Advertisement

Molecular Biology of RNA Viruses Isolated in Antarctica

  • Juan CristinaEmail author
Chapter
Part of the Springer Polar Sciences book series (SPPS)

Abstract

RNA viruses exist as collections of closely related viral genomes, termed quasispecies, subjected to a continuous process of genetic variation, competition among the variants generated, and selection of the most fitted distributions in a given environment. Large population sizes and high evolutionary rates make RNA viruses unique. Detailed studies on the molecular biology and evolution of RNA viruses are extremely important for our understanding of the role of these viruses in Antarctica, as well as to gain insight into their emergence and spread. Antarctic ecosystems are dominated by microorganisms, where RNA viruses play an important role as an active, persistent, and important component of the aquatic microbial community, both at Antarctic sea and freshwater environments. RNA virus infection of Antarctic wildlife is more significant than previously anticipated, where at least members of five different RNA virus families have been identified. RNA plant viruses have been also observed. Recent studies reveal the introduction, persistence, and evolution of emerging RNA viruses of extreme importance for human and/or animal health in Antarctica. To determine the role of Antarctica in the global emergence of these viruses is extremely important for the development of appropriate strategies to control infection caused by these viruses.

Keywords

RNA viruses Emergence and spread of virus Paramyxoviridae Orthomyxoviridae Birnaviridae Flaviviridae Togaviridae 

Notes

Acknowledgments

JC acknowledge the support from Comisión Sectorial de Investigación Cientifica (CSIC), through CSIC Grupos program, and PEDECIBA, Universidad de la República. I also acknowledge the support from Agencia Nacional de Investigación e Innovación (ANII) and Sistema Nacional de Investigadores, Uruguay.

References

  1. Adams, M. J., Adkins, S., Bragard, C., Gilmer, D., & Li, D. (2017). ICTV virus taxonomy profile: Virgaviridae. The Journal of General Virology, 98, 1999–2000.PubMedPubMedCentralCrossRefGoogle Scholar
  2. Adriaenssens, E. M., Kramer, R., Van Goethem, M. W., Makhalanyane, T. P., Hogg, I., & Cowan, D. A. (2017). Environmental drivers of viral community composition in Antarctic soils identified by viromics. Microbiome, 5, e83.CrossRefGoogle Scholar
  3. Aguirre de Cárcer, D., López-Bueno, A., Alonso-Lobo, J. M., Quesada, A., et al. (2016). Metagenomic analysis of lacustrine viral diversity along a latitudinal transect of the Antarctic Peninsula. FEMS Microbiology Ecology, 92, fiw074.  https://doi.org/10.1093/femsec/fiw074.CrossRefPubMedGoogle Scholar
  4. Alexander, D. J., Manvell, R. J., Collins, M. S., Brockman, S. J., Westbury, H. A., et al. (1989). Characterization of paramyxoviruses isolated from penguins in Antarctica and sub-Antarctica during 1976–1979. Archives of Virology, 109, 135–143.PubMedCrossRefGoogle Scholar
  5. Austin, F. J., & Webster, R. G. (1993). Evidence of ortho- and paramyxoviruses in fauna from Antarctica. Journal of Wildlife Diseases, 29, 568–571.PubMedCrossRefPubMedCentralGoogle Scholar
  6. Barbosa, A., & Palacios, M. J. (2009). Health of Antarctic birds: A review of their parasites, pathogens and diseases. Polar Biology, 32, 1095–1115.CrossRefGoogle Scholar
