Widespread Recombination, Reassortment, and Transmission of Unbalanced Compound Viral Genotypes in Natural Arenavirus Infections

English version České info

The facility with which viruses evolve underlies many of the problems they cause. Virus evolution is the reason we need a new flu vaccine each year. It’s how HIV and other viruses develop drug resistance. And it enables viruses to occasionally jump from animals to humans and cause new diseases. It is therefore important to understand how and under what circumstances viruses evolve. The arenaviruses are a group of viruses that infect mammals and snakes. Mammalian arenaviruses normally infect rodents but they can also infect humans, and, when they do severe and sometimes fatal disease can result. In this study, we studied genetic diversity in arenaviruses infecting captive snakes. We discovered an astonishing amount of diversity. Most snakes are infected by more than one virus strain, and these strains are merging and shuffling their genes (they are undergoing recombination and reassortment). The extent to which this is happening is exceptional, and has likely been caused by the importation and mixing in captivity of infected snakes from the wild. This provides an excellent opportunity to study the processes of virus evolution and may be an example of human activity altering its course.

Vyšlo v časopise: Widespread Recombination, Reassortment, and Transmission of Unbalanced Compound Viral Genotypes in Natural Arenavirus Infections. PLoS Pathog 11(5): e32767. doi:10.1371/journal.ppat.1004900
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004900

Souhrn

Zdroje

1. Holmes EC. Virus Evolution. In: D M Knipe, Howley P M, editors. Fields Virology. 6th ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2013. pp. 286–313.

2. Holland J, Spindler K, Horodyski F, Grabau E, Nichol S, VandePol S. Rapid evolution of RNA genomes. Science. 1982;215: 1577–1585. 7041255

3. Domingo E, Escarmís C, Sevilla N, Moya A, Elena SF, Quer J, et al. Basic concepts in RNA virus evolution. FASEB J. 1996;10: 859–864. 8666162

4. Eigen M. Self organization of matter and the evolution of biological macromolecules. Naturwissenschaften. 1971;58: 465–523. 4942363

5. Domingo E, Sheldon J, Perales C. Viral quasispecies evolution. Microbiol Mol Biol Rev MMBR. 2012;76: 159–216. doi: 10.1128/MMBR.05023-11 22688811

6. Lauring AS, Andino R. Quasispecies theory and the behavior of RNA viruses. PLoS Pathog. 2010;6: e1001005. doi: 10.1371/journal.ppat.1001005 20661479

7. Holland JJ, De La Torre JC, Steinhauer DA. RNA virus populations as quasispecies. Curr Top Microbiol Immunol. 1992;176: 1–20. 1600748

8. Hershey AD, Rotman R. Linkage Among Genes Controlling Inhibition of Lysis in a Bacterial Virus. Proc Natl Acad Sci U S A. 1948;34: 89–96. 16578282

9. Luria SE, Dulbecco R. Genetic Recombinations Leading to Production of Active Bacteriophage from Ultraviolet Inactivated Bacteriophage Particles. Genetics. 1949;34: 93–125. 17247312

10. Kirkegaard K, Baltimore D. The mechanism of RNA recombination in poliovirus. Cell. 1986;47: 433–443. 3021340

11. Domingo E. Virus Evolution. In: Knipe D M, Howley P M, editors. Fields Virology. 5th ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2007. pp. 389–421.

12. Fields BN, Joklik WK. Isolation and preliminary genetic and biochemical characterization of temperature-sensitive mutants of reovirus. Virology. 1969;37: 335–342. 5777554

13. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol Rev. 1992;56: 152–179. 1579108

14. Clavel F, Hance AJ. HIV drug resistance. N Engl J Med. 2004;350: 1023–1035. 14999114

15. Chen R, Quinones-Mateu ME, Mansky LM. Drug resistance, virus fitness and HIV-1 mutagenesis. Curr Pharm Des. 2004;10: 4065–4070. 15579088

16. Kew OM, Sutter RW, de Gourville EM, Dowdle WR, Pallansch MA. Vaccine-derived polioviruses and the endgame strategy for global polio eradication. Annu Rev Microbiol. 2005;59: 587–635. 16153180

17. Buchmeier MJ, de la Torre JC, Peters CJ. Arenaviridae: the viruses and their replication. In: Knipe D M, Howley P M, editors. Fields Virology. 5th ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2007. pp. 1791–1828.

