Abstract
Influenza A viruses infect a range of host species, including various mammals and more than 100 species of birds. For avian influenza viruses (AIV), prevalence varies between different groups of birds, with waterfowl showing the highest prevalence. We have sequenced the complete genome of A/Thick-billed Murre/Newfoundland/031/2007(H11N2), an AIV identified in the pelagic seabird, Thick-billed Murre (Uria lomvia). This represents the first complete genome sequence of an AIV from this host species, and only the second complete genome sequence from a seabird in the alcid group. All of the virus segments fall within the American avian lineage. Several of the segments show a close relationship to AIV identified in other marine host species, and also a strong geographic association with other AIV sequences from the northeastern coast of North America from recent years. The identification of this virus, and the growing number of AIV identified in seabird species, indicates these marine birds could be underappreciated host species. This has potential consequences for global influenza dynamics because of the seasonal distributions and migratory patterns of this group of birds.
Similar content being viewed by others
References
P.C. Crawford, E.J. Dubovi, W.L. Castleman, I. Stephenson, E.P.J. Gibbs, L. Chen, C. Smith, R.C. Hill, P. Ferro, J. Pompey, R.A. Bright, M.-J. Medina, I.G. Group, C.M. Johnson, C.W. Olsen, N.J. Cox, A.I. Klimov, J.M. Katz, R.O. Donis, Science 310, 482–485 (2005)
T. Kuiken, G. Rimmelzwaan, D. van Riel, G. van Amerongen, M. Baars, R. Fouchier, A. Osterhaus, Science 306, 241 (2004)
R.G. Webster, W.J. Bean, O.T. Gorman, T.M. Chambers, Y. Kawaoka, Microbiol. Rev. 56, 152–179 (1992)
D.J. Alexander, W.H. Allan, D. Parsons, G. Parsons, Res. Vet. Sci. 24, 242–247 (1978)
D.J. Alexander, G. Parsons, R.J. Manvell, Avian Pathol. 15, 647–662 (1986)
J. Keawcharoen, D. van Riel, G. van Amerongen, T. Bestebroer, W.E. Beyer, R. van Lavieren, A.D.M.E. Osterhaus, R.A.M. Fouchier, T. Kuiken, Emerg. Infect. Dis. 14, 600–607 (2008)
N. Gaidet, G. Cattoli, S. Hammoumi, S.H. Newman, W. Hagemeijer, J.Y. Takekawa, J. Cappelle, T. Dodman, T. Joannis, P. Gil, I. Monne, A. Fusaro, I. Capua, S. Manu, P. Micheloni, U. Ottosson, J.H. Mshelbwala, J. Lubroth, J. Domenech, F. Monicat, PLoS Pathog. 4, e1000127 (2008)
G.M. Jenkins, A. Rambaut, O.G. Pybus, E.C. Holmes, J. Mol. Evol. 54, 156–165 (2002)
W.J. Bean, N.J. Cox, A.P. Kendal, Nature 284, 638–640 (1980)
V.G. Dugan, R. Chen, D.J. Spiro, N. Sengamalay, J. Zaborsky, E. Ghedin, J. Nolting, D.E. Swayne, J.A. Runstadler, G.M. Happ, D.A. Senne, R. Wang, R.D. Slemons, E.C. Holmes, J.K. Taubenberger, PLoS Pathog. 4, e1000076 (2008)
A.V. Koehler, J.M. Pearce, P.L. Flint, J.C. Franson, H.C. Ip, Mol. Ecol. 17, 4754–4762 (2008)
J.C. Obenauer, J. Denson, P.K. Mehta, X. Su, S. Mukatira, D.B. Finkelstein, X. Xu, J. Wang, J. Ma, Y. Fan, K.M. Rakestraw, R.G. Webster, E. Hoffmann, S. Krauss, J. Zheng, Z. Zhang, C.W. Naeve, Science 311, 1576–1580 (2006)
B. Olsen, V.J. Munster, A. Wallensten, J. Waldenstrom, A.D.M.E. Osterhaus, R.A.M. Fouchier, Science 312, 384–388 (2006)
A. Fusaro, I. Monne, G. Cattoli, R. De Nardi, A. Salviato, A. Moreno Martin, I. Capua, C. Terregino, Arch. Virol. 155, 77–81 (2010)
N. Kishida, Y. Sakoda, M. Shiromoto, G.-R. Bai, N. Isoda, A. Takada, G. Laver, H. Kida, Virus Genes 37, 16–21 (2008)
S. Krauss, C.A. Obert, J. Franks, D. Walker, K. Jones, P. Seiler, L. Niles, S.P. Pryor, J.C. Obenauer, C.W. Naeve, L. Widjaja, R.J. Webby, R.G. Webster, PLoS Pathog. 3, e167 (2007)
J.-H. Liu, K. Okazaki, G.-R. Bai, W.-M. Shi, A. Mweene, H. Kida, Virus Genes 29, 81–86 (2004)
A. Wallensten, V.J. Munster, J. Elmberg, A.D.M.E. Osterhaus, R.A.M. Fouchier, B. Olsen, Arch. Virol. 150, 1685–1692 (2005)
W.B. Becker, J. Hyg. 64, 309–320 (1966)
Y. Kawaoka, T.M. Chambers, W.L. Sladen, R.G. Webster, Virology 163, 247–250 (1988)