  7. Barriga, G. P., Boric-Bargetto, D., San Martin, M. C., Neira, V., van Bakel, H., et al. (2016). Avian influenza virus H5 strain with North American and Eurasian lineage genes in an Antarctic penguin. Emerging Infectious Diseases, 22, 2221–2223.PubMedPubMedCentralCrossRefGoogle Scholar
  8. Baumeister, E., Leotta, G., Pontoriero, A., Campos, A., Montalti, D., et al. (2004). Serological evidences of influenza A virus infection in Antarctica migratory birds. International Congress Series, 1263, 737–740.CrossRefGoogle Scholar
  9. Bengtson, J. L., Boveng, P., Franzen, U., Have, P., Heide-Jorgensen, M. P., et al. (1991). Antibodies to canine distemper virus in antarctic seals. Marine Mammal Science, 7, 85–87.CrossRefGoogle Scholar
  10. Bevins, S. N., Dusek, R. J., White, C. L., Gidlewski, T., Bodenstein, B., et al. (2016). Widespread detection of highly pathogenic H5 influenza viruses in wild birds from the Pacific flyway of the United States. Scientific Reports, 6, 28980.PubMedPubMedCentralCrossRefGoogle Scholar
  11. Brooke, M. (2004). Albatrosses and petrels across the world. Oxford: Oxford University Press.Google Scholar
  12. Brum, J. R., Hurwitz, B. L., Schofield, O., Ducklow, H. W., & Sullivan, M. B. (2017). Seasonal time bombs: Dominant temperate viruses affect southern ocean microbial dynamics. The ISME Journal, 10, 437–449.CrossRefGoogle Scholar
  13. Cavicchioli, R., & Erdmann, S. (2015). The discovery of Antarctic RNA viruses: A new game changer. Molecular Ecology, 24, 4809–4811.PubMedCrossRefPubMedCentralGoogle Scholar
  14. Collins, P. L., & Melero, J. A. (2011). Progress in understanding and controlling respiratory syncytial virus: Still crazy after all these years. Virus Research, 162, 80–99.PubMedPubMedCentralCrossRefGoogle Scholar
  15. Culley, A. (2018). New insight into the RNA aquatic virosphere via viromics. Virus Research, 244, 84–89.PubMedCrossRefPubMedCentralGoogle Scholar
  16. Delmas, B., Mundt, E., Vakharia, V. N., & Wu, J. L. (2011). Family Birnaviridae. In A. M. Q. King, E. Lefkowitz, M. J. Adams, & E. B. Carstens (Eds.), Virus taxonomy: Ninth report of the international committee on taxonomy of viruses (pp. 496–507). San Diego: Elsevier.Google Scholar
  17. Domingo, E. (2006). Quasispecies: Concept and implications for virology. Heidelberg: Springer.CrossRefGoogle Scholar
  18. Domingo, E., Sabo, D., Taniguchi, T., & Weissmann, C. (1978). Nucleotide sequence heterogeneity of an RNA phage population. Cell, 13, 735–744.PubMedCrossRefPubMedCentralGoogle Scholar
  19. Ducklow, H. W., Baker, K., Martinson, D. G., Quetin, L. B., et al. (2007). Marine pelagic ecosystems: The West Antarctic Peninsula. Philosophical Transactions of the Royal Society B, 362, 67–94.CrossRefGoogle Scholar
  20. Dugan, V. G., Chen, R., Spiro, D. J., Sengamalay, N., Zaborsky, J., et al. (2008). The evolutionary genetics and emergence of avian influenza viruses in wild birds. PLoS Pathogens, 4, e1000076.PubMedPubMedCentralCrossRefGoogle Scholar
  21. Egevang, C., Stenhouse, I. J., Phillips, R. A., Petersen, A., Fox, J. W., et al. (2010). Tracking of Arctic terns Sterna paradisaea reveals longest animal migration. Proceedings of the National Academy of Sciences of the United States of America, 107, 10182–10189.CrossRefGoogle Scholar
