1887

Abstract

This study is focused on the identification of the faecal virome of healthy chickens raised in high-density, export-driven poultry farms in Brazil. Following high-throughput sequencing, a total of 7743 -assembled contigs were constructed and compared with known nucleotide/amino acid sequences from the GenBank database. Analyses with x revealed that 279 contigs (4 %) were related to sequences of eukaryotic viruses. Viral genome sequences (total or partial) indicative of members of recognized viral families, including , , , , , and , were identified, some of those representing novel genotypes. In addition, a range of circular replication-associated protein encoding DNA viruses were also identified. The characterization of the faecal virome of healthy chickens described here not only provides a description of the viruses encountered in such niche but should also represent a baseline for future studies comparing viral populations in healthy and diseased chicken flocks. Moreover, it may also be relevant for human health, since chickens represent a significant proportion of the animal protein consumed worldwide.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000711
2017-04-01
2020-01-22
Loading full text...

Full text loading...

/deliver/fulltext/jgv/98/4/690.html?itemId=/content/journal/jgv/10.1099/jgv.0.000711&mimeType=html&fmt=ahah

References

  1. Day JM, Oakley BB, Seal BS, Zsak L. Comparative analysis of the intestinal bacterial and RNA viral communities from sentinel birds placed on selected broiler chicken farms. PLoS One 2015;10:e0117210 [CrossRef][PubMed]
    [Google Scholar]
  2. Sergeant MJ, Constantinidou C, Cogan TA, Bedford MR, Penn CW et al. Extensive microbial and functional diversity within the chicken cecal microbiome. PLoS One 2014;9:e91941 [CrossRef][PubMed]
    [Google Scholar]
  3. Oakley BB, Morales CA, Line J, Berrang ME, Meinersmann RJ et al. The poultry-associated microbiome: network analysis and farm-to-fork characterizations. PLoS One 2013;8:e57190 [CrossRef][PubMed]
    [Google Scholar]
  4. Torok VA, Hughes RJ, Mikkelsen LL, Perez-Maldonado R, Balding K et al. Identification and characterization of potential performance-related gut microbiotas in broiler chickens across various feeding trials. Appl Environ Microbiol 2011;77:5868–5878 [CrossRef][PubMed]
    [Google Scholar]
  5. Danzeisen JL, Kim HB, Isaacson RE, Tu ZJ, Johnson TJ. Modulations of the chicken cecal microbiome and metagenome in response to anticoccidial and growth promoter treatment. PLoS One 2011;6:e27949 [CrossRef][PubMed]
    [Google Scholar]
  6. Shah JD, Baller J, Zhang Y, Silverstein K, Xing Z et al. Comparison of tissue sample processing methods for harvesting the viral metagenome and a snapshot of the RNA viral community in a turkey gut. J Virol Methods 2014;209:15–24 [CrossRef][PubMed]
    [Google Scholar]
  7. Shah JD, Desai PT, Zhang Y, Scharber SK, Baller J et al. Development of the intestinal RNA virus community of healthy broiler chickens. PLoS One 2016;11:e0150094 [CrossRef][PubMed]
    [Google Scholar]
  8. Mokili JL, Rohwer F, Dutilh BE. Metagenomics and future perspectives in virus discovery. Curr Opin Virol 2012;2:63–77 [CrossRef][PubMed]
    [Google Scholar]
  9. Rosario K, Breitbart M. Exploring the viral world through metagenomics. Curr Opin Virol 2011;1:289–297 [CrossRef][PubMed]
    [Google Scholar]
  10. Victoria JG, Kapoor A, Li L, Blinkova O, Slikas B et al. Metagenomic analyses of viruses in stool samples from children with acute flaccid paralysis. J Virol 2009;83:4642–4651 [CrossRef][PubMed]
