Archives of Virology

, Volume 157, Issue 8, pp 1509–1522

Phylogeographic analysis of avian influenza viruses isolated from Charadriiformes in Belgium confirms intercontinental reassortment in gulls

  • Steven Van Borm
  • Toon Rosseel
  • Didier Vangeluwe
  • Frank Vandenbussche
  • Thierry van den Berg
  • Bénédicte Lambrecht
Original Article

DOI: 10.1007/s00705-012-1323-x

Cite this article as:
Van Borm, S., Rosseel, T., Vangeluwe, D. et al. Arch Virol (2012) 157: 1509. doi:10.1007/s00705-012-1323-x

Abstract

Nine influenza viruses isolated from gulls and shorebirds in Belgium (2008-2010), including H3N8, H5N2, H6N1, H11N9, H13N6, H13N8, and H16N3 subtypes, were targeted using random amplification and next-generation sequencing. The gene segments of these viruses segregated into three phylogeographic lineage types: (1) segments circulating in waterfowl in Eurasia with sporadic introduction in other species and in the Americas (“Eurasian avian”), (2) segments circulating in American waterfowl with sporadic introduction to other species and regions (“American avian”), and (3) segments circulating exclusively in gulls and shorebirds and having increased connectivity between the two hemispheres (“Charadriiformes specific”). Notably, an H6N1 and an H5N2 isolated from L. argentatus had mainly Eurasian avian genes but shared a matrix segment of American avian origin (first documentation in European gulls of transhemispheric reassortment). These data support the growing evidence of an important role of Charadriiformes birds in the dynamic nature of avian influenza ecology.