  22. Eggers, H. J., & Tamm, I. (1965). Coxsackie A9 virus: Mutation from drug dependence to drug independence. Science, 148, 97–98.PubMedCrossRefPubMedCentralGoogle Scholar
  23. Eigen, M. (1971). Self organization of matter and the evolution of biological macromolecules. Naturwissenschaften, 58, 465–523.PubMedCrossRefPubMedCentralGoogle Scholar
  24. Eigen, M. (1992). Steps towards life: A perspective on evolution. Oxford: Oxford University Press.Google Scholar
  25. Eigen, M., & Schuster, P. (1977). The hypercycle. A principle of natural self-organization. Part A: Emergence of the hypercycle. Naturwissenschaften, 64, 541–565.PubMedCrossRefPubMedCentralGoogle Scholar
  26. Evans, C., Brandsma, J., Pond, D. W., & Venables, H. J. (2017). Drivers of interannual variability in virioplankton abundance at the coastal western Antarctic peninsula and the potential effects of climate change. Environmental Microbiology, 19, 740–755.PubMedCrossRefPubMedCentralGoogle Scholar
  27. Fajardo, A., Cristina, J., & Moreno, P. (2016). Emergence and spreading potential of Zika virus. Frontiers in Microbiology, 7, 1667.PubMedPubMedCentralCrossRefGoogle Scholar
  28. Foreman, C. M., Dieser, M., Greenwood, M., Cory, R. M., Laybourn-Parry, J., et al. (2010). When a habitat freezes solid: Microorganisms over-winter within the ice column of a coastal Antarctic lake. FEMS Microbiology Ecology, 76, 401–412.CrossRefGoogle Scholar
  29. Forrester, N. L., Palacios, G., Tesh, R. B., Savji, N., Guzman, H., et al. (2012). Genome-scale phylogeny of the alphavirus genus suggests a marine origin. Journal of Virology, 86, 2729–2738.PubMedPubMedCentralCrossRefGoogle Scholar
  30. Gardner, H., Kerry, K., Riddle, M., Brouwer, S., & Gleeson, L. (1997). Poultry virus infection in Antarctic penguins. Nature, 387, 245.PubMedCrossRefGoogle Scholar
  31. Glatz, R. E., Lepp, P. W., Ward, B. B., & Francis, C. A. (2006). Planktonic microbial community composition across steep physical/chemical gradients in permanently ice-covered Lake Bonney, Antarctica. Geobiology, 4, 53–67.CrossRefGoogle Scholar
  32. Gould, A. R., Kattenbelt, J. A., Selleck, P., Hansson, E., Della-Porta, A., et al. (2001). Virulent Newcastle disease in Australia: Molecular epidemiological analysis of viruses isolated prior to and during the outbreaks of 1998–2000. Virus Research, 77, 51–60.PubMedCrossRefGoogle Scholar
  33. Hill, N. J., Takekawa, J. Y., Cardona, C. J., Meixell, B. W., Ackerman, J. T., et al. (2012). Cross-seasonal patterns of avian influenza virus in breeding and wintering migratory birds: A flyway perspective. Vector Borne and Zoonotic Diseases, 12, 243–253.PubMedPubMedCentralCrossRefGoogle Scholar
  34. Hurt, A. C., Hansbro, P. M., Selleck, P., Olsen, B., Minton, et al. (2006). Isolation of avian influenza viruses from two different transhemispheric migratory shorebird species in Australia. Archives of Virology, 151, 2301–2309.PubMedCrossRefGoogle Scholar
  35. Hurt, A. C., Vijaykrishna, D., Butler, J., Baas, C., Maurer-Stroh, S., et al. (2014). Detection of evolutionarily distinct avian influenza a viruses in Antarctica. MBio, 5(3), e01098–e01040.PubMedPubMedCentralCrossRefGoogle Scholar
