Scholar]
  62. 62.
    Stenglein MD. 2022. 2022_Annual_Review_of_Virology. Code Repository https://github.com/stenglein-lab/2022_Annual_Review_of_Virology
    [Google Scholar]
  63. 63.
    Bogner P, Capua I, Lipman DJ, Cox NJ. 2006. A global initiative on sharing avian flu data. Nature 442:7106981
    [Crossref] [Google Scholar]
  64. 64.
    Armién AG, Wolf TM, Mor SK, Ng TFF, Bracht AJ et al. 2020. Molecular and biological characterization of a Cervidpoxvirus isolated from moose with necrotizing dermatitis. Vet. Pathol. 57:2296–310
    [Crossref] [Google Scholar]
  65. 65.
    Rezaei Javan R, Ramos-Sevillano E, Akter A, Brown J, Brueggemann AB. 2019. Prophages and satellite prophages are widespread in Streptococcus and may play a role in pneumococcal pathogenesis. Nat. Commun. 10:14852
    [Crossref] [Google Scholar]
  66. 66.
    Prada D, Boyd V, Baker ML, O'Dea M, Jackson B 2019. Viral diversity of microbats within the South West Botanical Province of Western Australia. Viruses 11:121157
    [Crossref] [Google Scholar]
  67. 67.
    Strydom E, Pietersen G. 2018. Diversity of partial RNA-dependent RNA polymerase gene sequences of soybean blotchy mosaic virus isolates from different host-, geographical- and temporal origins. Arch. Virol. 163:51299–305
    [Crossref] [Google Scholar]
  68. 68.
    L'Heritier PH, Teissier G 1937. Une anomalie physiologique héréditaire chez la Drosophile. C. R. Acad. Sci. Paris 231:192–94
    [Google Scholar]
  69. 69.
    Roossinck MJ. 2010. Lifestyles of plant viruses. Philos. Trans. R. Soc. B 365:15481899–905
    [Crossref] [Google Scholar]
  70. 70.
    Ghabrial SA, Castón JR, Jiang D, Nibert ML, Suzuki N. 2015. 50-plus years of fungal viruses. Virology 479–480:356–68
    [Crossref] [Google Scholar]
  71. 71.
    Boccardo G, Lisa V, Luisoni E, Milne RG. 1987. Cryptic plant viruses. Adv. Virus Res. 32:171–214
    [Crossref] [Google Scholar]
  72. 72.
    Obbard DJ. 2018. Expansion of the metazoan virosphere: progress, pitfalls, and prospects. Curr. Opin. Virol. 31:17–23
    [Crossref] [Google Scholar]
  73. 73.
    Wang D. 2015. Fruits of virus discovery: new pathogens and new experimental models. J. Virol. 89:31486–88
    [Crossref] [Google Scholar]
  74. 74.
    Shi M, Zhang Y-Z, Holmes EC. 2018. Meta-transcriptomics and the evolutionary biology of RNA viruses. Virus Res 243:83–90
    [Crossref] [Google Scholar]
  75. 75.
    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. 15:3161–68
    [Crossref] [Google Scholar]
  76. 76.
    Allander T, Emerson SU, Engle RE, Purcell RH, Bukh J. 2001. A virus discovery method incorporating DNase treatment and its application to the identification of two bovine parvovirus species. PNAS 98:2011609–14
    [Crossref] [Google Scholar]
  77. 77.
    Breitbart M, Salamon P, Andresen B, Mahaffy JM, Segall AM et al. 2002. Genomic analysis of uncultured marine viral communities. PNAS 99:2214250–55
    [Crossref] [Google Scholar]
  78. 78.
    Wang D, Coscoy L, Zylberberg M, Avila PC, Boushey HA et al. 2002. Microarray-based detection and genotyping of viral pathogens. PNAS 99:2415687–92
    [Crossref] [Google Scholar]
  79. 79.
    Min Jou W, Haegeman G, Ysebaert M, Fiers W 1972. Nucleotide sequence of the gene coding for the bacteriophage MS2 coat protein. Nature 237:535082–88
    [Crossref] [Google Scholar]
  80. 80.
    Sanger F, Air GM, Barrell BG, Brown NL, Coulson AR et al. 1977. Nucleotide sequence of bacteriophage φX174 DNA. Nature 265:5596687–95
    [Crossref] [Google Scholar]
  81. 81.
    Racaniello VR, Baltimore D. 1981. Molecular cloning of poliovirus cDNA and determination of the complete nucleotide sequence of the viral genome. PNAS 78:84887–91
    [Crossref] [Google Scholar]
  82. 82.
    Angly FE, Felts B, Breitbart M, Salamon P, Edwards RA et al. 2006. The marine viromes of four oceanic regions. PLOS Biol 4:11e368
    [Crossref] [Google Scholar]
  83. 83.