18. Salvato MS, Clegg JCS, Buchmeier MJ, Charrel RN, Gonzalez JP, Lukashevich IS, et al. Arenaviridae. Virus taxonomy: classification and nomenclature of viruses: Ninth Report of the International Committee on Taxonomy of Viruses. San Diego: Elsevier; pp. 715–723.

19. Emonet SF, de la Torre JC, Domingo E, Sevilla N. Arenavirus genetic diversity and its biological implications. Infect Genet Evol J Mol Epidemiol Evol Genet Infect Dis. 2009;9: 417–429.

20. Gonzalez JP, Emonet S, de Lamballerie X, Charrel R. Arenaviruses. Curr Top Microbiol Immunol. 2007;315: 253–288. 17848068

21. Charrel RN, Coutard B, Baronti C, Canard B, Nougairede A, Frangeul A, et al. Arenaviruses and hantaviruses: from epidemiology and genomics to antivirals. Antiviral Res. 2011;90: 102–114. doi: 10.1016/j.antiviral.2011.02.009 21356244

22. Radoshitzky S, Bào Y, Buchmeier M, Charrel R, Clawson A, Clegg C, et al. Past, Present, and Future of Arenavirus Taxonomy. Arch Virol. 2015; In Press.

23. Stenglein MD, Sanders C, Kistler AL, Ruby JG, Franco JY, Reavill DR, et al. 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. 2012;3: e00180–00112. doi: 10.1128/mBio.00180-12 22893382

24. Chang L-W, Jacobson ER. Inclusion Body Disease, A Worldwide Infectious Disease of Boid Snakes: A Review. J Exot Pet Med. 2010;19: 216–225.

25. Bodewes R, Kik MJL, Raj VS, Schapendonk CME, Haagmans BL, Smits SL, et al. Detection of novel divergent arenaviruses in boid snakes with inclusion body disease in The Netherlands. J Gen Virol. 2013;94: 1206–1210. doi: 10.1099/vir.0.051995-0 23468423

26. Hetzel U, Sironen T, Laurinmäki P, Liljeroos L, Patjas A, Henttonen H, et al. Isolation, identification, and characterization of novel arenaviruses, the etiological agents of boid inclusion body disease. J Virol. 2013;87: 10918–10935. doi: 10.1128/JVI.01123-13 23926354

27. Hepojoki J, Kipar A, Korzyukov Y, Bell-Sakyi L, Vapalahti O, Hetzel U. Replication of Boid Inclusion Body Disease-Associated Arenaviruses Is Temperature Sensitive in both Boid and Mammalian Cells. J Virol. 2015;89: 1119–1128. doi: 10.1128/JVI.03119-14 25378485

28. Koellhoffer JF, Dai Z, Malashkevich VN, Stenglein MD, Liu Y, Toro R, et al. Structural Characterization of the Glycoprotein GP2 Core Domain from the CAS Virus, a Novel Arenavirus-Like Species. J Mol Biol. 2013; 426:1452–1468 doi: 10.1016/j.jmb.2013.12.009 24333483

29. Charrel RN, Lemasson J-J, Garbutt M, Khelifa R, Micco PD, Feldmann H, et al. New insights into the evolutionary relationships between arenaviruses provided by comparative analysis of small and large segment sequences. Virology. 2003;317: 191–196. 14698659

30. Zapata JC, Salvato MS. Arenavirus variations due to host-specific adaptation. Viruses. 2013;5: 241–278. doi: 10.3390/v5010241 23344562

31. Emonet S, Lemasson J-J, Gonzalez J-P, de Lamballerie X, Charrel RN. Phylogeny and evolution of old world arenaviruses. Virology. 2006;350: 251–257. 16494913

32. Sevilla N, de la Torre JC. Arenavirus diversity and evolution: quasispecies in vivo. Curr Top Microbiol Immunol. 2006;299: 315–335. 16568904

33. Archer AM, Rico-Hesse R. High Genetic Divergence and Recombination in Arenaviruses from the Americas. Virology. 2002;304: 274–281. 12504568

34. Charrel RN, de Lamballerie X, Emonet S. Phylogeny of the genus Arenavirus. Curr Opin Microbiol. 2008;11: 362–368. doi: 10.1016/j.mib.2008.06.001 18602020

35. Charrel RN, Feldmann H, Fulhorst CF, Khelifa R, de Chesse R, de Lamballerie X. Phylogeny of New World arenaviruses based on the complete coding sequences of the small genomic segment identified an evolutionary lineage produced by intrasegmental recombination. Biochem Biophys Res Commun. 2002;296: 1118–1124. 12207889

