1887

Abstract

Ranaviruses have been implicated in recent declines in global amphibian populations. Compared with the family , to which the genus belongs, ranaviruses have a wide host range in that species/strains are known to infect fish, amphibians and reptiles, presumably due to recent host-switching events. We used eight sequenced ranavirus genomes and two selection-detection methods (site based and branch based) to identify genes that exhibited signatures of positive selection, potentially due to the selective pressures at play during host switching. We found evidence of positive selection acting on four genes via the site-based method, three of which were newly acquired genes unique to ranavirus genomes. Using the branch-based method, we identified eight additional candidate genes that exhibited signatures of / (non-synonymous/synonymous substitution rate) >1 in the clade where intense host switching had occurred. We found that these branch-specific patterns of elevated / were enriched in a small group of viral genes that have been acquired most recently in the ranavirus genome, compared with core genes that are shared among all members of the family . Our results suggest that the group of newly acquired genes in the ranavirus genome may have undergone recent adaptive changes that have facilitated interspecies and interclass host switching.

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2013-09-01
2019-12-08
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References

  1. Anisimova M., Bielawski J. P., Yang Z.. ( 2001; ). Accuracy and power of the likelihood ratio test in detecting adaptive molecular evolution. . Mol Biol Evol 18:, 1585–1592. [CrossRef] [PubMed]
    [Google Scholar]
  2. Bandín I., Dopazo C.. ( 2011; ). Host range, host specificity and hypothesized host shift events among viruses of lower vertebrates. . Vet Res 42:, 67. [CrossRef] [PubMed]
    [Google Scholar]
  3. Bayley A. E., Hill B. J., Feist S. W.. ( 2013; ). Susceptibility of the European common frog Rana temporaria to a panel of ranavirus isolates from fish and amphibian hosts. . Dis Aquat Organ 103:, 171–183. [CrossRef] [PubMed]
    [Google Scholar]
  4. Bhatt S., Lam T. T., Lycett S. J., Leigh Brown A. J., Bowden T. A., Holmes E. C., Guan Y., Wood J. L., Brown I. H.. & other authors ( 2013; ). The evolutionary dynamics of influenza A virus adaptation to mammalian hosts. . Philos Trans R Soc Lond B Biol Sci 368:, 20120382. [CrossRef] [PubMed]
    [Google Scholar]
  5. Chen G., Ward B. M., Yu K. H., Chinchar V. G., Robert J.. ( 2011; ). Improved knockout methodology reveals that frog virus 3 mutants lacking either the 18K immediate-early gene or the truncated vIF-2α gene are defective for replication and growth in vivo. . J Virol 85:, 11131–11138. [CrossRef] [PubMed]
    [Google Scholar]
  6. Chinchar V. G.. ( 2002; ). Ranaviruses (family Iridoviridae): emerging cold-blooded killers. . Arch Virol 147:, 447–470. [CrossRef] [PubMed]
    [Google Scholar]
  7. Chinchar V. G., Hyatt A., Miyazaki T., Williams T.. ( 2009; ). Family Iridoviridae: poor viral relations no longer. . Curr Top Microbiol Immunol 328:, 123–170. [CrossRef] [PubMed]
    [Google Scholar]
  8. Choe H., Jemielity S., Abraham J., Radoshitzky S. R., Farzan M.. ( 2011; ). Transferrin receptor 1 in the zoonosis and pathogenesis of New World hemorrhagic fever arenaviruses. . Curr Opin Microbiol 14:, 476–482. [CrossRef] [PubMed]