    [Google Scholar]
  11. Breitbart M, Hewson I, Felts B, Mahaffy JM, Nulton J et al. Metagenomic analyses of an uncultured viral community from human feces. J Bacteriol 2003;185:6220–6223 [CrossRef][PubMed]
    [Google Scholar]
  12. Shan T, Li L, Simmonds P, Wang C, Moeser A et al. The fecal virome of pigs on a high-density farm. J Virol 2011;85:11697–11708 [CrossRef][PubMed]
    [Google Scholar]
  13. Zhang B, Tang C, Yue H, Ren Y, Song Z. Viral metagenomics analysis demonstrates the diversity of viral flora in piglet diarrhoeic faeces in China. J Gen Virol 2014;95:1603–1611 [CrossRef][PubMed]
    [Google Scholar]
  14. Day JM, Zsak L. Recent progress in the characterization of avian enteric viruses. Avian Dis 2013;57:573–580 [CrossRef][PubMed]
    [Google Scholar]
  15. Yeoman CJ, Chia N, Jeraldo P, Sipos M, Goldenfeld ND et al. The microbiome of the chicken gastrointestinal tract. Anim Health Res Rev 2012;13:89–99 [CrossRef]
    [Google Scholar]
  16. Devaney R, Trudgett J, Trudgett A, Meharg C, Smyth V. A metagenomic comparison of endemic viruses from broiler chickens with runting-stunting syndrome and from normal birds. Avian pathol 2016;45:1–14[Crossref]
    [Google Scholar]
  17. Breitbart M, Haynes M, Kelley S, Angly F, Edwards RA et al. Viral diversity and dynamics in an infant gut. Res Microbiol 2008;159:367–373 [CrossRef][PubMed]
    [Google Scholar]
  18. Berk AJ. Adenoviridae. In Knipe DM, Howley PM. (editors) Fields Virology, 2nd ed. Philadelphia: Lippincott Willians & Wilkins; 2013
    [Google Scholar]
  19. Schrenzel M, Oaks JL, Rotstein D, Maalouf G, Snook E et al. Characterization of a new species of adenovirus in falcons. J Clin Microbiol 2005;43:3402–3413 [CrossRef][PubMed]
    [Google Scholar]
  20. Hess M. Detection and differentiation of avian adenoviruses: a review. Avian Pathol 2000;29:195–206 [CrossRef]
    [Google Scholar]
  21. Zhao J, Zhong Q, Zhao Y, Hu YX, Zhang GZ. Pathogenicity and complete genome characterization of fowl adenoviruses isolated from chickens associated with inclusion body hepatitis and hydropericardium syndrome in China. PLoS One 2015;10:e0133073 [CrossRef][PubMed]
    [Google Scholar]
  22. Fitzgerald SD. Adenovirus Infections. In Fadly AM, Glisson JR, McDouglas LR, Nolan LK, Swayne DE. et al (editors) Diseases of Poultry Ames: Blackwell Publishing; 2008; p.1324
    [Google Scholar]
  23. Domanska-Blicharz K, Tomczyk G, Smietanka K, Kozaczynski W, Minta Z. Molecular characterization of fowl adenoviruses isolated from chickens with gizzard erosions. Poult Sci 2011;90:983–989 [CrossRef][PubMed]
    [Google Scholar]
  24. Mettifogo E, Nuñez LFN, Santander Parra SH, Astolfi-Ferreira CS, Ferreira AJP. Fowl adenovirus group I as a causal agent of inclusion body hepatitis/hydropericardium syndrome (IBH/HPS) outbreak in brazilian broiler flocks. Pesq Vet Bras 2014;34:733–737 [CrossRef]
    [Google Scholar]
  25. Li L, Pesavento PA, Gaynor AM, Duerr RS, Phan TG et al. A Gyrovirus infecting a sea bird. Arch Virol 2015;160:2105–2109 [CrossRef][PubMed]
    [Google Scholar]
  26. ICTV. Virus Taxonomy 2015; Release: international committee on taxonomy of viruses; 2016. www.ictvonline.org/virusTaxonomy.asp accessed 15-Nov-2016
  27. Chu DK, Poon LL, Chiu SS, Chan KH, Ng EM et al. Characterization of a novel gyrovirus in human stool and chicken meat. J Clin Virol 2012;55:209–213 [CrossRef][PubMed]
    [Google Scholar]
