Widespread Reassortment Shapes the Evolution and Epidemiology of Bluetongue Virus following European Invasion

PLoS Pathogens

Volumn 11, Issue 8, 2015, Pages

  Nomikou, Kyriaki ^a   Hughes, Joseph ^b   Wash, Rachael ^c   Kellam, Paul ^c,d   Breard, Emmanuel ^e   Zientara, Stéphan ^e   Palmarini, Massimo ^b   Biek, Roman ^b,f   Mertens, Peter ^a  

^a INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

^b MRC UNIVERSITY OF GLASGOW CENTRE FOR VIRUS RESEARCH   (United Kingdom)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e FRENCH AGENCY FOR FOOD   (France)

^f UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

LIVE VACCINE;

ARTICLE; BLUETONGUE ORBIVIRUS; EPISTASIS; EVOLUTION; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC REASSORTMENT; GENETIC VARIABILITY; GENOTYPE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHYLOGENY; POLYMERASE CHAIN REACTION; RNA EXTRACTION; SEROTYPE; UNINDEXED SEQUENCE; VIRUS ISOLATION; BLUETONGUE; EUROPE; GENETICS; MOLECULAR EVOLUTION; MOLECULAR GENETICS; REAL TIME POLYMERASE CHAIN REACTION;

BLUETONGUE; BLUETONGUE VIRUS; EUROPE; EVOLUTION, MOLECULAR; MOLECULAR SEQUENCE DATA; PHYLOGENY; REAL-TIME POLYMERASE CHAIN REACTION; REASSORTANT VIRUSES;

EID: 84940735813     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005056     Document Type: Article

References (79)