  36. Hurt, A. C., Su, Y. C., Aban, M., Peck, H., Lau, H., et al. (2016). Evidence for the introduction, reassortment, and persistence of diverse influenza a viruses in Antarctica. Journal of Virology, 90, 9674–9682.PubMedPubMedCentralCrossRefGoogle Scholar
  37. Junglen, S., Korries, M., Grasse, W., Wieseler, J., & Kopp, A. (2017). Host range restriction of insect-specific flaviviruses occurs at several levels of the viral life cycle. mSphere, 2, e00375–e00316.  https://doi.org/10.1128/mSphere.00375-16.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Kerry, K., Irvine, L., Beggs, A., & Watts, J. (2009). An unusual mortality event among Adélie penguins in the vicinity of Mawson Station, Antarctica. In Health of Antarctic wildlife (pp. 107–112). Berlin: Springer.CrossRefGoogle Scholar
  39. Kim, S. H., & Samal, S. K. (2016). Newcastle disease virus as a vaccine vector for development of human and veterinary vaccines. Viruses, 8, 183.  https://doi.org/10.3390/v8070183.CrossRefPubMedCentralGoogle Scholar
  40. Klema, V. J., Padmanabhan, R., & Choi, K. H. (2015). Flaviviral replication complex: Coordination between RNA synthesis and 5′-RNA capping. Viruses, 7, 4640–4656.PubMedPubMedCentralCrossRefGoogle Scholar
  41. Kopp, M., Peter, H. U., Mustafa, O., Lisovski, S., Ritz, M. S., et al. (2011). South polar skuas from a single breeding population overwinter in different oceans though show similar migration patterns. Marine Ecology Progress Series, 435, 263–267.CrossRefGoogle Scholar
  42. Krauss, S., Walker, D., Pryor, S. P., Niles, L., Chenghong, L., et al. (2004). Influenza A viruses of migrating wild aquatic birds in North America. Vector Borne and Zoonotic Diseases, 4, 177–189.PubMedCrossRefPubMedCentralGoogle Scholar
  43. Krishnamurthy, S. R., & Wang, D. (2017). Origins and challenges of viral dark matter. Virus Research, 239, 136–142.PubMedCrossRefPubMedCentralGoogle Scholar
  44. Krumbholz, A., Groth, M., Esefeld, J., Peter, H. U., & Zell, R. (2017). Genome sequence of a novel Picorna-like RNA virus from feces of the Antarctic fur seal (Arctocephalus gazella). Genome Announcement, 5(36), e01001–e01017.  https://doi.org/10.1128/genomeA.01001-17.CrossRefGoogle Scholar
  45. La Linn, M., Gardner, J., Warrilow, D., Darnell, G. A., McMahon, C. R., et al. (2001). Arbovirus of marine mammals: A new alphavirus isolated from the elephant seal louse, Lepidophthirus macrorhini. Journal of Virology, 75, 4103–4109.PubMedPubMedCentralCrossRefGoogle Scholar
  46. Lamb, R. A., & Kolakofsky, D. (2001). Paramyxoviridae: The viruses and their replication. In B. N. Fields, D. M. Knipe, & P. M. Howley (Eds.), Virology (pp. 1305–1340). Philadelphia: Lippincott Williams and Wilkins.Google Scholar
  47. Lang, A. S., Rise, M. L., Culley, A. I., & Steward, G. F. (2009). RNA viruses in the sea. FEMS Microbiology Reviews, 33, 295–323.PubMedCrossRefPubMedCentralGoogle Scholar
  48. Langstaff, I. G., McKenzie, J. S., Stanislawek, W. L., Reed, C. E., et al. (2009). Surveillance for highly pathogenic avian influenza in migratory shorebirds at the terminus of the East Asian-Australasian flyway. New Zealand Veterinary Journal, 57, 160–165.PubMedCrossRefPubMedCentralGoogle Scholar
  49. Laws, R. M., & Taylor, R. (1957). A mass dying of crabeater seals, Lobodon carcinophagus (gray). Journal of Zoology, 129, 315–324.Google Scholar