    [Google Scholar]
  9. Collins J., Storfer A.. ( 2003; ). Global amphibian declines: sorting the hypotheses. . Divers Distrib 9:, 89–98. [CrossRef]
    [Google Scholar]
  10. Daszak P., Berger L., Cunningham A. A., Hyatt A. D., Green D. E., Speare R.. ( 1999; ). Emerging infectious diseases and amphibian population declines. . Emerg Infect Dis 5:, 735–748. [CrossRef] [PubMed]
    [Google Scholar]
  11. Delport W., Poon A. F., Frost S. D., Kosakovsky Pond S. L.. ( 2010; ). Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. . Bioinformatics 26:, 2455–2457. [CrossRef] [PubMed]
    [Google Scholar]
  12. Demogines A., Farzan M., Sawyer S. L.. ( 2012a; ). Evidence for ACE2-utilizing coronaviruses (CoVs) related to severe acute respiratory syndrome CoV in bats. . J Virol 86:, 6350–6353. [CrossRef] [PubMed]
    [Google Scholar]
  13. Demogines A., Truong K. A., Sawyer S. L.. ( 2012b; ). Species-specific features of DARC, the primate receptor for Plasmodium vivax and Plasmodium knowlesi . . Mol Biol Evol 29:, 445–449. [CrossRef] [PubMed]
    [Google Scholar]
  14. Demogines A., Abraham J., Choe H., Farzan M., Sawyer S. L.. ( 2013; ). Dual host-virus arms races shape an essential housekeeping protein. . PLoS Biol 11:, e1001571. [CrossRef] [PubMed]
    [Google Scholar]
  15. Do J. W., Moon C. H., Kim H. J., Ko M. S., Kim S. B., Son J. H., Kim J. S., An E. J., Kim M. K.. & other authors ( 2004; ). Complete genomic DNA sequence of rock bream iridovirus. . Virology 325:, 351–363. [CrossRef] [PubMed]
    [Google Scholar]
  16. Eaton H., Metcalf J., Penny E., Tcherepanove V., Upton C., Brunetti C. R.. ( 2007; ). Comparative genomic analysis of the family Iridoviridae: re-annotating and defining the core set of iridovirus genes. . Virol J 4:, 11–17. [CrossRef] [PubMed]
    [Google Scholar]
  17. Elde N. C., Child S. J., Eickbush M. T., Kitzman J. O., Rogers K. S., Shendure J., Geballe A. P., Malik H. S.. ( 2012; ). Poxviruses deploy genomic accordions to adapt rapidly against host antiviral defenses. . Cell 150:, 831–841. [CrossRef] [PubMed]
    [Google Scholar]
  18. Endo T., Ikeo K., Gojobori T.. ( 1996; ). Large-scale search for genes on which positive selection may operate. . Mol Biol Evol 13:, 685–690. [CrossRef] [PubMed]
    [Google Scholar]
  19. Gifford R. J.. ( 2011; ). Viral evolution in deep time: lentiviruses and mammals. . Trends Genet 28:, 89–100. [CrossRef] [PubMed]
    [Google Scholar]
  20. Goldman N., Yang Z.. ( 1994; ). A codon-based model of nucleotide substitution for protein-coding DNA sequences. . Mol Biol Evol 11:, 725–736.[PubMed]
    [Google Scholar]
  21. Grayfer L., Andino F. J., Chen G., Chinchar G. V., Robert J.. ( 2012; ). Immune evasion strategies of ranaviruses and innate immune responses to these emerging pathogens. . Viruses 4:, 1075–1092. [CrossRef] [PubMed]
    [Google Scholar]
  22. Harrison R. L., Bonning B. C.. ( 2004; ). Application of maximum-likelihood models to selection pressure analysis of group I nucleopolyhedrovirus genes. . J Gen Virol 85:, 197–210. [CrossRef] [PubMed]
    [Google Scholar]
  23. He J. G., Deng M., Weng S. P., Li Z., Zhou S. Y., Long Q. X., Wang X. Z., Chan S. M.. ( 2001; ). Complete genome analysis of the mandarin fish infectious spleen and kidney necrosis iridovirus. . Virology 291:, 126–139. [CrossRef] [PubMed]
    [Google Scholar]