36. Riviere Y, Oldstone MB. Genetic reassortants of lymphocytic choriomeningitis virus: unexpected disease and mechanism of pathogenesis. J Virol. 1986;59: 363–368. 2426464

37. Lukashevich IS. Generation of reassortants between African arenaviruses. Virology. 1992;188: 600–605. 1585636

38. Vezza AC, Bishop DHL. Recombination Between Temperature-Sensitive Mutants of the Arenavirus Pichinde. J Virol. 1977;24: 712–715. 916035

39. Bodewes R, Raj VS, Kik MJL, Schapendonk CM, Haagmans BL, Smits SL, et al. Updated phylogenetic analysis of arenaviruses detected in boid snakes. J Virol. 2014;88: 1399–1400. doi: 10.1128/JVI.02753-13 24379418

40. Hetzel U, Sironen T, Laurinmäki P, Liljeroos L, Patjas A, Henttonen H, et al. Reply to “Updated phylogenetic analysis of arenaviruses detected in boid snakes.” J Virol. 2014;88: 1401. doi: 10.1128/JVI.03044-13 24379419

41. Chang L-W, Fu A, Wozniak E, Chow M, Duke DG, Green L, et al. Immunohistochemical detection of a unique protein within cells of snakes having inclusion body disease, a world-wide disease seen in members of the families Boidae and Pythonidae. PloS One. 2013;8: e82916. doi: 10.1371/journal.pone.0082916 24340066

42. Ladner JT, Beitzel B, Chain PSG, Davenport MG, Donaldson E, Frieman M, et al. Standards for Sequencing Viral Genomes in the Era of High-Throughput Sequencing. mBio. 2014;5: e01360–14. doi: 10.1128/mBio.01360-14 24939889

43. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9: 357–359. doi: 10.1038/nmeth.1923 22388286

44. Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinforma Oxf Engl. 2006;22: 1658–1659.

45. Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P. RDP3: a flexible and fast computer program for analyzing recombination. Bioinforma Oxf Engl. 2010;26: 2462–2463.

46. Sharp GB, Kawaoka Y, Jones DJ, Bean WJ, Pryor SP, Hinshaw V, et al. Coinfection of wild ducks by influenza A viruses: distribution patterns and biological significance. J Virol. 1997;71: 6128–6135. 9223507

47. Ghedin E, Fitch A, Boyne A, Griesemer S, DePasse J, Bera J, et al. Mixed infection and the genesis of influenza virus diversity. J Virol. 2009;83: 8832–8841. doi: 10.1128/JVI.00773-09 19553313

48. Takayama S, Yamazaki S, Matsuo S, Sugii S. Multiple Infection ofTT Virus(TTV) with Different Genotypes in Japanese Hemophiliacs. Biochem Biophys Res Commun. 1999;256: 208–211. 10066448

49. Niel C, Saback FL, Lampe E. Coinfection with multiple TT virus strains belonging to different genotypes is a common event in healthy Brazilian adults. J Clin Microbiol. 2000;38: 1926–1930. 10790123

50. Schmitt M, Dondog B, Waterboer T, Pawlita M, Tommasino M, Gheit T. Abundance of Multiple High-Risk Human Papillomavirus (HPV) Infections Found in Cervical Cells Analyzed by Use of an Ultrasensitive HPV Genotyping Assay. J Clin Microbiol. 2010;48: 143–149. doi: 10.1128/JCM.00991-09 19864475

51. Weng Z, Barthelson R, Gowda S, Hilf ME, Dawson WO, Galbraith DW, et al. Persistent Infection and Promiscuous Recombination of Multiple Genotypes of an RNA Virus within a Single Host Generate Extensive Diversity. PLoS ONE. 2007;2: e917. 17878952

52. Lehmann-Grube F. A carrier state of lymphocytic choriomeningitis virus in L cell cultures. Nature. 1967;213: 770–773. 4961982

53. Nguyen-hong-Diet null, Libíková H. Viral superinfection in cells carrying an arenavirus and/or a togavirus. Acta Virol. 1978;22: 477–484. 35946

54. Damonte EB, Mersich SE, Coto CE. Response of cells persistently infected with arenaviruses to superinfection with homotypic and heterotypic viruses. Virology. 1983;129: 474–478. 6312683