L. Widjaja, S.L. Krauss, R.J. Webby, T. Xie, R.G. Webster, J. Virol. 78, 8771–8779 (2004)
H. Ip, P. Flint, J.C. Franson, R. Dusek, D. Derksen, R. Gill, C. Ely, J. Pearce, R. Lanctot, S. Matsuoka, D. Irons, J. Fischer, R. Oates, M. Petersen, T. Fondell, D. Rocque, J. Pedersen, T. Rothe, Virol. J. 5, 71 (2008)
V.J. Munster, C. Baas, P. Lexmond, J. Waldenström, A. Wallensten, T. Fransson, G.F. Rimmelzwaan, W.E.P. Beyer, M. Schutten, B. Olsen, A.D.M.E. Osterhaus, R.A.M. Fouchier, PLoS Pathog. 3, e61 (2007)
A. Gaston, Seabirds: a natural history (Yale University Press, New Haven, 2004)
E. Spackman, D.A. Senne, T.J. Myers, L.L. Bulaga, L.P. Garber, M.L. Perdue, K. Lohman, L.T. Daum, D.L. Suarez, J. Clin. Microbiol. 40, 3256–3260 (2002)
E. Hoffmann, J. Stech, Y. Guan, R.G. Webster, D.R. Perez, Arch. Virol. 146, 2275–2289 (2001)
B.-F. Qiu, W.-J. Liu, D.-X. Peng, S.-L. Hu, Y.-H. Tang, X.-F. Liu, J. Virol. Methods 155, 193–198 (2009)
S.F. Altschul, T.L. Madden, A.A. Schaffer, J. Zhang, Z. Zhang, W. Miller, D.J. Lipman, Nucleic Acids Res. 25, 3389–3402 (1997)
K. Tamura, J. Dudley, M. Nei, S. Kumar, Mol. Biol. Evol. 24, 1596–1599 (2007)
L. Tranquilla, A. Hedd, C. Burke, W.A. Montevecchi, P.M. Regular, G.J. Robertson, L.A. Stapleton, S. Wilhelm, D.A. Fifield, A.D. Buren, Estuar. Coast. Shelf Sci. (2010). doi: 10.1016/j.ecss.2010.06.003
A.A. Sazonov, D.K. Lvov, R.G. Webster, T.V. Sokolova, N.A. Braude, N.V. Portyanko, Arch. Virol. 53, 1–7 (1977)
D. Bordage, J.-P.L. Savard, BNA177, in The birds of North America, ed. by A. Poole, F. Gill (The Academy of Natural Sciences, Philadelphia, PA, 1995)
A.J. Gaston, J.M. Hipfner, BNA497, in The birds of North America, ed. by A. Poole, F. Gill (The Academy of Natural Sciences, Philadelphia, PA, 2000)
G.J. Robertson, J.-P.L. Savard, BNA651, in The birds of North America, ed. by A. Poole, F. Gill (The Academy of Natural Sciences, Philadelphia, PA, 2002)
R. Chen, E.C. Holmes, Virology 383, 156–161 (2009)
V. Bakken, F. Mehlum, Arctic 58, 268–275 (2005)
G. Donaldson, A.J. Gaston, K. Kampp, J. Chardine, D.N. Nettleship, R.D. Elliot, Winter distributions of thick-billed murres from the eastern Canadian Arctic and western Greenland in relation to age and time of year, Occasional Paper 96 (Canadian Wildlife Service, Ottawa, 1997)
A.J. Gaston, Populations, movements, and wintering areas of Thick-billed Murres (Uria lomvia) in eastern Canada, CWS Progress Notes 110 (Canadian Wildlife Service, Ottawa, 1980)
F. Huettmann, A.W. Diamond, Can. J. Zool. 78, 624–647 (2000)
P. Lyngs, Medd Grønl Biosci 38, 1–67 (2003)
Acknowledgments
We thank C. Keane, A. Blundon, A. Hedd, C. Burke, P. Regular and L. Stapleton for assistance with swab sample processing, and S. Wilhelm, P. Ryan and other Environment Canada staff for collecting and storing the dead murres. The Newfoundland and Labrador Department of Natural Resources and the Strategic Applications of Genomics in the Environment (STAGE) program at Environment Canada provided support for this study. AG was supported in part by funds from the Memorial University Department of Biology Honour’s program. MW was supported by a CGS-M fellowship from the Natural Sciences and Engineering Research Council (NSERC) and a merit fellowship from Memorial University. Research in ASL’s lab is supported by grants from NSERC, the Canada Foundation for Innovation, and the Industrial Research and Innovation Fund from the Government of Newfoundland and Labrador.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Granter, A., Wille, M., Whitney, H. et al. The genome sequence of an H11N2 avian influenza virus from a Thick-billed Murre (Uria lomvia) shows marine-specific and regional patterns of relationships to other viruses. Virus Genes 41, 224–230 (2010). https://doi.org/10.1007/s11262-010-0504-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11262-010-0504-5