  24. He J. G., L., Deng M., He H. H., Weng S. P., Wang X. H., Zhou S. Y., Long Q. X., Wang X. Z., Chan S. M.. ( 2002; ). Sequence analysis of the complete genome of an iridovirus isolated from the tiger frog. . Virology 292:, 185–197. [CrossRef] [PubMed]
    [Google Scholar]
  25. Herfst S., Schrauwen E. J., Linster M., Chutinimitkul S., de Wit E., Munster V. J., Sorrell E. M., Bestebroer T. M., Burke D. F.. & other authors ( 2012; ). Airborne transmission of influenza A/H5N1 virus between ferrets. . Science 336:, 1534–1541. [CrossRef] [PubMed]
    [Google Scholar]
  26. Hoelzer K., Shackelton L. A., Parrish C. R., Holmes E. C.. ( 2008; ). Phylogenetic analysis reveals the emergence, evolution and dispersal of carnivore parvoviruses. . J Gen Virol 89:, 2280–2289. [CrossRef] [PubMed]
    [Google Scholar]
  27. Huang Y., Huang X., Liu H., Gong J., Ouyang Z., Cui H., Cao J., Zhao Y., Wang X.. & other authors ( 2009; ). Complete sequence determination of a novel reptile iridovirus isolated from soft-shelled turtle and evolutionary analysis of Iridoviridae . . BMC Genomics 10:, 224. [CrossRef] [PubMed]
    [Google Scholar]
  28. Jancovich J. K., Mao J., Chinchar V. G., Wyatt C., Case S. T., Kumar S., Valente G., Subramanian S., Davidson E. W.. & other authors ( 2003; ). Genomic sequence of a ranavirus (family Iridoviridae) associated with salamander mortalities in North America. . Virology 316:, 90–103. [CrossRef] [PubMed]
    [Google Scholar]
  29. Jancovich J. K., Davidson E. W., Parameswaran N., Mao J., Chinchar V. G., Collins J. P., Jacobs B. L., Storfer A.. ( 2005; ). Evidence for emergence of an amphibian iridoviral disease because of human-enhanced spread. . Mol Ecol 14:, 213–224. [CrossRef] [PubMed]
    [Google Scholar]
  30. Jancovich J. K., Bremont M., Touchman J. W., Jacobs B. L.. ( 2010; ). Evidence for multiple recent host species shifts among the ranaviruses (family Iridoviridae). . J Virol 84:, 2636–2647. [CrossRef] [PubMed]
    [Google Scholar]
  31. Kaelber J. T., Demogines A., Harbison C. E., Allison A. B., Goodman L. B., Ortega A. N., Sawyer S. L., Parrish C. R.. ( 2012; ). Evolutionary reconstructions of the transferrin receptor of Caniforms supports canine parvovirus being a re-emerged and not a novel pathogen in dogs. . PLoS Pathog 8:, e1002666. [CrossRef] [PubMed]
    [Google Scholar]
  32. Kelley L. A., Sternberg M. J.. ( 2009; ). Protein structure prediction on the Web: a case study using the Phyre server. . Nat Protoc 4:, 363–371. [CrossRef] [PubMed]
    [Google Scholar]
  33. Kosakovsky Pond S. L., Posada D., Gravenor M. B., Woelk C. H., Frost S. D.. ( 2006; ). gard: a genetic algorithm for recombination detection. . Bioinformatics 22:, 3096–3098. [CrossRef] [PubMed]
    [Google Scholar]
  34. Kosiol C., Vinar T., da Fonseca R. R., Hubisz M. J., Bustamante C. D., Nielsen R., Siepel A.. ( 2008; ). Patterns of positive selection in six mammalian genomes. . PLoS Genet 4:, e1000144. [CrossRef] [PubMed]
    [Google Scholar]
  35. Larkin M. A., Blackshields G., Brown N. P., Chenna R., McGettigan P. A., McWilliam H., Valentin F., Wallace I. M., Wilm A.. & other authors ( 2007; ). Clustal W and Clustal X version 2.0. . Bioinformatics 23:, 2947–2948. [CrossRef] [PubMed]
    [Google Scholar]
  36. Lei X. Y., Ou T., Zhu R. L., Zhang Q. Y.. ( 2012; ). Sequencing and analysis of the complete genome of Rana grylio virus (RGV). . Arch Virol 157:, 1559–1564. [CrossRef] [PubMed]
    [Google Scholar]