55. Bruns M, Zeller W, Lehmann-Grube F. Studies on the mechanism of lymphocytic choriomeningitis virus homologous interference. Med Microbiol Immunol (Berl). 1986;175: 101–104. 3014286

56. Ellenberg P, Edreira M, Scolaro L. Resistance to superinfection of Vero cells persistently infected with Junin virus. Arch Virol. 2004;149: 507–522. 14991440

57. Welsh RM, Pfau CJ. Determinants of lymphocytic choriomeningitis interference. J Gen Virol. 1972;14: 177–187. 4622135

58. Tauraso N, Shelokov A. PROTECTION AGAINST JUNIN VIRUS BY IMMUNIZATION WITH LIVE TACARIBE VIRUS. Proc Soc Exp Biol Med Soc Exp Biol Med N Y N. 1965;119: 608–611. 14328956

59. Weissenbacher MC, Coto CE, Calello MA. Cross-protection between Tacaribe complex viruses. Presence of neutralizing antibodies against Junin virus (Argentine hemorrhagic fever) in guinea pigs infected with Tacaribe virus. Intervirology. 1975;6: 42–49. 178627

60. Weissenbacher MC, Coto CE, Calello MA, Rondinone SN, Damonte EB, Frigerio MJ. Cross-protection in nonhuman primates against Argentine hemorrhagic fever. Infect Immun. 1982;35: 425–430. 6276301

61. Hall MP, Unch J, Binkowski BF, Valley MP, Butler BL, Wood MG, et al. Engineered luciferase reporter from a deep sea shrimp utilizing a novel imidazopyrazinone substrate. ACS Chem Biol. 2012;7: 1848–1857. doi: 10.1021/cb3002478 22894855

62. Emonet SF, Garidou L, McGavern DB, de la Torre JC. Generation of recombinant lymphocytic choriomeningitis viruses with trisegmented genomes stably expressing two additional genes of interest. Proc Natl Acad Sci U S A. 2009;106: 3473–3478. doi: 10.1073/pnas.0900088106 19208813

63. A revision of the system of nomenclature for influenza viruses: a WHO Memorandum. Bull World Health Organ. 1980;58: 585–591. 6969132

64. Collis A, Fenili R. The Modern U.S. Reptile Industry [Internet]. Georgetown Economic Services, LLC; 2011. http://www.whitehouse.gov/sites/default/files/omb/assets/oira_1018/1018_04182011-3.pdf

65. Webster RG. Wet markets—a continuing source of severe acute respiratory syndrome and influenza? The Lancet. 2004;363: 234–236. 14738798

66. Knust B, Ströher U, Edison L, Albariño CG, Lovejoy J, Armeanu E, et al. Lymphocytic Choriomeningitis Virus in Employees and Mice at Multipremises Feeder-Rodent Operation, United States, 2012. Emerg Infect Dis. 2014;20: 240–247. doi: 10.3201/eid2002.130860 24447605

67. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001;29: e45. 11328886

68. Peirson SN, Butler JN, Foster RG. Experimental validation of novel and conventional approaches to quantitative real-time PCR data analysis. Nucleic Acids Res. 2003;31: e73. 12853650

69. Stenglein MD, Jacobson ER, Wozniak EJ, Wellehan JFX, Kincaid A, Gordon M, et al. Ball Python Nidovirus: a Candidate Etiologic Agent for Severe Respiratory Disease in Python regius. mBio. 2014;5: e01484–14. doi: 10.1128/mBio.01484-14 25205093

70. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinforma Oxf Engl. 2009;25: 2078–2079.

71. Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Heled J, et al. Geneious v5.1 [Internet]. 2010. http://www.geneious.com

72. Ruby JG, Bellare P, DeRisi JL. PRICE: Software for the Targeted Assembly of Components of (Meta)Genomic Sequence Data. G3 GenesGenomesGenetics. 2013; g3.113.005967.

73. Katoh K, Standley DM. MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability. Mol Biol Evol. 2013;30: 772–780. doi: 10.1093/molbev/mst010 23329690

74. Talavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol. 2007;56: 564–577. 17654362

75. Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods. 2012;9: 772–772. doi: 10.1038/nmeth.2109 22847109

76. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 2003;52: 696–704. 14530136

77. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinforma Oxf Engl. 2003;19: 1572–1574.

78. Hamada M, Kiryu H, Sato K, Mituyama T, Asai K. Prediction of RNA secondary structure using generalized centroid estimators. Bioinformatics. 2009;25: 465–473. doi: 10.1093/bioinformatics/btn601 19095700