1. Simon-Loriere E, Holmes EC, Why do RNA viruses recombine? Nat Rev Microbiol. 2011;9: 617–626. doi: 10.1038/nrmicro2614 21725337
2. McDonald SM, Patton JT, Assortment and packaging of the segmented rotavirus genome. Trends Microbiol. 2011;19: 136–144. doi: 10.1016/j.tim.2010.12.002 21195621
3. Horimoto T, Kawaoka Y, Influenza: lessons from past pandemics, warnings from current incidents. Nat Rev Microbiol. 2005;3: 591–600. 16064053
4. Taubenberger JK, Kash JC, Influenza virus evolution, host adaptation, and pandemic formation. Cell Host and Microbe. Elsevier Inc.; 2010. pp. 440–451. doi: 10.1016/j.chom.2010.05.009
5. Mukherjee A, Dutta D, Ghosh S, Bagchi P, Chattopadhyay S, Nagashima S, et al. Full genomic analysis of a human group A rotavirus G9P[6] strain from Eastern India provides evidence for porcine-to-human interspecies transmission. Arch Virol. 2009;154: 733–746. doi: 10.1007/s00705-009-0363-3 19333549
6. Lakdawala SS, Wu Y, Wawrzusin P, Kabat J, Broadbent AJ, Lamirande EW, et al. Influenza A virus assembly intermediates fuse in the cytoplasm. PLoS Pathog. 2014;10. doi: 10.1371/journal.ppat.1003971
7. Mertens PPC, Maan S, Samuel A, Attoui H, Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA, Orbivirus, Reoviridae. In: Virus Taxonomy, VIIIth Report of the ICTV. Elsevier/Academic Press, London; 2005. pp. 466–483.
8. Attoui H, Maan S, Anthony SJ, Mertens PPCPC, Mellor PS, Baylis M, Mellor PS, Baylis M, Mertens PPC, et al. 3-Bluetongue virus, other orbiviruses and other reoviruses: Their relationships and taxonomy [Internet]. 1st ed. Bluetongue. Elsevier/Academic Press, London; 2009.
9. Batten C, Darpel K, Henstock M, Fay P, Veronesi E, Gubbins S, Ikegami T, et al. Evidence for transmission of bluetongue virus serotype 26 through direct contact. PLoS One. 2014;9: e96049. doi: 10.1371/journal.pone.0096049 24797910
10. Mertens PPC, Brown F, Sangar D, Assignment of the genome segments of bluetongue virus type 1 to the proteins which they encode. Virology. 1984;135: 207–217. 6328750
11. Ratinier M, Caporale M, Golder M, Franzoni G, Allan K, Nunes SF, Heise M, et al. Identification and characterization of a novel non-structural protein of bluetongue virus. PLoS Pathog. 2011;7: e1002477. doi: 10.1371/journal.ppat.1002477 22241985
12. Huismans H, Erasmus BJ, Identification of the serotype-specific and group-specific antigens of bluetongue virus. Onderstepoort J Vet Res. 1981;48: 51–58. 6273773
13. Kahlon J, Sugiyama K, Roy P, Molecular basis of bluetongue virus neutralization. J Virol. 1983;48: 627–632. 6313962
14. Maan S, Maan NS, Nomikou K, Veronesi E, Bachanek-Bankowska K, Belaganahalli MN, et al. Complete genome characterisation of a novel 26th bluetongue virus serotype from Kuwait. PLoS One. 2011;6. doi: 10.1371/journal.pone.0026147
15. Shaw AE, Ratinier M, Nunes SF, Nomikou K, Caporale M, Golder M, et al. Reassortment between two serologically unrelated bluetongue virus strains is flexible and can involve any genome segment. J Virol. 2013;87: 543–557. doi: 10.1128/JVI.02266-12 23097432
16. Maan S, Maan NS, Ross-smith N, Batten CA, Shaw AE, Anthony SJ, et al. Sequence analysis of bluetongue virus serotype 8 from the Netherlands 2006 and comparison to other European strains. Virology. 2008;377: 308–318. doi: 10.1016/j.virol.2008.04.028 18570969
17. Samal SK, Livingston CW, McConnell S, Ramig RF, Analysis of mixed infection of sheep with bluetongue virus serotypes 10 and 17: evidence for genetic reassortment in the vertebrate host. J Virol. 1987;61: 1086–1091. doi: 10.1099/0022-1317-68-9-2319 3029402
18. Samal SK, El-Hussein A, Holbrook FR, Beaty BJ, Ramig RF, Mixed infection of Culicoides variipennis with bluetongue virus serotypes 10 and 17: evidence for high frequency reassortment in the vector. J Gen Virol. 1987;68: 2319–2329. 2821173
19. Oberst RD, Stott JL, Blanchard-Channell M, Osburn BI, Genetic reassortment of bluetongue virus serotype 11 strains in the bovine. Vet Microbiol. 1987;15: 11–18. 2830703