    Tisza MJ, Pastrana DV, Welch NL, Stewart B, Peretti A et al. 2020. Discovery of several thousand highly diverse circular DNA viruses. eLife 9:e51971
    [Crossref] [Google Scholar]
  84. 84.
    de la Higuera I, Kasun GW, Torrance EL, Pratt AA, Maluenda A et al. 2020. Unveiling crucivirus diversity by mining metagenomic data. mBio 11:5e01410–20
    [Crossref] [Google Scholar]
  85. 85.
    Gregory AC, Zayed AA, Conceição-Neto N, Temperton B, Bolduc B et al. 2019. Marine DNA viral macro- and microdiversity from pole to pole. Cell 177:51109–23.e14
    [Crossref] [Google Scholar]
  86. 86.
    Roux S, Hallam SJ, Woyke T, Sullivan MB. 2015. Viral dark matter and virus-host interactions resolved from publicly available microbial genomes. eLife 4:e08490
    [Crossref] [Google Scholar]
  87. 87.
    Gilbert KB, Holcomb EE, Allscheid RL, Carrington JC. 2019. Hiding in plain sight: new virus genomes discovered via a systematic analysis of fungal public transcriptomes. PLOS ONE 14:7e0219207
    [Crossref] [Google Scholar]
  88. 88.
    Nayfach S, Páez-Espino D, Call L, Low SJ, Sberro H et al. 2021. Metagenomic compendium of 189,680 DNA viruses from the human gut microbiome. Nat. Microbiol. 6:7960–70
    [Crossref] [Google Scholar]
  89. 89.
    Armstrong J. 1985. Nucleotide Sequences 1985: A Compilation from the GenBank and EMBL Data Libraries: A Special Supplement to Nucleic Acids Research Washington, DC: IRL Press
    [Google Scholar]
  90. 90.
    Roossinck MJ. 2015. Metagenomics of plant and fungal viruses reveals an abundance of persistent lifestyles. Front. Microbiol. 5:767
    [Crossref] [Google Scholar]
  91. 91.
    Stenglein MD, Sanders C, Kistler AL, Ruby JG, Franco JY et al. 2012. Identification, characterization, and in vitro culture of highly divergent arenaviruses from boa constrictors and annulated tree boas: candidate etiological agents for snake inclusion body disease. mBio 3:4e00180–12
    [Crossref] [Google Scholar]
  92. 92.
    Bodewes R, Kik MJL, Raj VS, Schapendonk CME, Haagmans BL et al. 2013. Detection of novel divergent arenaviruses in boid snakes with inclusion body disease in the Netherlands. J. Gen. Virol. 94:Part 61206–10
    [Crossref] [Google Scholar]
  93. 93.
    Hetzel U, Sironen T, Laurinmäki P, Liljeroos L, Patjas A et al. 2013. Isolation, identification, and characterization of novel arenaviruses, the etiological agents of boid inclusion body disease. J. Virol. 87:2010918–35
    [Crossref] [Google Scholar]
  94. 94.
    Hyndman TH, Marschang RE, Wellehan JFX, Nicholls PK. 2012. Isolation and molecular identification of Sunshine virus, a novel paramyxovirus found in Australian snakes. Infect. Genet. Evol. 12:71436–46
    [Crossref] [Google Scholar]
  95. 95.
    Hyndman TH, Shilton CM, Stenglein MD, Wellehan JFX. 2018. Divergent bornaviruses from Australian carpet pythons with neurological disease date the origin of extant Bornaviridae prior to the end-Cretaceous extinction. PLOS Pathog 14:2e1006881
    [Crossref] [Google Scholar]
  96. 96.
    Stenglein MD, Jacobson ER, Wozniak EJ, Wellehan JFX, Kincaid A et al. 2014. Ball python nidovirus: a candidate etiologic agent for severe respiratory disease in Python regius. mBio 5:5e01484–14
    [Crossref] [Google Scholar]
  97. 97.
    Bodewes R, Lempp C, Schürch AC, Habierski A, Hahn K et al. 2014. Novel divergent nidovirus in a python with pneumonia. J. Gen. Virol. 95:Part 112480–85
    [Crossref] [Google Scholar]
  98. 98.
    Zhang J, Finlaison DS, Frost MJ, Gestier S, Gu X et al. 2018. Identification of a novel nidovirus as a potential cause of large scale mortalities in the endangered Bellinger River snapping turtle (Myuchelys georgesi). PLOS ONE 13:10e0205209
    [Crossref] [Google Scholar]
  99. 99.
    O'Dea MA, Jackson B, Jackson C, Xavier P, Warren K 2016. Discovery and partial genomic characterisation of a novel nidovirus associated with respiratory disease in wild shingleback lizards (Tiliqua rugosa). PLOS ONE 11:11e0165209
    [Crossref] [Google Scholar]
  100. 100.
