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Genetic and antigenic characterization of an expanding H3 influenza A virus clade in US swine visualized by Nextstrain

Megan N. Neveau, Michael A. Zeller, View ORCID ProfileBryan S. Kaplan, View ORCID ProfileCarine K. Souza, View ORCID ProfilePhillip C. Gauger, View ORCID ProfileAmy L. Vincent, View ORCID ProfileTavis K. Anderson
doi: https://doi.org/10.1101/2021.11.17.469008
Megan N. Neveau
aDepartment of Veterinary Diagnostic and Production Animal Medicine, College of Veterinary Medicine, Iowa State University, Ames, Iowa, USA
bBioinformatics and Computational Biology Program, Iowa State University, Ames, Iowa, USA
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Michael A. Zeller
aDepartment of Veterinary Diagnostic and Production Animal Medicine, College of Veterinary Medicine, Iowa State University, Ames, Iowa, USA
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Bryan S. Kaplan
cVirus and Prion Research Unit, National Animal Disease Center, USDA-ARS, Ames, Iowa, USA
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Carine K. Souza
cVirus and Prion Research Unit, National Animal Disease Center, USDA-ARS, Ames, Iowa, USA
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Phillip C. Gauger
aDepartment of Veterinary Diagnostic and Production Animal Medicine, College of Veterinary Medicine, Iowa State University, Ames, Iowa, USA
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Amy L. Vincent
cVirus and Prion Research Unit, National Animal Disease Center, USDA-ARS, Ames, Iowa, USA
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Tavis K. Anderson
cVirus and Prion Research Unit, National Animal Disease Center, USDA-ARS, Ames, Iowa, USA
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  • For correspondence: tavis.anderson@usda.gov
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Abstract

Defining factors that influence spatial and temporal patterns of influenza A virus (IAV) is essential to inform vaccine strain selection and strategies to reduce the spread of potentially zoonotic swine-origin IAV. The relative frequency of detection of the H3 phylogenetic clade 1990.4.a (colloquially known as C-IVA) in US swine declined to 7% in 2017, but increased to 32% in 2019. We conducted phylogenetic and phenotypic analyses to determine putative mechanisms associated with increased detection. We created an implementation of Nextstrain to visualize the emergence, spatial spread, and genetic evolution of H3 IAV-S, identifying two C-IVA clades that emerged in 2017 and cocirculated in multiple US states. Phylodynamic analysis of the HA gene documented low relative genetic diversity from 2017 to 2019, suggesting clonal expansion. The major H3 C-IVA clade contained an N156H amino acid substitution, but HI assays demonstrated no significant antigenic drift. The minor HA clade was paired with the NA clade N2-2002B prior to 2016, but acquired and maintained N2-2002A in 2016, resulting in a loss in antigenic cross-reactivity between N2-2002B and −2002A containing H3N2 strains. The major C-IVA clade viruses acquired a nucleoprotein (NP) of the H1N1pdm09 lineage through reassortment in replacement of the North American swine lineage NP. Instead of genetic or antigenic diversity within the C-IVA HA, our data suggest that population immunity to H3 2010.1, along with antigenic diversity of the NA and acquisition of the H1N1pdm09 NP gene likely explain the re-emergence and transmission of C-IVA H3N2 in swine.

Importance Genetically distinct clades of influenza A virus (IAV) in swine undermines efforts to control the disease. Swine producers commonly use vaccines, and vaccine strains are selected by identifying the most common hemagglutinin (HA) gene from viruses detected in a farm or a region. In 2019, we identified an increase in detection frequency of an H3 phylogenetic clade, C-IVA, which was previously circulating at much lower levels in U.S. swine. Our study identified genetic and antigenic factors contributing to its resurgence by linking comprehensive phylodynamic analyses with empirical wet-lab experiments and visualized these evolutionary analyses in a Nextstrain implementation. The contemporary C-IVA HA genes did not demonstrate an increase in genetic diversity nor significant antigenic changes. N2 genes did demonstrate antigenic diversity, and the expanding C-IVA clade acquired a nucleoprotein (NP) gene segment via reassortment. Virus phenotype and vaccination targeting prior dominant HA clades likely contributed to the clade’s success.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://github.com/flu-crew/h3-iva-evolution

  • https://flu-crew.org/

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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Posted November 19, 2021.
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Genetic and antigenic characterization of an expanding H3 influenza A virus clade in US swine visualized by Nextstrain
Megan N. Neveau, Michael A. Zeller, Bryan S. Kaplan, Carine K. Souza, Phillip C. Gauger, Amy L. Vincent, Tavis K. Anderson
bioRxiv 2021.11.17.469008; doi: https://doi.org/10.1101/2021.11.17.469008
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Genetic and antigenic characterization of an expanding H3 influenza A virus clade in US swine visualized by Nextstrain
Megan N. Neveau, Michael A. Zeller, Bryan S. Kaplan, Carine K. Souza, Phillip C. Gauger, Amy L. Vincent, Tavis K. Anderson
bioRxiv 2021.11.17.469008; doi: https://doi.org/10.1101/2021.11.17.469008

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