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Archives of Virology

, Volume 161, Issue 9, pp 2519–2526 | Cite as

Evidence for wild waterfowl origin of H7N3 influenza A virus detected in captive-reared New Jersey pheasants

  • Andrew M. RameyEmail author
  • Mia Kim Torchetti
  • Rebecca L. Poulson
  • Deborah Carter
  • Andrew B. Reeves
  • Paul Link
  • Patrick Walther
  • Camille Lebarbenchon
  • David E. Stallknecht
Original Article

Abstract

In August 2014, a low-pathogenic H7N3 influenza A virus was isolated from pheasants at a New Jersey gamebird farm and hunting preserve. In this study, we use phylogenetic analyses and calculations of genetic similarity to gain inference into the genetic ancestry of this virus and to identify potential routes of transmission. Results of maximum-likelihood (ML) and maximum-clade-credibility (MCC) phylogenetic analyses provide evidence that A/pheasant/New Jersey/26996-2/2014 (H7N3) had closely related H7 hemagglutinin (HA) and N3 neuraminidase (NA) gene segments as compared to influenza A viruses circulating among wild waterfowl in the central and eastern USA. The estimated time of the most recent common ancestry (TMRCA) between the pheasant virus and those most closely related from wild waterfowl was early 2013 for both the H7 HA and N3 NA gene segments. None of the viruses from waterfowl identified as being most closely related to A/pheasant/New Jersey/26996-2/2014 at the HA and NA gene segments in ML and MCC phylogenetic analyses shared ≥99 % nucleotide sequence identity for internal gene segment sequences. This result indicates that specific viral strains identified in this study as being closely related to the HA and NA gene segments of A/pheasant/New Jersey/26996-2/2014 were not the direct predecessors of the etiological agent identified during the New Jersey outbreak. However, the recent common ancestry of the H7 and N3 gene segments of waterfowl-origin viruses and the virus isolated from pheasants suggests that viral diversity maintained in wild waterfowl likely played an important role in the emergence of A/pheasant/New Jersey/26996-2/2014.

Keywords

Gene Segment Nucleotide Sequence Identity Genetic Ancestry Domestic Bird Coalescent Analysis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

We appreciate field and laboratory support by Nick Davis-Fields, Alinde Fojtik, Clara Kienzle, and John Reed. We thank John Pearce, Mary Pantin-Jackwood, and two anonymous reviewers for providing critical reviews.

Compliance with ethical standards

This project was Funded by the U.S. Geological Survey through the Wildlife Program of the Ecosystems Mission area, the National Institute of Allergy and Infectious Diseases, National Institutes of Health, Department of Health and Human Services, under contract HHSN272201400006C., and by ‘chaire mixte: institut national de la santé et de la recherche médicale – université de La Réunion’. 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. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Supplementary material

