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Characterizing a century of genetic diversity and contemporary antigenic diversity of N1 neuraminidase in IAV from North American swine

View ORCID ProfileDavid E. Hufnagel, View ORCID ProfileKatharine M. Young, View ORCID ProfileZebulun Arendsee, View ORCID ProfileL. Claire Gay, View ORCID ProfileC. Joaquin Caceres, View ORCID ProfileDaniela S. Rajão, View ORCID ProfileDaniel R. Perez, View ORCID ProfileAmy L. Vincent Baker, View ORCID ProfileTavis K. Anderson
doi: https://doi.org/10.1101/2022.11.18.517097
David E. Hufnagel
aVirus and Prion Research Unit, National Animal Disease Center, USDA-ARS, 1920 Dayton Ave, Ames, IA, 50010, USA
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  • ORCID record for David E. Hufnagel
Katharine M. Young
aVirus and Prion Research Unit, National Animal Disease Center, USDA-ARS, 1920 Dayton Ave, Ames, IA, 50010, USA
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Zebulun Arendsee
aVirus and Prion Research Unit, National Animal Disease Center, USDA-ARS, 1920 Dayton Ave, Ames, IA, 50010, USA
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L. Claire Gay
bDepartment of Population Health, College of Veterinary Medicine, University of Georgia, 953 College Station Rd, Athens, GA 30602, USA
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C. Joaquin Caceres
bDepartment of Population Health, College of Veterinary Medicine, University of Georgia, 953 College Station Rd, Athens, GA 30602, USA
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Daniela S. Rajão
bDepartment of Population Health, College of Veterinary Medicine, University of Georgia, 953 College Station Rd, Athens, GA 30602, USA
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Daniel R. Perez
bDepartment of Population Health, College of Veterinary Medicine, University of Georgia, 953 College Station Rd, Athens, GA 30602, USA
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Amy L. Vincent Baker
aVirus and Prion Research Unit, National Animal Disease Center, USDA-ARS, 1920 Dayton Ave, Ames, IA, 50010, USA
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Tavis K. Anderson
aVirus and Prion Research Unit, National Animal Disease Center, USDA-ARS, 1920 Dayton Ave, Ames, IA, 50010, USA
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  • For correspondence: tavis.anderson@usda.gov
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ABSTRACT

Influenza A viruses (IAV) of the H1N1 classical swine lineage became endemic in North American swine following the 1918 pandemic. Additional human-to-swine transmission events after 1918, and a spillover of H1 viruses from wild birds in Europe, potentiated a rapid increase in genomic diversity via reassortment between introductions and the endemic classical swine lineage. To determine mechanisms affecting reassortment and evolution, we conducted a phylogenetic analysis of N1 and paired HA swine IAV genes in North America between 1930 and 2020. We described fourteen N1 clades within the N1 Eurasian avian lineage (including the N1 pandemic clade) and the N1 classical swine lineage. Seven N1 genetic clades had evidence for contemporary circulation. To assess antigenic drift associated with N1 genetic diversity, we generated a panel of representative swine N1 antisera and quantified the antigenic distance between wild-type viruses using enzyme-linked lectin assays and antigenic cartography. Within the N1 lineage, antigenic similarity was variable and reflected shared evolutionary history. Sustained circulation and evolution of N1 genes in swine had resulted in significant antigenic distance between the N1 pandemic clade and classical swine lineage. We also observed a significant increase in the rate of evolution in the N1 pandemic clade relative to the classical lineage. Between 2010 and 2020, N1 clades and N1-HA pairings fluctuated in detection frequency across North America, with hotspots of diversity generally appearing and disappearing within two years. We also identified frequent N1-HA reassortment events (n = 36), which were rarely sustained (n = 6) and sometimes also concomitant with the emergence of new N1 genetic clades (n = 3). These data form a baseline from which we can identify N1 clades that expand in range or genetic diversity that may impact viral phenotypes or vaccine immunity and subsequently the health of North American swine.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://github.com/flu-crew/N1-diversity

  • https://doi.org/10.15482/USDA.ADC/1528285

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. This article is a US Government work. It is not subject to copyright under 17 USC 105 and is also made available for use under a CC0 license.
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Characterizing a century of genetic diversity and contemporary antigenic diversity of N1 neuraminidase in IAV from North American swine
David E. Hufnagel, Katharine M. Young, Zebulun Arendsee, L. Claire Gay, C. Joaquin Caceres, Daniela S. Rajão, Daniel R. Perez, Amy L. Vincent Baker, Tavis K. Anderson
bioRxiv 2022.11.18.517097; doi: https://doi.org/10.1101/2022.11.18.517097
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Characterizing a century of genetic diversity and contemporary antigenic diversity of N1 neuraminidase in IAV from North American swine
David E. Hufnagel, Katharine M. Young, Zebulun Arendsee, L. Claire Gay, C. Joaquin Caceres, Daniela S. Rajão, Daniel R. Perez, Amy L. Vincent Baker, Tavis K. Anderson
bioRxiv 2022.11.18.517097; doi: https://doi.org/10.1101/2022.11.18.517097

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