  28. Fehér E, Pazár P, Kovács E, Farkas SL, Lengyel G et al. Molecular detection and characterization of human gyroviruses identified in the ferret fecal virome. Arch Virol 2014;159:3401–3406 [CrossRef][PubMed]
    [Google Scholar]
  29. Phan TG, da Costa AC, Zhang W, Pothier P, Ambert-Balay K et al. A new Gyrovirus in human feces. Virus Genes 2015;51:132–135 [CrossRef][PubMed]
    [Google Scholar]
  30. Todd D, Connor TJ, Calvert VM, Creelan JL, Meehan BM et al. Molecular cloning of an attenuated chicken anaemia virus isolate following repeated cell culture passage. Avian Pathol 1995;24:171–187 [CrossRef]
    [Google Scholar]
  31. Zhang X, Xie Q, Ji J, Chang S, Liu J et al. Complete genome sequence analysis of a recent chicken anemia virus isolate and comparison with a chicken anemia virus isolate from human fecal samples in China. J Virol 2012;86:10896–10897 [CrossRef][PubMed]
    [Google Scholar]
  32. Rimondi A, Pinto S, Olivera V, Dibárbora M, Pérez-Filgueira M et al. Comparative histopathological and immunological study of two field strains of chicken anemia virus. Vet Res 2014;45:102 [CrossRef][PubMed]
    [Google Scholar]
  33. Eltahir YM, Qian K, Jin W, Wang P, Qin A. Molecular epidemiology of chicken anemia virus in commercial farms in China. Virol J 2011;8:145 [CrossRef][PubMed]
    [Google Scholar]
  34. dos Santos HF, Knak MB, de Castro FL, Slongo J, Ritterbusch GA et al. Variants of the recently discovered avian Gyrovirus 2 are detected in Southern Brazil and the Netherlands. Vet Microbiol 2012;155:230–236 [CrossRef][PubMed]
    [Google Scholar]
  35. Abolnik C, Wandrag DB. Avian Gyrovirus 2 and avirulent Newcastle disease virus coinfection in a chicken flock with neurologic symptoms and high mortalities. Avian Dis 2014;58:90–94 [CrossRef][PubMed]
    [Google Scholar]
  36. Phan TG, Li L, O'Ryan MG, Cortes H, Mamani N et al. A third Gyrovirus species in human faeces. J Gen Virol 2012;93:1356–1361 [CrossRef][PubMed]
    [Google Scholar]
  37. Rijsewijk FA, Dos Santos HF, Teixeira TF, Cibulski SP, Varela AP et al. Discovery of a genome of a distant relative of chicken anemia virus reveals a new member of the genus Gyrovirus. Arch Virol 2011;156:1097–1100 [CrossRef][PubMed]
    [Google Scholar]
  38. Ye J, Tian X, Xie Q, Zhang Y, Sheng Y et al. Avian Gyrovirus 2 DNA in fowl from live poultry markets and in healthy humans, China. Emerg Infect Dis 2015;21:1486–1488 [CrossRef][PubMed]
    [Google Scholar]
  39. Delwart E, Li L. Rapidly expanding genetic diversity and host range of the Circoviridae viral family and other Rep encoding small circular ssDNA genomes. Virus Res 2012;164:114–121 [CrossRef][PubMed]
    [Google Scholar]
  40. Rosario K, Duffy S, Breitbart M. A field guide to eukaryotic circular single-stranded DNA viruses: insights gained from metagenomics. Arch Virol 2012;157:1851–1871 [CrossRef][PubMed]
    [Google Scholar]
  41. Blinkova O, Victoria J, Li Y, Keele BF, Sanz C et al. Novel circular DNA viruses in stool samples of wild-living chimpanzees. J Gen Virol 2010;91:74–86 [CrossRef][PubMed]
    [Google Scholar]
  42. Phan TG, Kapusinszky B, Wang C, Rose RK, Lipton HL et al. The fecal viral flora of wild rodents. PLoS Pathog 2011;7:e1002218 [CrossRef][PubMed]
    [Google Scholar]
  43. Ge X, Li J, Peng C, Wu L, Yang X et al. Genetic diversity of novel circular ssDNA viruses in bats in China. J Gen Virol 2011;92:2646–2653 [CrossRef][PubMed]
    [Google Scholar]
  44. Lima FE, Cibulski SP, Dos Santos HF, Teixeira TF, Varela AP et al. Genomic characterization of novel circular ssDNA viruses from insectivorous bats in Southern Brazil. PLoS One 2015;10:e0118070 [CrossRef][PubMed]