    Sarker S, Hannon C, Athukorala A, Bielefeldt-Ohmann H. 2021. Emergence of a novel pathogenic poxvirus infection in the endangered green sea turtle (Chelonia mydas) highlights a key threatening process. Viruses 13:2219
    [Crossref] [Google Scholar]
  101. 101.
    Wu F, Zhao S, Yu B, Chen Y-M, Wang W et al. 2020. A new coronavirus associated with human respiratory disease in China. Nature 579:7798265–69
    [Crossref] [Google Scholar]
  102. 102.
    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. 87:2211966–77
    [Crossref] [Google Scholar]
  103. 103.
    Coyle MC, Elya CN, Bronski M, Eisen MB. 2018. Entomophthovirus: an insect-derived iflavirus that infects a behavior manipulating fungal pathogen of dipterans. bioRxiv 371526. https://doi.org/10.1101/371526
    [Crossref]
  104. 104.
    Li L, Victoria JG, Wang C, Jones M, Fellers GM et al. 2010. Bat guano virome: predominance of dietary viruses from insects and plants plus novel mammalian viruses. J. Virol. 84:146955–65
    [Crossref] [Google Scholar]
  105. 105.
    Roux S, Hawley AK, Torres Beltran M, Scofield M, Schwientek P et al. 2014. Ecology and evolution of viruses infecting uncultivated SUP05 bacteria as revealed by single-cell- and meta-genomics. eLife 3:e03125
    [Crossref] [Google Scholar]
  106. 106.
    Fredericks DN, Relman DA. 1996. Sequence-based identification of microbial pathogens: a reconsideration of Koch's postulates. Clin. Microbiol. Rev. 9:118–33
    [Crossref] [Google Scholar]
  107. 107.
    Walker PJ, Siddell SG, Lefkowitz EJ, Mushegian AR, Adriaenssens EM et al. 2021. Changes to virus taxonomy and to the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses 2021. Arch. Virol. 166:92633–48
    [Crossref] [Google Scholar]
  108. 108.
    Batson J, Dudas G, Haas-Stapleton E, Kistler AL, Li LM et al. Single mosquito metatranscriptomics identifies vectors, emerging pathogens and reservoirs in one assay. eLife 10:e68353
    [Crossref] [Google Scholar]
  109. 109.
    Hermida Lorenzo RJ, Cadar D, Koundouno FR, Juste J, Bialonski A et al. 2021. Metagenomic snapshots of viral components in Guinean bats. Microorganisms 9:3599
    [Crossref] [Google Scholar]
  110. 110.
    Geoghegan JL, Di Giallonardo F, Wille M, Ortiz-Baez AS, Costa VA et al. 2021. Virome composition in marine fish revealed by meta-transcriptomics. Virus Evol 7:1veab005
    [Crossref] [Google Scholar]
  111. 111.
    Tokarz R, Lipkin WI. 2020. Discovery and surveillance of tick-borne pathogens. J. Med. Entomol. 58:41525–35
    [Crossref] [Google Scholar]
  112. 112.
    Modha S, Hughes J, Bianco G, Ferguson HM, Helm B et al. 2019. Metaviromics reveals unknown viral diversity in the biting midge Culicoides impunctatus. Viruses 11:9865
    [Crossref] [Google Scholar]
  113. 113.
    Dezordi FZ, dos Santos Vasconcelos CR, Rezende AM, Wallau GL. 2020. In and outs of Chuviridae endogenous viral elements: origin of a potentially new retrovirus and signature of ancient and ongoing arms race in mosquito genomes. Front. Genet. 11:1291
    [Crossref] [Google Scholar]
  114. 114.
    Hahn MA, Rosario K, Lucas P, Dheilly NM. 2020. Characterization of viruses in a tapeworm: phylogenetic position, vertical transmission, and transmission to the parasitized host. ISME J 14:71755–67
    [Crossref] [Google Scholar]
  115. 115.
    Bryant JL. 2008. Animal models in virology. Sourcebook of Models for Biomedical Research PM Conn 557–63 Totowa, NJ: Humana
    [Google Scholar]
  116. 116.
    Xu J, Cherry S. 2014. Viruses and antiviral immunity in Drosophila. Dev. Comp. Immunol. 42:167–84
    [Crossref] [Google Scholar]
  117. 117.
    L'heritier P. 1958. The hereditary virus of Drosophila. Adv. Virus Res. 5:195–245
    [Crossref] [Google Scholar]
  118. 118.
    Rosshart SP, Herz J, Vassallo BG, Hunter A, Wall MK et al. 2019. Laboratory mice born to wild mice have natural microbiota and model human immune responses. Science 365:6452eaaw4361
    [Crossref] [Google Scholar]
  119. 119.