20. Stott JL, Oberst RD, Channell MB, Osburn BI, Genome segment reassortment between two serotypes of bluetongue virus in a natural host. J Virol. 1987;61: 2670–2674. 3039160
21. Heidner HW, Iezzi LG, Osburn BI, MacLachlan NJ, Genetic variation and evolutionary relationships amongst bluetongue viruses endemic in the United States. Virus Res. 1991;21: 91–109. 1661983
22. Sugiyama K, Bishop DH, Roy P, Analyses of the genomes of bluetongue viruses recovered in the United States. I. Oligonucleotide fingerprint studies that indicate the existence of naturally occurring reassortant BTV isolates. Virology. 1981;114: 210–217. 6269284
23. Sugiyama K, Bishop DH, Roy P, Analysis of the genomes of bluetongue viruses recovered from different states of the United States and at different times. Am J Epidemiol. 1982;115: 332–347. 6278927
24. Squire KRE, Osburn BI, Chuang RY, Doi RH, A survey of electropherotype relationships of bluetongue virus isolates from the Western United States. J Gen Virol. 1983;64: 2103–2115. 6311948
25. Collisson E, Roy P, Analysis of the genomes of bluetongue virus serotype 10 vaccines and a recent BTV-10 isolate from Washington. Am J Vet Res. 1983;44: 235–243. 6299144
26. De Mattos CC, de Mattos CA, MacLachlan NJ, Giavedoni LD, Yilma T, Osburn BI, Phylogenetic comparison of the S3 gene of United States prototype strains of bluetongue virus with that of field isolates from California. J Virol. 1996;70: 5735–5739. 8764098
27. Osburn BI, de Mattos CA, de Mattos CC, MacLachlan NJ, Bluetongue disease and the molecular epidemiology of viruses from the western United States. Comp Immunol Microbiol Infect Dis. 1996;19: 181–190. 0147957196000033 [pii] 8800543
28. Pritchard LI, Sendow I, Lunt R, Hassan SH, Kattenbelt J, Gould AR, et al. Genetic diversity of bluetongue viruses in south east Asia. Virus Res. 2004;101: 193–201. 15041187
29. Gould AR, Pritchard LI, Relationships amongst bluetongue viruses revealed by comparisons of capsid and outer coat protein nucleotide sequences. Virus Res. 1990;17: 31–52. 2171239
30. Boyle DB, Bulach DM, Amos-Ritchie R, Adams MM, Walker PJ, Weir R, Genomic sequences of Australian bluetongue virus prototype serotypes reveal global relationships and possible routes of entry into Australia. J Virol. 2012;86: 6724–6731. doi: 10.1128/JVI.00182-12 22514341
31. Boyle DB, Amos-Ritchie R, Broz I, Walker PJ, Melville L, Flanagan D, et al. Evolution of bluetongue virus serotype 1 in northern Australia over 30 years. J Virol. 2014;88: 13981–13989. doi: 10.1128/JVI.02055-14 25253345
32. Carpi G, Holmes EC, Kitchen A, The evolutionary dynamics of bluetongue virus. J Mol Evol. 2010;70: 583–592. doi: 10.1007/s00239-010-9354-y 20526713
33. Mellor PS, Baylis M, Mertens PPC, Bluetongue. Bluetongue. Academic Press, London, United Kingdom.; 2009.
34. Purse BV, Mellor PS, Rogers DJ, Samuel AR, Mertens PPC, Baylis M, Climate change and the recent emergence of bluetongue in Europe. Nat Rev Microbiol. 2005;3: 171–181. 15685226
35. Carpenter S, Wilson A, Mellor PS, Culicoides and the emergence of bluetongue virus in northern Europe. Trends in Microbiology. 2009. pp. 172–178. doi: 10.1016/j.tim.2009.01.001 19299131
36. Hofmann MA, Renzullo S, Mader M, Chaignat V, Worwa G, Thuer B, Genetic characterization of toggenburg orbivirus, a new bluetongue virus, from goats, Switzerland. Emerg Infect Dis. 2008;14: 1855–1861. doi: 10.3201/eid1412.080818 19046507
37. Zientara S, Sailleau C, Viarouge C, Höper D, Beer M, Jenckel M, et al. Novel bluetongue virus in goats, Corsica, France, 2014. Emerg Infect Dis. 2014;20: 2123–2132. doi: 10.3201/eid2012.140924 25418049
38. Batten CA, Maan S, Shaw AE, Maan NS, Mertens PPC, A European field strain of bluetongue virus derived from two parental vaccine strains by genome segment reassortment. Virus Res. 2008;137: 56–63. doi: 10.1016/j.virusres.2008.05.016 18598726