    [Google Scholar]
  45. Kim HK, Park SJ, Nguyen VG, Song DS, Moon HJ et al. Identification of a novel single-stranded, circular DNA virus from bovine stool. J Gen Virol 2012;93:635–639 [CrossRef][PubMed]
    [Google Scholar]
  46. Woo PC, Lau SK, Teng JL, Tsang AK, Joseph M et al. Metagenomic analysis of viromes of dromedary camel fecal samples reveals large number and high diversity of circoviruses and picobirnaviruses. Virology 2014;471–473:117–125 [CrossRef][PubMed]
    [Google Scholar]
  47. Phan TG, da Costa AC, Del Valle Mendoza J, Bucardo-Rivera F, Nordgren J et al. The fecal virome of South and Central American children with diarrhea includes small circular DNA viral genomes of unknown origin. Arch Virol 2016;161:959–966 [CrossRef][PubMed]
    [Google Scholar]
  48. Ng TF, Chen LF, Zhou Y, Shapiro B, Stiller M et al. Preservation of viral genomes in 700-y-old caribou feces from a subarctic ice patch. Proc Natl Acad Sci USA 2014;111:16842–16847 [CrossRef][PubMed]
    [Google Scholar]
  49. Ng TF, Zhang W, Sachsenröder J, Kondov NO, Da Costa AC et al. A diverse group of small circular ssDNA viral genomes in human and non-human primate stools. Virus Evol 2015;1:vev017 [CrossRef][PubMed]
    [Google Scholar]
  50. Reuter G, Boros Á, Delwart E, Pankovics P. Novel circular single-stranded DNA virus from turkey faeces. Arch Virol 2014;159:2161–2164 [CrossRef][PubMed]
    [Google Scholar]
  51. Krupovic M, Ghabrial SA, Jiang D, Varsani A. Genomoviridae: a new family of widespread single-stranded DNA viruses. Arch Virol 2016;161:2633–2643 [CrossRef][PubMed]
    [Google Scholar]
  52. Yu X, Li B, Fu Y, Jiang D, Ghabrial SA et al. A geminivirus-related DNA mycovirus that confers hypovirulence to a plant pathogenic fungus. Proc Natl Acad Sci USA 2010;107:8387–8392 [CrossRef][PubMed]
    [Google Scholar]
  53. Kraberger S, Argüello-Astorga GR, Greenfield LG, Galilee C, Law D et al. Characterisation of a diverse range of circular replication-associated protein encoding DNA viruses recovered from a sewage treatment oxidation pond. Infect Genet Evol 2015;31:73–86 [CrossRef][PubMed]
    [Google Scholar]
  54. Phan TG, Mori D, Deng X, Rajindrajith S, Ranawaka U et al. Small circular single stranded DNA viral genomes in unexplained cases of human encephalitis, diarrhea, and in untreated sewage. Virology 2015;482:98–104 [CrossRef][PubMed]
    [Google Scholar]
  55. Zhou C, Zhang S, Gong Q, Hao A. A novel gemycircularvirus in an unexplained case of child encephalitis. Virol J 2015;12:197 [CrossRef][PubMed]
    [Google Scholar]
  56. Cheung AK, Ng TF, Lager KM, Bayles DO, Alt DP et al. A divergent clade of circular single-stranded DNA viruses from pig feces. Arch Virol 2013;158:2157–2162 [CrossRef][PubMed]
    [Google Scholar]
  57. Cheung AK, Ng TF, Lager KM, Alt DP, Delwart EL et al. Identification of a novel single-stranded circular DNA virus in pig feces. Genome Announc 2014;2:e00347-14 [CrossRef][PubMed]
    [Google Scholar]
  58. Li L, Kapoor A, Slikas B, Bamidele OS, Wang C et al. Multiple diverse circoviruses infect farm animals and are commonly found in human and chimpanzee feces. J Virol 2010;84:1674–1682 [CrossRef][PubMed]
    [Google Scholar]
  59. Sikorski A, Argüello-Astorga GR, Dayaram A, Dobson RC, Varsani A. Discovery of a novel circular single-stranded DNA virus from porcine faeces. Arch Virol 2013;158:283–289 [CrossRef][PubMed]
    [Google Scholar]
  60. Cotmore SF, Agbandje-Mckenna M, Chiorini JA, Mukha DV, Pintel DJ et al. The family Parvoviridae. Arch Virol 2014;159:1239–1247 [CrossRef][PubMed]