    Phan TG, Kapusinszky B, Wang C, Rose RK, Lipton HL, Delwart EL. 2011. The fecal viral flora of wild rodents. PLOS Pathog 7:9e1002218
    [Crossref] [Google Scholar]
  120. 120.
    Rosshart SP, Vassallo BG, Angeletti D, Hutchinson DS, Morgan AP et al. 2017. Wild mouse gut microbiota promotes host fitness and improves disease resistance. Cell 171:51015–28.e13
    [Crossref] [Google Scholar]
  121. 121.
    Wallace MA, Coffman KA, Gilbert C, Ravindran S, Albery GF et al. 2021. The discovery, distribution, and diversity of DNA viruses associated with Drosophila melanogaster in Europe. Virus Evol 7:1veab031
    [Crossref] [Google Scholar]
  122. 122.
    Williams SH, Che X, Garcia JA, Klena JD, Lee B et al. 2018. Viral diversity of house mice in New York City. mBio 9:2e01354–17
    [Google Scholar]
  123. 123.
    Félix M-A, Ashe A, Piffaretti J, Wu G, Nuez I et al. 2011. Natural and experimental infection of Caenorhabditis nematodes by novel viruses related to nodaviruses. PLOS Biol 9:1e1000586
    [Crossref] [Google Scholar]
  124. 124.
    Félix M-A, Wang D 2019. Natural viruses of Caenorhabditis nematodes. Annu. Rev. Genet. 53:313–26
    [Crossref] [Google Scholar]
  125. 125.
    Binesh CP. 2013. Mortality due to viral nervous necrosis in zebrafish Danio rerio and goldfish Carassius auratus. Dis. Aquat. Organ. 104:3257–60
    [Crossref] [Google Scholar]
  126. 126.
    Altan E, Kubiski SV, Boros Á, Reuter G, Sadeghi M et al. 2019. A highly divergent picornavirus infecting the gut epithelia of zebrafish (Danio rerio) in research institutions worldwide. Zebrafish 16:3291–99
    [Crossref] [Google Scholar]
  127. 127.
    Balla KM, Rice MC, Gagnon JA, Elde NC. 2020. Linking virus discovery to immune responses visualized during zebrafish infections. Curr. Biol. 30:112092–103.e5
    [Crossref] [Google Scholar]
  128. 128.
    Cross ST, Maertens BL, Dunham TJ, Rodgers CP, Brehm AL et al. 2020. Partitiviruses infecting Drosophila melanogaster and Aedes aegypti exhibit efficient biparental vertical transmission. J. Virol. 94:20e01070–20
    [Crossref] [Google Scholar]
  129. 129.
    Franz CJ, Renshaw H, Frezal L, Jiang Y, Félix M-A, Wang D 2014. Orsay, Santeuil and Le Blanc viruses primarily infect intestinal cells in Caenorhabditis nematodes. Virology 448:255–64
    [Crossref] [Google Scholar]
  130. 130.
    Palmer WH, Medd NC, Beard PM, Obbard DJ. 2018. Isolation of a natural DNA virus of Drosophila melanogaster, and characterisation of host resistance and immune responses. PLOS Pathog 14:6e1007050
    [Crossref] [Google Scholar]
  131. 131.
    Palmer WH, Joosten J, Overheul GJ, Jansen PW, Vermeulen M et al. 2019. Induction and suppression of NF-κB signalling by a DNA virus of Drosophila. J. Virol. 93:3e01443–18
    [Crossref] [Google Scholar]
  132. 132.
    Goldstein B, King N. 2016. The future of cell biology: emerging model organisms. Trends Cell Biol 26:11818–24
    [Crossref] [Google Scholar]
  133. 133.
    Russell JJ, Theriot JA, Sood P, Marshall WF, Landweber LF et al. 2017. Non-model model organisms. BMC Biol 15:155
    [Crossref] [Google Scholar]
  134. 134.
    Tang SKY, Marshall WF. 2017. Self-repairing cells: how single cells heal membrane ruptures and restore lost structures. Science 356:63421022–25
    [Crossref] [Google Scholar]
  135. 135.
    Hibshman JD, Clegg JS, Goldstein B. 2020. Mechanisms of desiccation tolerance: themes and variations in brine shrimp, roundworms, and tardigrades. Front. Physiol. 11:592016
    [Crossref] [Google Scholar]
  136. 136.
    Woznica A, King N. 2018. Lessons from simple marine models on the bacterial regulation of eukaryotic development. Curr. Opin. Microbiol. 43:108–16
    [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-virology-100220-112915
Loading
/content/journals/10.1146/annurev-virology-100220-112915
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error