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Genetic diversity and mutation of avian paramyxovirus serotype 1 (Newcastle disease virus) in wild birds and evidence for intercontinental spread

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Abstract

Avian paramyxovirus serotype 1 (APMV-1), or Newcastle disease virus, is the causative agent of Newcastle disease, one of the most economically important diseases for poultry production worldwide and a cause of periodic epizootics in wild birds in North America. In this study, we examined the genetic diversity of APMV-1 isolated from migratory birds sampled in Alaska, Japan, and Russia and assessed the evidence for intercontinental virus spread using phylogenetic methods. Additionally, we predicted viral virulence using deduced amino acid residues for the fusion protein cleavage site and estimated mutation rates for the fusion gene of class I and class II migratory bird isolates. All 73 isolates sequenced as part of this study were most closely related to virus genotypes previously reported for wild birds; however, five class II genotype I isolates formed a monophyletic clade exhibiting previously unreported genetic diversity, which met criteria for the designation of a new sub-genotype. Phylogenetic analysis of wild-bird isolates provided evidence for intercontinental virus spread, specifically viral lineages of APMV-1 class II genotype I sub-genotypes Ib and Ic. This result supports migratory bird movement as a possible mechanism for the redistribution of APMV-1. None of the predicted deduced amino acid motifs for the fusion protein cleavage site of APMV-1 strains isolated from migratory birds in Alaska, Japan, and Russia were consistent with those of previously identified virulent viruses. These data therefore provide no support for these strains contributing to the emergence of avian pathogens. The estimated mutation rates for fusion genes of class I and class II wild-bird isolates were faster than those reported previously for non-virulent APMV-1 strains. Collectively, these findings provide new insight into the diversity, spread, and evolution of APMV-1 in wild birds.

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Acknowledgments

We thank D. Williams-Coplin of the U.S. Department of Agriculture (USDA) for her assistance in sequencing APMV-1 fusion genes from Russian isolates. We are grateful to J. Pearce, T. DeGange, P. Bright, K. Briggs, and S. Gross of the U.S. Geological Survey (USGS) for financial and administrative support. Numerous biologists assisted with virus sampling, and their efforts are much appreciated. We thank past and current members of the Diagnostic Virology Laboratory at the USGS National Wildlife Health Center, including T. Egstad, K. Griffin, M. Houfe, and R. Long. Y. Gillies, J. Wiley, D. Goldberg, and R. Zane of the USGS and M. St. Peters of the U.S. Fish and Wildlife Service coordinated distribution of sampling materials, receipt of samples, and data verification. We appreciate reviews provided by J. Pearce, P. Miller (USDA), J. Phillips (University of Georgia), and two anonymous reviewers. None of the authors have any financial interests or conflict of interest with this article. Any use of trade names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

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Authors and Affiliations

  1. US Geological Survey, Alaska Science Center, 4210 University Drive, Anchorage, AK, 99508, USA

    Andrew M. Ramey & Andrew B. Reeves

  2. Southeastern Cooperative Wildlife Disease Study, The University of Georgia, 589 D. W. Brooks Drive, Athens, GA, 30602, USA

    Andrew M. Ramey

  3. Research Center for Animal Hygiene and Food Safety, Obihiro University of Agriculture and Veterinary Medicine, 2-11 Inada, Obihiro, Hokkaido, 080-8555, Japan

    Haruko Ogawa, Kunitoshi Imai, Vuong Nghia Bui & Emi Yamaguchi

  4. US Geological Survey, National Wildlife Health Center, 6006 Schroeder Road, Madison, WI, 53711, USA

    Hon S. Ip

  5. State Research Center of Virology and Biotechnology ‘VECTOR’, Novosibirsk Region, 630559, Koltsovo, Russia

    Nikita Y. Silko

  6. US Department of Agriculture, Agriculture Research Service, Southeast Poultry Research Laboratory, 934 College Station Road, Athens, GA, 30605, USA

    Claudio L. Afonso

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Correspondence to Andrew M. Ramey.

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705_2013_1761_MOESM1_ESM.eps

Supplemental Figure S1. Phylogenetic tree showing the relative positions of all avian paramyxovirus serotype 1 fusion gene complete coding sequences (1,662 bp; identified by GenBank accession number) analyzed as part of this study (n = 739). The maximum-likelihood tree was generated with MEGA version 5.1 [30] using the nucleotide: nearest-neighbor-interchange method with 10,000 bootstrap replicates. Bootstrap support values are reported to the left of nodes. Sub-genotypes for class I genotype 1 and class II genotype I isolates are indicated by brackets (EPS 3806 kb)

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Ramey, A.M., Reeves, A.B., Ogawa, H. et al. Genetic diversity and mutation of avian paramyxovirus serotype 1 (Newcastle disease virus) in wild birds and evidence for intercontinental spread. Arch Virol 158, 2495–2503 (2013). https://doi.org/10.1007/s00705-013-1761-0

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