  37. Lesbarrères D., Balseiro A., Brunner J., Chinchar V. G., Duffus A., Kerby J., Miller D. L., Robert J., Schock D. M.. & other authors ( 2012; ). Ranavirus: past, present and future. . Biol Lett 8:, 481–483. [CrossRef] [PubMed]
    [Google Scholar]
  38. L., Zhou S. Y., Chen C., Weng S. P., Chan S. M., He J. G.. ( 2005; ). Complete genome sequence analysis of an iridovirus isolated from the orange-spotted grouper, Epinephelus coioides . . Virology 339:, 81–100. [CrossRef] [PubMed]
    [Google Scholar]
  39. Mao J., Green D. E., Fellers G., Chinchar V. G.. ( 1999; ). Molecular characterization of iridoviruses isolated from sympatric amphibians and fish. . Virus Res 63:, 45–52. [CrossRef] [PubMed]
    [Google Scholar]
  40. Mavian C., López-Bueno A., Balseiro A., Casais R., Alcamí A., Alejo A.. ( 2012a; ). The genome sequence of the emerging common midwife toad virus identifies an evolutionary intermediate within ranaviruses. . J Virol 86:, 3617–3625. [CrossRef] [PubMed]
    [Google Scholar]
  41. Mavian C., López-Bueno A., Fernández Somalo M. P., Alcamí A., Alejo A.. ( 2012b; ). Complete genome sequence of the European sheatfish virus. . J Virol 86:, 6365–6366. [CrossRef] [PubMed]
    [Google Scholar]
  42. McLysaght A., Baldi P. F., Gaut B. S.. ( 2003; ). Extensive gene gain associated with adaptive evolution of poxviruses. . Proc Natl Acad Sci U S A 100:, 15655–15660. [CrossRef] [PubMed]
    [Google Scholar]
  43. Meyerson N., Sawyer S.. ( 2011; ). Two-stepping through time: mammals and viruses. . Trends Microbiol 9:, 286–294. [CrossRef] [PubMed]
    [Google Scholar]
  44. Miller D., Gray M., Storfer A.. ( 2011; ). Ecopathology of ranaviruses infecting amphibians. . Viruses 3:, 2351–2373. [CrossRef] [PubMed]
    [Google Scholar]
  45. Nielsen R., Yang Z.. ( 1998; ). Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. . Genetics 148:, 929–936.[PubMed]
    [Google Scholar]
  46. Nilsson J., Grahn M., Wright A. P.. ( 2011; ). Proteome-wide evidence for enhanced positive Darwinian selection within intrinsically disordered regions in proteins. . Genome Biol 12:, R65. [CrossRef] [PubMed]
    [Google Scholar]
  47. Parrish C. R., Holmes E. C., Morens D. M., Park E. C., Burke D. S., Calisher C. H., Laughlin C. A., Saif L. J., Daszak P.. ( 2008; ). Cross-species virus transmission and the emergence of new epidemic diseases. . Microbiol Mol Biol Rev 72:, 457–470. [CrossRef] [PubMed]
    [Google Scholar]
  48. Picco A. M., Collins J. P.. ( 2008; ). Amphibian commerce as a likely source of pathogen pollution. . Conserv Biol 22:, 1582–1589. [CrossRef] [PubMed]
    [Google Scholar]
  49. Rachowicz L., Hero J., Alford R., Taylor J., Morgan J., Vredenburg V., Collins J., Briggs C.. ( 2005; ). The novel and endemic pathogen hypotheses: competing explanations for the origin of emerging infectious diseases of wildlife. . Conserv Biol 19:, 1441–1448. [CrossRef]
    [Google Scholar]
  50. Ridenhour B., Storfer A.. ( 2008; ). Geographically variable selection in Ambystoma tigrinum virus (Iridoviridae) throughout the western USA . . J Evolution Biol 21:, 1151–1159. [CrossRef]
    [Google Scholar]
  51. Sabeti P. C., Schaffner S. F., Fry B., Lohmueller J., Varilly P., Shamovsky O., Palma A., Mikkelsen T. S., Altshuler D., Lander E. S.. ( 2006; ). Positive natural selection in the human lineage. . Science 312:, 1614–1620. [CrossRef] [PubMed]
    [Google Scholar]