  50. López-Bueno, A., Rastrojo, A., Peiró, R., Arenas, M., & Alcamí, A. (2015). Ecological connectivity shapes quasispecies structure of RNA viruses in an Antarctic lake. Molecular Ecology, 24, 4812–4825.PubMedCrossRefPubMedCentralGoogle Scholar
  51. MacDonald, D. M., & Conroy, J. W. H. (1971). Virus disease resembling puffinosis in the gentoo penguin (Pygoscelis papua). British Antarctica Survey Bulletin, 60, 80–83.Google Scholar
  52. Major, L., Linn, M. L., Slade, R. W., Schroder, W. A., Hyatt, A. D., et al. (2009). Ticks associated with Macquarie island penguins carry arboviruses from four genera. PLoS One, 4, e4375.PubMedPubMedCentralCrossRefGoogle Scholar
  53. McFarlane, R. (2009). Health assessment and diseases of the Weddell seal, Leptonochotes Weddelli, in Vestfold Hills, East Antarctica. In Health of Antarctic wildlife (pp. 139–166). Berlin: Springer.CrossRefGoogle Scholar
  54. Miller, G. D., Watts, J. M., & Shellam, G. R. (2008). Viral antibodies in south polar skuas around Davis Station, Antarctica. Antarctic Science, 20, 455–461.CrossRefGoogle Scholar
  55. Miller, P. J., Afonso, C. L., Spackman, E., Scott, M. A., Pedersen, J. C., et al. (2010). Evidence for a new avian paramyxovirus serotype 10 detected in rockhopper penguins from the Falkland Islands. Journal of Virology, 84, 11496–11504.PubMedPubMedCentralCrossRefGoogle Scholar
  56. Miranda, J. A., Culley, A. I., Schvarcz, C. R., & Steward, G. F. (2016). RNA viruses as major contributors to Antarctic virioplankton. Environmental Microbiology, 18, 3714–3727.PubMedCrossRefPubMedCentralGoogle Scholar
  57. Moline, M. A., Claustre, H., Frazer, T. K., Schofield, O., & Vernet, M. (2004). Alteration of the food web along the Antarctic Peninsula in response to a regional warming trend. Global Change Biology, 10, 1973–1980.CrossRefGoogle Scholar
  58. Moratorio, G., Iriarte, A., Moreno, P., Musto, H., & Cristina, J. (2013). A detailed comparative analysis on the overall codon usage patterns in West Nile virus. Infection, Genetics and Evolution, 14, 396–400.PubMedCrossRefPubMedCentralGoogle Scholar
  59. Morgan, I. R., & Westbury, H. A. (1981). Virological studies of Adélie Penguins (Pygoscelis adeliae) in Antarctica. Avian Diseases, 25, 1019–1026.PubMedCrossRefPubMedCentralGoogle Scholar
  60. Morgan, I. R., & Westbury, H. A. (1988). Studies of viruses in penguins in the Vestfold Hills. Hydrobiologia, 165, 263–269.CrossRefGoogle Scholar
  61. Morgan, I. R., Westbury, H. A., Caple, I. W., & Campbell, J. (1981). A survey of virus infection in sub-antarctic penguins on Macquarie Island, Southern Ocean. Australian Veterinary Journal, 57, 333–335.PubMedCrossRefPubMedCentralGoogle Scholar
  62. Munster, V. J., Baas, C., Lexmond, P., Waldenström, J., Wallensten, A., et al. (2007). Spatial, temporal, and species variation in prevalence of influenza A viruses in wild migratory birds. PLoS Pathogens, 3, e61.PubMedPubMedCentralCrossRefGoogle Scholar
  63. Murphy, R. C. (1936). The oceanic birds of South America. New York: Macmillan.Google Scholar
  64. Neira, V., Tapia, R., Verdugo, C., Barriga, G., Mor, S., et al. (2017). Novel avulaviruses in penguins, Antarctica. Emerging Infectious Diseases, 23, 1212–1121.PubMedPubMedCentralCrossRefGoogle Scholar