Supplementary material

705_2012_1323_MOESM1_ESM.docx (168 kb)
Supplementary material Evolutionary relationship between the complete PB2 coding sequences of nine AIV isolates from Charadriiformes and selected reference isolates (inferred using the neighbor-joining method). Confidence levels in bootstrap analysis (1000 replications) above 70% are indicated at nodes. Bootstrap support values used for defining the phylogeographic groupings are circled. Colored boxes indicate the phylogeographic clades (orange, Eurasian avian; light blue, American avian; green, Charadriiformes specific). Viruses characterized in this study are indicated in bold type. Viruses isolated from poultry are indicated in red. Asian HPAI H5N1 viruses are indicated in blue. (DOCX 168 kb)
705_2012_1323_MOESM2_ESM.docx (180 kb)
Supplementary material Evolutionary relationship between the complete PB1 coding sequences of nine AIV isolates from Charadriiformes and selected reference isolates (inferred using the neighbor-joining method). Confidence levels in bootstrap analysis (1000 replications) above 70% are indicated at nodes. Bootstrap support values used for defining the phylogeographic groupings are circled. Colored boxes indicate the phylogeographic clades (Orange, Eurasian avian; light blue, American avian; Green, Charadriiformes specific). Viruses characterized in this study are indicated in bold type. Viruses isolated from poultry are indicated in red. Asian HPAI H5N1 viruses are indicated in blue. Viruses isolated from an American geographic location in a predominantly Eurasian-origin clade are indicated in green, showing evidence for transhemispheric reassortment. (DOCX 180 kb)
705_2012_1323_MOESM3_ESM.docx (195 kb)
Supplementary material Evolutionary relationship between the complete PA coding sequences of nine AIV isolates from Charadriiformes and selected reference isolates (inferred using the neighbor-joining method). Confidence levels in bootstrap analysis (1000 replications) above 70% are indicated at nodes. Bootstrap support values used for defining the phylogeographic groupings are circled. Colored boxes indicate the phylogeographic clades (orange, Eurasian avian; light blue, American avian; green: Charadriiformes specific). Viruses characterized in this study are indicated in bold type. Asian HPAI H5N1 viruses are indicated in blue. Viruses isolated from an American geographic location in a predominantly Eurasian-origin clade are indicated in green, showing evidence for transhemispheric reassortment. (DOCX 195 kb)
705_2012_1323_MOESM4_ESM.docx (168 kb)
Supplementary material Evolutionary relationship between the complete NP coding sequences of nine AIV isolates from Charadriiformes and selected reference isolates (inferred using the neighbor-joining method). Confidence levels in bootstrap analysis (1000 replications) above 70% are indicated at nodes. Bootstrap support values used for defining the phylogeographic groupings are circled. Colored boxes indicate the phylogeographic clades (orange, Eurasian avian; light blue, American avian; green: Charadriiformes specific). Viruses characterized in this study are indicated in bold type. Viruses isolated from poultry are indicated in red. Asian HPAI H5N1 viruses are indicated in blue. Viruses isolated from an American geographic location in a predominantly Eurasian-origin clade are indicated in green, showing evidence for transhemispheric reassortment. (DOCX 168 kb)
705_2012_1323_MOESM5_ESM.docx (189 kb)
Supplementary material Evolutionary relationship between the complete NS1/NS2 coding sequences of nine AIV isolated from Charadriiformes and selected reference isolates (inferred using the neighbor-joining method). Confidence levels in bootstrap analysis (1000 replications) above 70% are indicated at nodes. Bootstrap support values used for defining the phylogeographic groupings are circled. Colored boxes indicate the phylogeographic clades (orange: Eurasian avian; light blue, American avian; green, Charadriiformes specific). Viruses characterized in this study are indicated in bold type. Viruses isolated from poultry are indicated in red. Asian HPAI H5N1 viruses are indicated in blue. Viruses isolated from an American geographic location in a predominantly Eurasian-origin clade are indicated in green, showing evidence for transhemispheric reassortment. (DOCX 188 kb)
705_2012_1323_MOESM6_ESM.docx (64 kb)
Supplementary material Evolutionary relationship between the complete hemagglutinin H3 coding sequence of A/Arenaria interpres/Belgium/17044-27/2008 (H3N8) and selected reference isolates (inferred using the neighbor-joining method). Confidence levels in bootstrap analysis (1000 replications) above 70% are indicated at nodes. Phylogeographic groupings are indicated near the defining node. Viruses characterized in this study are indicated in bold type. Viruses isolated from an American geographic location in a predominantly Eurasian-origin clade are indicated in green, showing evidence for transhemispheric reassortment. (DOCX 64 kb)
705_2012_1323_MOESM7_ESM.docx (58 kb)
Supplementary material Evolutionary relationship between the complete hemagglutinin H5 coding sequences of A/Larus argentatus/Belgium/02936cls9/2010 (H5N2) and selected reference isolates (inferred using the neighbor-joining method). Confidence levels in bootstrap analysis (1000 replications) above 70% are indicated at nodes. Phylogeographic groupings are indicated near the defining node. Viruses characterized in this study are indicated in bold type. Viruses isolated from poultry are indicated in red. Asian HPAI H5N1 viruses are indicated in blue. (DOCX 57 kb)
705_2012_1323_MOESM8_ESM.docx (101 kb)
Supplementary material Evolutionary relationship between the complete hemagglutinin H6 coding sequences of A/Larus argentatus/Belgium/02936pcs3/2010 (H6N1) and selected reference isolates (inferred using the neighbor-joining method). Confidence levels in bootstrap analysis (1000 replications) above 70% are indicated at nodes. Phylogeographic groupings are indicated near the defining node. Viruses characterized in this study are indicated in bold type. Viruses isolated from poultry are indicated in red. Viruses isolated from an American geographic location in a predominantly Eurasian-origin clade are indicated in green, showing evidence for transhemispheric reassortment. (DOCX 101 kb)