  52. Sawyer S. L., Elde N. C.. ( 2012; ). A cross-species view on viruses. . Curr Opin Virol 2:, 561–568. [CrossRef] [PubMed]
    [Google Scholar]
  53. Shackelton L. A., Parrish C. R., Truyen U., Holmes E. C.. ( 2005; ). High rate of viral evolution associated with the emergence of carnivore parvovirus. . Proc Natl Acad Sci U S A 102:, 379–384. [CrossRef] [PubMed]
    [Google Scholar]
  54. Slobedman B., Barry P. A., Spencer J. V., Avdic S., Abendroth A.. ( 2009; ). Virus-encoded homologs of cellular interleukin-10 and their control of host immune function. . J Virol 83:, 9618–9629. [CrossRef] [PubMed]
    [Google Scholar]
  55. Song W. J., Qin Q. W., Qiu J., Huang C. H., Wang F., Hew C. L.. ( 2004; ). Functional genomics analysis of Singapore grouper iridovirus: complete sequence determination and proteomic analysis. . J Virol 78:, 12576–12590. [CrossRef] [PubMed]
    [Google Scholar]
  56. Stamatakis A.. ( 2006; ). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. . Bioinformatics 22:, 2688–2690. [CrossRef] [PubMed]
    [Google Scholar]
  57. Stuart S. N., Chanson J. S., Cox N. A., Young B. E., Rodrigues A. S., Fischman D. L., Waller R. W.. ( 2004; ). Status and trends of amphibian declines and extinctions worldwide. . Science 306:, 1783–1786. [CrossRef] [PubMed]
    [Google Scholar]
  58. Tan W. G., Barkman T. J., Gregory Chinchar V., Essani K.. ( 2004; ). Comparative genomic analyses of frog virus 3, type species of the genus Ranavirus (family Iridoviridae). . Virology 323:, 70–84. [CrossRef] [PubMed]
    [Google Scholar]
  59. Tidona C. A., Darai G.. ( 1997; ). The complete DNA sequence of lymphocystis disease virus. . Virology 230:, 207–216. [CrossRef] [PubMed]
    [Google Scholar]
  60. Tidona C., Darai G.. ( 2000; ). Iridovirus homologues of cellular genes: implications for the molecular evolution of large DNA viruses. . Virus Genes 21:, 77–81. [CrossRef] [PubMed]
    [Google Scholar]
  61. Tsai C. T., Ting J. W., Wu M. H., Wu M. F., Guo I. C., Chang C. Y.. ( 2005; ). Complete genome sequence of the grouper iridovirus and comparison of genomic organization with those of other iridoviruses. . J Virol 79:, 2010–2023. [CrossRef] [PubMed]
    [Google Scholar]
  62. Wain L. V., Bailes E., Bibollet-Ruche F., Decker J. M., Keele B. F., Van Heuverswyn F., Li Y., Takehisa J., Ngole E. M.. & other authors ( 2007; ). Adaptation of HIV-1 to its human host. . Mol Biol Evol 24:, 1853–1860. [CrossRef] [PubMed]
    [Google Scholar]
  63. Williams T., Barbosa-Solomieu V., Chinchar V. G.. ( 2005; ). A decade of advances in iridovirus research. . Adv Virus Res 65:, 173–248. [CrossRef] [PubMed]
    [Google Scholar]
  64. Yang Z.. ( 1998; ). Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. . Mol Biol Evol 15:, 568–573. [CrossRef] [PubMed]
    [Google Scholar]
  65. Yang Z.. ( 2007; ). paml 4: phylogenetic analysis by maximum likelihood. . Mol Biol Evol 24:, 1586–1591. [CrossRef] [PubMed]
    [Google Scholar]
  66. Yang Z., Swanson W. J., Vacquier V. D.. ( 2000; ). Maximum-likelihood analysis of molecular adaptation in abalone sperm lysin reveals variable selective pressures among lineages and sites. . Mol Biol Evol 17:, 1446–1455. [CrossRef] [PubMed]
    [Google Scholar]
  67. Zhang Q. Y., Xiao F., Xie J., Li Z. Q., Gui J. F.. ( 2004; ). Complete genome sequence of lymphocystis disease virus isolated from China. . J Virol 78:, 6982–6994. [CrossRef] [PubMed]
    [Google Scholar]
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