    [Google Scholar]
  61. Koo BS, Lee HR, Jeon EO, Han MS, Min KC et al. Genetic characterization of three novel chicken parvovirus strains based on analysis of their coding sequences. Avian Pathol 2015;44:28–34 [CrossRef]
    [Google Scholar]
  62. Finkler F, De Lima DA, Cerva C, Cibulski SP, Teixeira TF et al. Chicken parvovirus viral loads in cloacal swabs from malabsorption syndrome-affected and healthy broilers. Trop Anim Health Prod 2016;48:1685–1689 [CrossRef][PubMed]
    [Google Scholar]
  63. Tan M, Wei C, Huang P, Fan Q, Quigley C et al. Tulane virus recognizes sialic acids as cellular receptors. Sci Rep 2015;5:11784 [CrossRef][PubMed]
    [Google Scholar]
  64. Clarke IN, Estes MK, Green KY, Hansman GS, Knowles NJ et al. Caliciviridae. In King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ. (editors) Virus Taxonomy Classification and Nomenclature of Viruses Ninth Report of the International Committee on Taxonomy of Viruses, 9th ed. San Diego: Academic Press; 2012; p.1272
    [Google Scholar]
  65. Wolf S, Reetz J, Hoffmann K, Gründel A, Schwarz BA et al. Discovery and genetic characterization of novel caliciviruses in German and Dutch poultry. Arch Virol 2012;157:1499–1507 [CrossRef][PubMed]
    [Google Scholar]
  66. L'Homme Y, Sansregret R, Plante-Fortier E, Lamontagne AM, Ouardani M et al. Genomic characterization of swine caliciviruses representing a new genus of Caliciviridae. Virus Genes 2009;39:66–75 [CrossRef][PubMed]
    [Google Scholar]
  67. Glass PJ, White LJ, Ball JM, Leparc-Goffart I, Hardy ME et al. Norwalk virus open reading frame 3 encodes a minor structural protein. J Virol 2000;74:6581–6591 [CrossRef][PubMed]
    [Google Scholar]
  68. Sosnovtsev SV, Green KY. Identification and genomic mapping of the ORF3 and VPg proteins in feline calicivirus virions. Virology 2000;277:193–203 [CrossRef][PubMed]
    [Google Scholar]
  69. Wolf S, Reetz J, Otto P. Genetic characterization of a novel calicivirus from a chicken. Arch Virol 2011;156:1143–1150 [CrossRef][PubMed]
    [Google Scholar]
  70. Ganesh B, Masachessi G, Mladenova Z. Animal Picobirnavirus. VirusDisease 2014;25:223–238 [CrossRef][PubMed]
    [Google Scholar]
  71. Bányai K, Potgieter C, Gellért Á, Ganesh B, Tempesta M et al. Genome sequencing identifies genetic and antigenic divergence of porcine picobirnaviruses. J Gen Virol 2014;95:2233–2239 [CrossRef][PubMed]
    [Google Scholar]
  72. Ribeiro Silva R, Bezerra DA, Kaiano JH, Oliveira DS, Silvestre RV et al. Genogroup I avian picobirnavirus detected in Brazilian broiler chickens: a molecular epidemiology study. J Gen Virol 2014;95:117–122 [CrossRef][PubMed]
    [Google Scholar]
  73. Adams MJ, Lefkowitz EJ, King AM, Bamford DH, Breitbart M et al. Ratification vote on taxonomic proposals to the international committee on taxonomy of viruses (2015). Arch Virol 2015;160:1837–1850 [CrossRef][PubMed]
    [Google Scholar]
  74. Boros Á, Pankovics P, Adonyi Á, Fenyvesi H, Day JM et al. A diarrheic chicken simultaneously co-infected with multiple picornaviruses: complete genome analysis of avian picornaviruses representing up to six genera. Virology 2016;489:63–74 [CrossRef][PubMed]
    [Google Scholar]
  75. Lau SK, Woo PC, Yip CC, Li KS, Fan RY et al. Chickens host diverse picornaviruses originated from potential interspecies transmission with recombination. J Gen Virol 2014;95:1929–1944 [CrossRef][PubMed]
    [Google Scholar]