705_2012_1323_MOESM9_ESM.docx (83 kb)
Supplementary material Evolutionary relationship between the complete hemagglutinin H11 coding sequences of A/Arenaria interpres/Belgium/06765cls2/2009 (H11N9) and selected reference isolates (inferred using the neighbor-joining method). Confidence levels in bootstrap analysis (1000 replications) above 70% are indicated at nodes. Phylogeographic groupings are indicated near the defining node. Viruses characterized in this study are indicated in bold type. (DOCX 83 kb)
705_2012_1323_MOESM10_ESM.docx (46 kb)
Supplementary material Evolutionary relationship between the complete hemagglutinin H12 coding sequences of A/Arenaria interpres/Belgium/02936pcs1/2010 (H12N5) and selected reference isolates (inferred using the neighbor-joining method). Confidence levels in bootstrap analysis (1000 replications) above 70% are indicated at nodes. Phylogeographic groupings are indicated near the defining node. Viruses characterized in this study are indicated in bold type. (DOCX 46 kb)
705_2012_1323_MOESM11_ESM.docx (51 kb)
Supplementary material Evolutionary relationship between the complete neuraminidase N1 coding sequences of A/Larus argentatus/Belgium/02936pcs3/2010 (H6N1) and selected reference isolates (inferred using the neighbor-joining method). Confidence levels in bootstrap analysis (1000 replications) above 70% are indicated at nodes. Bootstrap support values used for defining the phylogeographic groupings are circled. The orange box indicates the Eurasian avian phylogeographic clade. Viruses characterized in this study are indicated in bold type. Viruses isolated from poultry are indicated in red. Asian HPAI H5N1 viruses are indicated in blue. (DOCX 51 kb)
705_2012_1323_MOESM12_ESM.docx (66 kb)
Supplementary material Evolutionary relationship between the complete neuraminidase N2 coding sequences of A/Larus argentatus/Belgium/02936cls9/2010 (H5N2) and selected reference isolates (inferred using the neighbor-joining method). Confidence levels in bootstrap analysis (1000 replications) above 70% are indicated at nodes. Bootstrap support values used for defining the phylogeographic groupings are circled. The orange box indicates the Eurasian avian phylogeographic clade. Viruses characterized in this study are indicated in bold type. (DOCX 65 kb)
705_2012_1323_MOESM13_ESM.docx (62 kb)
Supplementary material Evolutionary relationship between the complete neuraminidase N3 coding sequences of A/Larus argentatus/Belgium/14469-16/2008 (H16N3) and selected reference isolates (inferred using the neighbor-joining method). Confidence levels in bootstrap analysis (1000 replications) above 70% are indicated at nodes. Bootstrap support values used for defining the phylogeographic groupings are circled. The green box indicates the Charadriiformes-specific phylogeographic clade. Viruses characterized in this study are indicated in bold type. (DOCX 62 kb)
705_2012_1323_MOESM14_ESM.docx (63 kb)
Supplementary material Evolutionary relationship between the complete neuraminidase N5 coding sequences of A/Arenaria interpres/Belgium/02936pcs1/2010 (H12N5) and selected reference isolates (inferred using the neighbor-joining method). Confidence levels in bootstrap analysis (1000 replications) above 70% are indicated at nodes. Bootstrap support values used for defining the phylogeographic groupings are circled. The orange box indicates the Eurasian avian phylogeographic clade. Viruses characterized in this study are indicated in bold type. Viruses isolated from an American geographic location in a predominantly Eurasian-origin clade are indicated in green, showing evidence for transhemispheric reassortment. (DOCX 62 kb)
705_2012_1323_MOESM15_ESM.docx (81 kb)
Supplementary material Evolutionary relationship between the complete neuraminidase N6 coding sequences of A/Larus argentatus/Belgium/17429-3/2008 (H13N6), A/Larus argentatus/Belgium/17429-1′/2008 (H13N6), and selected reference isolates (inferred using the neighbor-joining method). Confidence levels in bootstrap analysis (1000 replications) above 70% are indicated at nodes. Bootstrap support values used for defining the phylogeographic groupings are circled. The green box indicates the Charadriiformes-specific phylogeographic clade. Viruses characterized in this study are indicated in bold type. (DOCX 80 kb)
705_2012_1323_MOESM16_ESM.docx (95 kb)
Supplementary material Evolutionary relationship between the complete neuraminidase N8 coding sequences of A/Arenaria interpres/Belgium/17044-27/2008 (H13N8), A/Larus argentatus/Belgium/14469-20/2008 (H13N8), and selected reference isolates (inferred using the neighbor-joining method). Confidence levels in bootstrap analysis (1000 replications) above 70% are indicated at nodes. Bootstrap support values used for defining the phylogeographic groupings are circled. The orange box indicates the Eurasian avian phylogeographic clade. The grey box indicates a Charadriiformes-specific subclade. Viruses characterized in this study are indicated in bold type (DOCX 95 kb)
705_2012_1323_MOESM17_ESM.docx (71 kb)
Supplementary material Evolutionary relationship between the complete neuraminidase N9 coding sequences of A/Arenaria interpres/Belgium/06765cls2/2009 (H11N9) and selected reference isolates (inferred using the neighbor-joining method). Confidence levels in bootstrap analysis (1000 replications) above 70% are indicated at nodes. Bootstrap support values used for defining the phylogeographic groupings are circled. The orange box indicates the Eurasian avian phylogeographic clade. Viruses characterized in this study are indicated in bold type. (DOCX 70 kb)

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Steven Van Borm
    • 1
  • Toon Rosseel
    • 1
  • Didier Vangeluwe
    • 2
  • Frank Vandenbussche
    • 1
  • Thierry van den Berg
    • 1
  • Bénédicte Lambrecht
    • 1
  1. 1.Department of VirologyVeterinary and Agrochemical Research CenterUccleBelgium
  2. 2.Belgian Ringing CenterRoyal Belgian Institute for Natural SciencesBrusselsBelgium

Personalised recommendations