39. Lorusso A, Sghaier S, Carvelli A, Di Gennaro A, Leone A, Marini V, et al. Bluetongue virus serotypes 1 and 4 in Sardinia during autumn 2012: New incursions or re-infection with old strains? Infect Genet Evol. Elsevier B.V.; 2013;19: 81–87. doi: 10.1016/j.meegid.2013.06.028
40. Lorusso A, Costessi A, Pirovano W, Marcacci M, Cammá C, Savini G, Complete genome sequence analysis of a reassortant strain of bluetongue virus serotype 16 from Italy. Genome Annoucements. 2013. pp. e00622–13. doi: 10.1128/genomeA.00622-13
41. Savini G, MacLachlan NJ, Sanchez-Vizcaino JM, Zientara S, Vaccines against bluetongue in Europe. Comp Immunol Microbiol Infect Dis. 2008;31: 101–120. 17765305
42. Barros SC, Ramos F, Luís TM, Vaz A, Duarte M, Henriques M, et al. Molecular epidemiology of bluetongue virus in Portugal during 2004–2006 outbreak. Vet Microbiol. 2007;124: 25–34. 17521832
43. Maan S, Maan NS, van Rijn PA, van Gennip RGP, Sanders O, Wright IM, Fouchier RAM, et al. Full genome characterisation of bluetongue virus serotype 6 from the Netherlands 2008 and comparison to other field and vaccine strains. PLoS One. 2010;5: e10323. doi: 10.1371/journal.pone.0010323 20428242
44. Vandenbussche F, Sailleau C, Rosseel T, Desprat A, Viarouge C, Richardson J, et al. Full-genome sequencing of four bluetongue virus serotype 11 viruses. Transbound Emerg Dis. 2013; 1865–1682. doi: 10.1111/tbed.12178
45. Listeš E, Monaco F, Labrović A, Paladini C, Leone A, Di Gialleonardo L, et al. First evidence of bluetongue virus serotype 16 in Croatia. Vet Microbiol. 2009;138: 92–97. doi: 10.1016/j.vetmic.2009.03.011 19376658
46. Ragonnet-Cronin M, Hodcroft E, Hué S, Fearnhill E, Delpech V, Brown AJL, et al. Automated analysis of phylogenetic clusters. BMC Bioinformatics. 2013;14: 317. doi: 10.1186/1471-2105-14-317 24191891
47. Kosakovsky Pond SL, Frost SDW, Pond SLK, Frost SDW, Not So Different After All: A Comparison of Methods for Detecting Amino Acid Sites Under Selection. Mol Biol. 2004;22: 1208–1222.
48. Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Kosakovsky Pond SL, Detecting individual sites subject to episodic diversifying selection. PLoS Genet. 2012;8. doi: 10.1371/journal.pgen.1002764
49. Caporale M, Wash R, Pini A, Savini G, Franchi P, Golder M, et al. Determinants of bluetongue virus virulence in murine models of disease. J Virol. 2011;85: 11479–11489. doi: 10.1128/JVI.05226-11 21865388
50. Kobayashi N, Kojima K, Taniguchi K, Urasawa T, Urasawa S, Non-random selection of gene segment 3 and random selection of gene segment 5 observed in reassortants generated in vitro between rotavirus SA11 and RRV. Res Virol. 1995;146: 53–59. 7754237
51. Lu L, Lycett SJ, Leigh Brown AJ, Reassortment patterns of avian influenza virus internal segments among different subtypes. BMC Evol Biol. 2014;14: 16. doi: 10.1186/1471-2148-14-16 24456010
52. Rambaut A, Pybus OG, Nelson MI, Viboud C, Taubenberger JK, Holmes EC, The genomic and epidemiological dynamics of human influenza A virus. Nature. 2008;453: 615–619. doi: 10.1038/nature06945 18418375
53. Elliott RM, Orthobunyaviruses: recent genetic and structural insights. Nat Rev Microbiol. Nature Publishing Group; 2014;12: 673–685. doi: 10.1038/nrmicro3332
54. Anbalagan S, Cooper E, Klumper P, Simonson RR, Hause BM, Whole genome analysis of epizootic hemorrhagic disease virus identified limited genome constellations and preferential reassortment. J Gen Virol. 2014;95: 434–441. doi: 10.1099/vir.0.059659-0 24189621
55. Nason EL, Rothagel R, Mukherjee SK, Kar AK, Forzan M, Prasad BVV, et al. Interactions between the inner and outer capsids of bluetongue virus. J Virol. 2004;78: 8059–8067. 15254177
56. Roy P, Noad R, Bluetongue virus assembly and morphogenesis. Curr Top Microbiol Immunol. 2006;309: 87–116. 16909898
57. Gouet P, Diprose JM, Grimes JM, Malby R, Burroughs JN, Zientara S, et al. The highly ordered double-stranded RNA genome of bluetongue virus revealed by crystallography. Cell. 1999;97: 481–490. 10338212