705_2016_2947_MOESM1_ESM.pdf (1.2 mb)
Supplemental Figure S1 Maximum-likelihood phylogenetic tree depicting the inferred relationship among 501 sequences for H7 hemagglutinin gene segments derived from influenza A viruses isolated from wild and domestic birds in North America. Branch tips for sequences selected for maximum-clade-credibility analysis are colored red. Bootstrap support values > 70 are presented. Sequences generated for this study are indicated in bold font. The position of the sequence for A/pheasant/New Jersey/26996-2/2014 (H7N3) is indicated with an asterisk (*). Supplemental Figure S2. Maximum-likelihood phylogenetic tree depicting the inferred relationship among 501 sequences for N3 neuraminidase gene segments derived from influenza A viruses isolated from wild and domestic birds in North America. Branch tips for sequences selected for maximum-clade-credibility analysis are colored red. Bootstrap support values > 70 are presented. Sequences determined in this study are indicated in bold font. The position of the sequence for A/pheasant/New Jersey/26996-2/2014 (H7N3) is indicated with an asterisk (*). Supplemental Figure S3. Maximum-clade-credibility tree depicting the inferred ancestry of sequences of PB2 gene segments derived from influenza A viruses isolated from wild and domestic birds in North America. Posterior probability values > 0.7 are reported. Grey bars indicate the 95% HPD for the time of the most recent common ancestors. Sequences generated for this study are indicated in bold. The branch tip for A/pheasant/New Jersey/26996-2/2014 (H7N3) is colored red. Supplemental Figure S4. Maximum-clade-credibility tree depicting the inferred ancestry of sequences of PB1 gene segments derived from influenza A viruses isolated from wild and domestic birds in North America. Posterior probability values > 0.7 are reported. Grey bars indicate the 95% HPD for the time of the most recent common ancestors. Sequences generated for this study are indicated in bold. The branch tip for A/pheasant/New Jersey/26996-2/2014 (H7N3) is colored red. Supplemental Figure S5. Maximum-clade-credibility tree depicting the inferred ancestry of sequences of PA gene segments derived from influenza A viruses isolated from wild and domestic birds in North America. Posterior probability values > 0.7 are reported. Grey bars indicate the 95% HPD for the time of the most recent common ancestors. Sequences generated for this study are indicated in bold. The branch tip for A/pheasant/New Jersey/26996-2/2014 (H7N3) is colored red. Supplemental Figure S6. Maximum-clade-credibility tree depicting the inferred ancestry of sequences of NP gene segments derived from influenza A viruses isolated from wild and domestic birds in North America. Posterior probability values > 0.7 are reported. Grey bars indicate the 95% HPD for the time of the most recent common ancestors. Sequences generated for this study are indicated in bold. The branch tip for A/pheasant/New Jersey/26996-2/2014 (H7N3) is colored red. Supplemental Figure S7. Maximum-clade-credibility tree depicting the inferred ancestry of sequences of M gene segments derived from influenza A viruses isolated from wild and domestic birds in North America. Posterior probability values > 0.7 are reported. Grey bars indicate the 95% HPD for the time of the most recent common ancestors. Sequences generated for this study are indicated in bold. The branch tip for A/pheasant/New Jersey/26996-2/2014 (H7N3) is colored red. Supplemental Figure S8. Maximum-clade-credibility tree depicting the inferred ancestry of sequences of NS gene segments derived from influenza A viruses isolated from wild and domestic birds in North America. Posterior probability values > 0.7 are reported. Grey bars indicate the 95% HPD for the time of the most recent common ancestors. Sequences generated for this study are indicated in bold. The branch tip for A/pheasant/New Jersey/26996-2/2014 (H7N3) is colored red. (PDF 1246 kb)
705_2016_2947_MOESM2_ESM.pdf (9 kb)
Supplementary material 2 (PDF 9 kb)
705_2016_2947_MOESM3_ESM.xlsx (14 kb)
Supplementary material 3 (XLSX 14 kb)

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Copyright information

© Springer-Verlag Wien (Outside the USA) 2016

Authors and Affiliations

  • Andrew M. Ramey
    • 1
    Email author
  • Mia Kim Torchetti
    • 2
  • Rebecca L. Poulson
    • 3
  • Deborah Carter
    • 3
  • Andrew B. Reeves
    • 1
  • Paul Link
    • 4
  • Patrick Walther
    • 5
  • Camille Lebarbenchon
    • 6
  • David E. Stallknecht
    • 3
  1. 1.U.S. Geological SurveyAlaska Science CenterAnchorageUSA
  2. 2.National Veterinary Services Laboratories, Veterinary ServicesU.S. Department of AgricultureAmesUSA
  3. 3.Southeastern Cooperative Wildlife Disease Study, Department of Population Health, College of Veterinary MedicineUniversity of GeorgiaAthensUSA
  4. 4.Louisiana Department of Wildlife and FisheriesBaton RougeUSA
  5. 5.US Fish and Wildlife ServiceTexas Chenier Plain Refuge ComplexAnahuacUSA
  6. 6.Université de La Réunion, UMR Processus Infectieux en Milieu Insulaire Tropical, INSERM 1187, CNRS 9192, IRD 249Saint DenisRéunion

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