Evolution of a reassortant North American gull influenza virus lineage: drift, shift and stability

Jeffrey S Hall,Hon S Ip,Vivien Dugan,Rebecca A Halpin,Joshua L Teslaa,Sean W Nashold,Timothy Stockwell,David E Wentworth

doi:10.1186/1743-422x-10-179

Jeffrey S Hall, Hon S Ip + Show 6 more

Open Access

https://doi.org/10.1186/1743-422x-10-179

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Abstract

BackgroundThe role of gulls in the ecology of avian influenza (AI) is different than that of waterfowl. Different constellations of subtypes circulate within the two groups of birds and AI viruses isolated from North American gulls frequently possess reassortant genomes with genetic elements from both North America and Eurasian lineages. A 2008 isolate from a Newfoundland Great Black-backed Gull contained a mix of North American waterfowl, North American gull and Eurasian lineage genes.MethodsWe isolated, sequenced and phylogenetically compared avian influenza viruses from 2009 Canadian wild birds.ResultsWe analyzed six 2009 virus isolates from Canada and found the same phylogenetic lineage had persisted over a larger geographic area, with an expanded host range that included dabbling and diving ducks as well as gulls. All of the 2009 virus isolates contained an internal protein coding set of genes of the same Eurasian lineage genes except PB1 that was from a North American lineage, and these genes continued to evolve by genetic drift. We show evidence that the 2008 Great Black-backed Gull virus was derived from this lineage with a reassortment of a North American PA gene into the more stable core set of internal protein coding genes that has circulated in avian populations for at least 2 years. From this core, the surface glycoprotein genes have switched several times creating H13N6, H13N2, and H16N3 subtypes. These gene segments were from North American lineages except for the H16 and N3 vRNAs.ConclusionsThis process appears similar to genetic shifts seen with swine influenza where a stable “triple reassortant internal gene” core has circulated in swine populations with genetic shifts occurring with hemaggluttinin and neuraminidase proteins getting periodically switched. Thus gulls may serve as genetic mixing vessels for different lineages of avian influenza, similar to the role of swine with regards to human influenza. These findings illustrate the need for continued surveillance in gull and waterfowl populations, both on the Pacific and especially Atlantic coasts of North America, to document virus intercontinental movement and the role of gull species in the evolution and epidemiology of AI.

Highlights

The principle reservoirs of avian influenza virus (AIV) are wild waterfowl (Anseriformes) and shorebirds and gulls (Charadriiformes) [1]
Because AIV has a genome comprised of eight RNA segments, if a host cell becomes infected with two or more viruses, these vRNAs can reassort and the resulting progeny may contain hybrid genomes of the parental viruses
From 2719 swab samples taken in 2009, we were able to isolate 55 avian influenza viruses from Canadian birds, primarily from waterfowl in the Maritime Provinces. Genomic sequencing of these isolates and phylogenetic comparisons of each full length RNA segment revealed that the majority of the viruses were related to North American duck viruses

Summary

Introduction

The principle reservoirs of avian influenza virus (AIV) are wild waterfowl (Anseriformes) and shorebirds and gulls (Charadriiformes) [1]. No completely Eurasian influenza virus has been isolated in North America, there is increasing evidence that reassortment between the lineages occurs regularly. Alaska and areas of Asia adjacent to the Bering Sea are sites of active interlineage reassortment [4,5,6] This is not surprising given the proximity of Asia and North America in that region and that large numbers of birds cross between the continents during seasonal migrations. Different constellations of subtypes circulate within the two groups of birds and AI viruses isolated from North American gulls frequently possess reassortant genomes with genetic elements from both North America and Eurasian lineages. A 2008 isolate from a Newfoundland Great Black-backed Gull contained a mix of North American waterfowl, North American gull and Eurasian lineage genes

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