Extensive Geographic Mosaicism in Avian Influenza Viruses from Gulls in the Northern Hemisphere

Abstract

Due to limited interaction of migratory birds between Eurasia and America, two independent avian influenza virus (AIV) gene pools have evolved. There is evidence of low frequency reassortment between these regions, which has major implications in global AIV dynamics. Indeed, all currently circulating lineages of the PB1 and PA segments in North America are of Eurasian origin. Large-scale analyses of intercontinental reassortment have shown that viruses isolated from Charadriiformes (gulls, terns, and shorebirds) are the major contributor of these outsider events. To clarify the role of gulls in AIV dynamics, specifically in movement of genes between geographic regions, we have sequenced six gull AIV isolated in Alaska and analyzed these along with 142 other available gull virus sequences. Basic investigations of host species and the locations and times of isolation reveal biases in the available sequence information. Despite these biases, our analyses reveal a high frequency of geographic reassortment in gull viruses isolated in America. This intercontinental gene mixing is not found in the viruses isolated from gulls in Eurasia. This study demonstrates that gulls are important as vectors for geographically reassorted viruses, particularly in America, and that more surveillance effort should be placed on this group of birds.

Long-Term Effect of Serial Infections with H13 and H16 Low-Pathogenic Avian Influenza Viruses in Black-Headed Gulls

“…Therefore, exposure to a LPAIV with the same HA and NA genes may have strengthened the protective effect against reinoculation with the homologous virus. The NS gene segment of H13 belonged to allele B, and that of H16 belonged to allele A (the most common NS allele) (32,33). The NS1 protein, one of the two proteins encoded by the NS gene segment, is able to inhibit the host innate immune response by antagonizing interferon.…”

Narrative overview on wild bird migration in the context of highly pathogenic avian influenza incursion into the European Union

“…However, some groups such as shorebirds and gulls in the Charadriiformes are of relevance for IAV. For instance, given specific environmental conditions shorebirds may become infected with LPAIV, such as Ruddy Turnstones (Arenaria interpres) and other spring migrating shorebirds in Delaware Bay in the US (Krauss et al, 2010;Maxted et al, 2012), while gulls have been repeatedly shown to carry gull-specific IAV of the H13 and H16 subtypes (Wille et al, 2011a;Verhagen et al, 2014;Arnal et al, 2015).…”

“…Several studies have identified gulls as carriers of LPAIV, although primarily of the gull-specific H13 and H16 subtypes (Wille et al, 2011a;Verhagen et al, 2014;Arnal et al, 2015). It is a diverse group of birds that includes species that are predominantly marine (such as the Black-legged Kittiwake (Rissa tridactyla) and Glaucous Gull (Larus hyperboreus)) and species that alternate between marine or coastal environments, wetlands and agricultural land depending on the time of the year and geography.…”

Evaluation of Seabirds in Newfoundland and Labrador, Canada, as Hosts of Influenza A Viruses

“…Positive samples had real-time reverse transcriptase PCR (rRT-PCR) threshold cycle values ,35 or were successfully cultured. Hemagglutinin and neuraminidase subtypes were determined by sequencing (Wille et al 2011). In addition to swab samples, blood was collected from 115 adult Common Murres and 41 adult Atlantic Puffins (Fratercula arctica) in 2011 using established protocols, and tested for anti-nucleoprotein (NP) antibodies using the AI MultiSScreen Ab Test (IDEXX, Westbrook, Maine, USA) as recommended by the manufacturer.…”

“…This could result from interactions among birds from the two regions during the nonbreeding season, and AIV has now been detected twice in Thick-billed Murres during the winter. Ecologically, gulls would be more likely to act as intermediates for moving viruses between waterfowl and seabirds, as they often breed on the same islands as seabirds and also use coastal and inland waters that are utilized by waterfowl, but this is not well supported virologically because gulls mostly carry distinct lineages of AIV (Kawaoka et al 1988;Fouchier et al 2005;Wille et al 2011), which have not been identified in seabirds. It has been suggested that if AIV is introduced to a seabird colony, transmission should be high because of high host densities and immunologically naïve chicks (Clancy et al 2006).…”