  76. Bullman S, Kearney K, O'Mahony M, Kelly L, Whyte P et al. Identification and genetic characterization of a novel picornavirus from chickens. J Gen Virol 2014;95:1094–1103 [CrossRef][PubMed]
    [Google Scholar]
  77. Kim HR, Yoon SJ, Lee HS, Kwon YK. Identification of a picornavirus from chickens with transmissible viral proventriculitis using metagenomic analysis. Arch Virol 2015;160:701–709 [CrossRef][PubMed]
    [Google Scholar]
  78. Boros Á, Pankovics P, Knowles NJ, Nemes C, Delwart E et al. Comparative complete genome analysis of chicken and turkey megriviruses (family Picornaviridae): long 3′ untranslated regions with a potential second open reading frame and evidence for possible recombination. J Virol 2014;88:6434–6443 [CrossRef][PubMed]
    [Google Scholar]
  79. Otto P, Liebler-Tenorio EM, Elschner M, Reetz J, Löhren U et al. Detection of rotaviruses and intestinal lesions in broiler chicks from flocks with runting and stunting syndrome (RSS). Avian Dis 2006;50:411–418 [CrossRef][PubMed]
    [Google Scholar]
  80. Ito H, Sugiyama M, Masubuchi K, Mori Y, Minamoto N. Complete nucleotide sequence of a group A avian rotavirus genome and a comparison with its counterparts of mammalian rotaviruses. Virus Res 2001;75:123–138 [CrossRef][PubMed]
    [Google Scholar]
  81. Matthijnssens J, Otto PH, Ciarlet M, Desselberger U, Van Ranst M et al. VP6-sequence-based cutoff values as a criterion for rotavirus species demarcation. Arch Virol 2012;157:1177–1182 [CrossRef][PubMed]
    [Google Scholar]
  82. Trojnar E, Otto P, Johne R. The first complete genome sequence of a chicken group A rotavirus indicates independent evolution of mammalian and avian strains. Virology 2009;386:325–333 [CrossRef][PubMed]
    [Google Scholar]
  83. Kindler E, Trojnar E, Heckel G, Otto PH, Johne R. Analysis of rotavirus species diversity and evolution including the newly determined full-length genome sequences of rotavirus F and G. Infect Genet Evol 2013;14:58–67 [CrossRef][PubMed]
    [Google Scholar]
  84. Nakagomi O, Nakagomi T. Genomic relationships among rotaviruses recovered from various animal species as revealed by RNA–RNA hybridization assays. Res Vet Sci 2002;73:207–214 [CrossRef][PubMed]
    [Google Scholar]
  85. Johne R, Reetz J, Kaufer BB, Trojnar E. Generation of an avian-mammalian rotavirus reassortant by using a helper virus-dependent reverse genetics system. J Virol 2015;90:1439–1443 [CrossRef][PubMed]
    [Google Scholar]
  86. Sambrook J, Russel DW. Molecular Cloning: A Laboratory Manual, 3rd ed. USA: Cold Spring Harbor; 2001
    [Google Scholar]
  87. Dean FB, Hosono S, Fang L, Wu X, Faruqi AF et al. Comprehensive human genome amplification using multiple displacement amplification. Proc Natl Acad Sci USA 2002;99:5261–5266 [CrossRef][PubMed]
    [Google Scholar]
  88. Nakamura S, Yang CS, Sakon N, Ueda M, Tougan T et al. Direct metagenomic detection of viral pathogens in nasal and fecal specimens using an unbiased high-throughput sequencing approach. PLoS One 2009;4:e4219 [CrossRef][PubMed]
    [Google Scholar]
  89. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012;19:455–477 [CrossRef][PubMed]
    [Google Scholar]
  90. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 1997;25:4876–4882 [CrossRef][PubMed]
    [Google Scholar]
  91. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013;30:2725–2729 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000711
Loading
/content/journal/jgv/10.1099/jgv.0.000711
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most cited articles

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