58. Grimes JM, Jakana J, Ghosh M, Basak AK, Roy P, Chiu W, et al. An atomic model of the outer layer of the bluetongue virus core derived from X-ray crystallography and electron cryomicroscopy. Structure. 1997;5: 885–893. 9261080
59. Roy P, Bluetongue virus: Dissection of the polymerase complex. J Gen Virol. 2008;89: 1789–1804. doi: 10.1099/vir.0.2008/002089-0 18632949
60. Mertens PPC, Diprose J, The bluetongue virus core: A nano-scale transcription machine. Virus Res. 2004;101: 29–43. 15010215
61. Nunes SF, Hamers C, Ratinier M, Shaw A, Brunet S, Hudelet P, et al. A synthetic biology approach for a vaccine platform against known and newly emerging serotypes of bluetongue virus. J Virol. 2014;88: 12222–12232. doi: 10.1128/JVI.02183-14 25142610
62. Bonneau KR, Mullens BA, MacLachlan NJ, Occurrence of genetic drift and founder effect during quasispecies evolution of the VP2 and NS3/NS3A genes of bluetongue virus upon passage between sheep, cattle, and Culicoides sonorensis. J Virol. 2001;75: 8298–8305. 11483775
63. Caporale M, Di Gialleonorado L, Janowicz A, Wilkie G, Shaw A, Savini G, et al. Virus and host factors affecting the clinical outcome of bluetongue virus Infection. J Virol. 2014;88: 10399–10411. doi: 10.1128/JVI.01641-14 24991012
64. Maan NS, Maan S, Belaganahalli MN, Ostlund EN, Johnson DJ, Nomikou K, et al. Identification and differentiation of the twenty six bluetongue virus serotypes by RT-PCR amplification of the serotype-specific genome segment 2. PLoS One. 2012;7: e32601. doi: 10.1371/journal.pone.0032601 22389711
65. Maan S, Rao S, Maan NS, Anthony SJ, Attoui H, Samuel AR, et al. Rapid cDNA synthesis and sequencing techniques for the genetic study of bluetongue and other dsRNA viruses. J Virol Methods. 2007;143: 132–139. 17433453
66. Potgieter AC, Page NA, Liebenberg J, Wright IM, Landt O, van Dijk AA, Improved strategies for sequence-independent amplification and sequencing of viral double-stranded RNA genomes. J Gen Virol. 2009;90: 1423–1432. doi: 10.1099/vir.0.009381-0 19264638
67. The GAP Group, GAP—Groups, Algorithms, and Programming version 4.7.5. 2014.
68. Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P, RDP3: A flexible and fast computer program for analyzing recombination. Bioinformatics. 2010;26: 2462–2463. doi: 10.1093/bioinformatics/btq467 20798170
69. Suyama M, Torrents D, Bork P, PAL2NAL: Robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 2006;34: 609–612.
70. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Molecular Systems Biology. 2011. doi: 10.1038/msb.2011.75
71. Shapiro B, Ho SYW, Drummond AJ, Suchard MA, Pybus OG, Rambaut A, A bayesian phylogenetic method to estimate unknown sequence ages. Mol Biol Evol. 2011;28: 879–887. doi: 10.1093/molbev/msq262 20889726
72. Drummond AJ, Suchard MA, Xie D, Rambaut A, Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 2012;29: 1969–1973. doi: 10.1093/molbev/mss075 22367748
73. Shapiro B, Rambaut A, Drummond AJ, Choosing Appropriate Substitution Models for the Phylogenetic Analysis of Protein-Coding Sequences. Mol Biol. 2003;23: 2003–2005.
74. Rambaut A, Suchard M, Xie D, Drummond A. Tracer version 1.6. 2013.
75. Maddison WP, Maddison DR. Mesquite: a modular system for evolutionary analysis version 3.01. 2014.
76. Huerta-Cepas J, Dopazo J, Gabaldón T, ETE: a python environment for tree exploration. BMC Bioinformatics. 2010;11: 24. doi: 10.1186/1471-2105-11-24 20070885
77. Bahl J, Krauss S, Kühnert D, Fourment M, Raven G, Pryor SP, et al. Influenza A virus migration and persistence in North American wild birds. PLoS Pathog. 2013;9. doi: 10.1371/journal.ppat.1003570
78. Oksanen J, Kindt R, Legendre P, O’Hara B, Simpson G, Solymos P, et al. Vegan: community ecology package. R package version 1.15–2. 2009.
79. Dormann CF, Gruber B, Frund J. The bipartite package version 0.5. R Project for Statistical Computing, Vienna, Austria; 2008.