  65. Neumann, G., Brownlee, G. G., Fodor, E., & Kawaoka, Y. (2004). Orthomyxovirus replication, transcription, and polyadenylation. Current Topics in Microbiology and Immunology, 283, 121–143.PubMedPubMedCentralGoogle Scholar
  66. Olsen, B., Munster, V. J., Wallensten, A., Waldenström, J., Osterhaus, A. D., et al. (2006). Global patterns of influenza A virus in wild birds. Science, 312, 384–388.PubMedCrossRefPubMedCentralGoogle Scholar
  67. Perales C, Lorenzo-Redondo R, López-Galíndez C, Martínez MA, Domingo E (2010) Mutant spectra in virus behavior. Future Virology 5.  https://doi.org/10.2217/fvl.10.61 CrossRefGoogle Scholar
  68. Polischuk, V., Budzanivska, I., Shevchenko, T., & Oliynik, S. (2007). Evidence for plant viruses in the region of Argentina Islands, Antarctica. FEMS Microbiology Ecology, 59, 409–417.PubMedCrossRefPubMedCentralGoogle Scholar
  69. Pomeroy, L. W., Bjørnstad, O. N., & Holmes, E. C. (2008). The evolutionary and epidemiological dynamics of the Paramyxoviridae. Journal of Molecular Evolution, 66, 98–106.PubMedPubMedCentralCrossRefGoogle Scholar
  70. Power, A., Huang, H., Roehrig, J., Strauss, E., & Weaver, S. (2017). Togaviridae. In J. N. Maclachlan, E. J. Dubovi, S. W. Barthold, D. F. Swayne, & J. R. Winton (Eds.), Fenner’s veterinary virology (pp. 511–524). Boston: Academic.Google Scholar
  71. Priscu, J. C., Fritsen, C. H., Adams, E. E., Giovannoni, S. J., Paerl, H. W., et al. (1998). Perennial Antarctic lake ice: An oasis for life in a polar desert. Science, 280, 2095–2098.PubMedCrossRefGoogle Scholar
  72. Ramirez, A., Fajardo, A., Moros, Z., Gerder, M., Caraballo, G., et al. (2010). Evolution of dengue virus type 3 genotype III in Venezuela: Diversification, rates and population dynamics. Virology Journal, 7, 329.PubMedPubMedCentralCrossRefGoogle Scholar
  73. Rastrojo, A., & Alcamí, A. (2018). Viruses in polar lake and soil ecosystems. Advances in Virus Research, 101, 39–54.PubMedCrossRefGoogle Scholar
  74. Sanjuán, R. (2012). From molecular genetics to phylodynamics: Evolutionary relevance of mutation rates across viruses. PLoS Pathogens, 8, e1002685.PubMedPubMedCentralCrossRefGoogle Scholar
  75. Scholthof, K. B., Adkins, S., Czosnek, H., Palukaitis, P., Jacquot, E., et al. (2011). Top 10 plant viruses in molecular plant pathology. Molecular Plant Pathology, 12, 938–954.PubMedCrossRefGoogle Scholar
  76. Selleck, P. W., Arzey, G., Kirkland, P. D., Reece, R. L., Gould, A. R., et al. (2003). An outbreak of highly pathogenic avian influenza in Australia in 1997 caused by an H7N4 virus. Avian Diseases, 47, 806–811.PubMedCrossRefGoogle Scholar
  77. Senne, D. A. (2007). Avian influenza in North and South America, 2002–2005. Avian Diseases, 51, 167–173.PubMedCrossRefGoogle Scholar
  78. Senne, D. A., Panigrahy, B., Kawaoka, Y., Pearson, J. E., Süss, J., et al. (1996). Survey of the hemagglutinin (HA) cleavage site sequence of H5 and H7 avian influenza viruses: Amino acid sequence at the HA cleavage site as a marker of pathogenicity potential. Avian Diseases, 40, 425–437.PubMedCrossRefGoogle Scholar
  79. Shi, M., Lin, X. D., Tian, J. H., Chen, L. J., Chen, X., et al. (2016). Redefining the invertebrate RNA virosphere. Nature, 540, 539–543.CrossRefGoogle Scholar
  80. Siniff, D. B., Garrott, R. A., Rotella, J. J., Fraser, W. R., & Ainley, D. G. (2008). Opinion: Projecting the effects of environmental change on Antarctic seals. Antarctic Science, 20, 425–435.CrossRefGoogle Scholar
  81. Smeele, Z. E., Ainley, D. G., & Varsani, A. (2018). Viruses associated with Antarctic wildlife: From serology based detection to identification of genomes using high throughput sequencing. Virus Research, 243, 91–105.PubMedCrossRefPubMedCentralGoogle Scholar
  82. Soñora, M., Moreno, P., Echeverría, N., Fischer, S., Comas, V., et al. (2015). An evolutionary insight into Newcastle disease viruses isolated in Antarctica. Archives of Virology, 160, 1893–1900.PubMedCrossRefPubMedCentralGoogle Scholar
  83. Stenvers, O., Plötz, J., & Ludwig, H. (1992). Antarctic seals carry antibodies against seal herpesvirus. Archives of Virology, 123, 421–424.PubMedCrossRefPubMedCentralGoogle Scholar
  84. Steward, G. F., Culley, A. I., Mueller, J. A., Wood-Charlson, E. M., et al. (2013). Are we missing half of the viruses in the ocean? The ISME Journal, 7, 672–679.PubMedCrossRefPubMedCentralGoogle Scholar
  85. Taubenberger, J. K., & Kash, J. C. (2010). Influenza virus evolution, host adaptation, and pandemic formation. Cell Host and Microbe, 7, 440–451.PubMedCrossRefPubMedCentralGoogle Scholar
  86. Thomazelli, L. M., Araujo, J., Oliveira, D. B., Sanfilippo, L., Ferreira, C. S., et al. (2010). Newcastle disease virus in penguins from King George Island on the Antarctic region. Veterinary Microbiology, 146, 155–160.PubMedCrossRefPubMedCentralGoogle Scholar
  87. Vignuzzi, M., Stone, J. K., Arnold, J. J., Cameron, C. E., & Andino, R. (2006). Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature, 439, 344–348.PubMedCrossRefPubMedCentralGoogle Scholar
  88. Wallensten, A., Munster, V. J., Osterhaus, A. D., Waldenstr, J., & Bonnedahl, J. (2006). Mounting evidence for the presence of influenza A virus in the avifauna of the Antarctic region. Antarctic Science, 18, 353–356.CrossRefGoogle Scholar
  89. Watts, J. M., Miller, G. D., & Shellam, G. R. (2009). Infectious bursal disease virus and Antarctic birds. In K. R. Kerry & M. Riddle (Eds.), Health of Antarctic wildlife (pp. 95–105). Berlin: Springer Berlin Heidelberg.CrossRefGoogle Scholar
  90. Williams, T. D. (1995). The Penguins: Spheniscidae, 2. Oxford: Oxford University Press.Google Scholar
  91. Wright, P. F., Neumann, G., & Kawaoka, Y. (2007). Orthomyxoviruses. In D. M. Knipe & P. M. Howley (Eds.), Fields virology (Vol. 2, 5th ed., pp. 1691–1740). Philadelphia: Lippincott Williams and Wilkins.Google Scholar
  92. Xiao, S., Paldurai, A., Nayak, B., Mirande, A., Collins, P. L., et al. (2013). Complete genome sequence of a highly virulent Newcastle disease virus currently circulating in Mexico. Genome Announcements.  https://doi.org/10.1128/genomeA.00177-12.
  93. Zhang, X., Yao, T., Ma, X., & Wang, N. (2001). Analysis of the characteristics of microorganisms packed in the ice core of Malan Glacier, Tibet. Science in China Series D, 44, 165–170.Google Scholar
  94. Zhang, X., Jia, R., Shen, H., Wang, M., Yin, Z., et al. (2017). Structures and functions of the envelope glycoprotein in Flavivirus infections. Viruses, 9, E338.  https://doi.org/10.3390/v9110338.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Laboratorio de Virología Molecular, CIN, Facultad de CienciasUniversidad de la RepúblicaMontevideoUruguay

Personalised recommendations