Spatial and temporal coevolution of N2 neuraminidase and H1 and H3 hemagglutinin genes of influenza A virus in US swine
Abstract
Abstract The neuraminidase (NA) and hemagglutinin (HA) are essential surface glycoproteins of influenza A virus (IAV). In this study, the evolution of subtype N2 NA paired with H1 and H3 subtype HA in swine was evaluated to understand if the genetic diversity of HA and NA were linked. Using time-scaled Bayesian phylodynamic analyses, the relationships of paired swine N2 with H1 or H3 from 2009 to 2018 were evaluated. These data demonstrated increased relative genetic diversity within the major N2 clades circulating in swine in the USA (N2.1998 between 2014 and 2017 and N2.2002 between 2010 and 2016). Preferential pairing was observed among specific NA and HA genetic clades. Gene reassortment between cocirculating influenza A strains resulted in novel pairings that persisted. The changes in genetic diversity in the NA gene were quantified using Bayesian phylodynamic analyses, and increases in diversity were observed subsequent to novel NA–HA reassortment events. The rate of evolution among NA–N2 clades and HA–H1 and HA–H3 clades were similar. Bayesian phylodynamic analyses demonstrated strong spatial patterns in N2 genetic diversity, but frequent interstate movement of rare N2 clades provided opportunity for reassortment and emergence of new N2–HA pairings. The frequent regional movement of pigs and theirmore »
- Publication Date:
- Research Org.:
- Oak Ridge Associated Universities (ORAU), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE; USDOE: Iowa State University; USDA; National Institute of Allergy and Infectious Diseases (NIAID); Defense Advanced Research Projects Agency (DARPA)
- OSTI Identifier:
- 1846217
- Alternate Identifier(s):
- OSTI ID: 1982727
- Grant/Contract Number:
- AC05-06OR23100; HHSN272201400008C; HR00112020034
- Resource Type:
- Published Article
- Journal Name:
- Virus Evolution
- Additional Journal Information:
- Journal Name: Virus Evolution Journal Volume: 7 Journal Issue: 2; Journal ID: ISSN 2057-1577
- Publisher:
- Oxford University Press
- Country of Publication:
- United Kingdom
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Virology; Neuraminidase; Genomic epidemiology; Influenza A virus; Swine; Vaccine
Citation Formats
Zeller, Michael A., Chang, Jennifer, Vincent, Amy L., Gauger, Phillip C., and Anderson, Tavis K. Spatial and temporal coevolution of N2 neuraminidase and H1 and H3 hemagglutinin genes of influenza A virus in US swine. United Kingdom: N. p., 2021.
Web. doi:10.1093/ve/veab090.
Zeller, Michael A., Chang, Jennifer, Vincent, Amy L., Gauger, Phillip C., & Anderson, Tavis K. Spatial and temporal coevolution of N2 neuraminidase and H1 and H3 hemagglutinin genes of influenza A virus in US swine. United Kingdom. https://doi.org/10.1093/ve/veab090
Zeller, Michael A., Chang, Jennifer, Vincent, Amy L., Gauger, Phillip C., and Anderson, Tavis K. Fri .
"Spatial and temporal coevolution of N2 neuraminidase and H1 and H3 hemagglutinin genes of influenza A virus in US swine". United Kingdom. https://doi.org/10.1093/ve/veab090.
@article{osti_1846217,
title = {Spatial and temporal coevolution of N2 neuraminidase and H1 and H3 hemagglutinin genes of influenza A virus in US swine},
author = {Zeller, Michael A. and Chang, Jennifer and Vincent, Amy L. and Gauger, Phillip C. and Anderson, Tavis K.},
abstractNote = {Abstract The neuraminidase (NA) and hemagglutinin (HA) are essential surface glycoproteins of influenza A virus (IAV). In this study, the evolution of subtype N2 NA paired with H1 and H3 subtype HA in swine was evaluated to understand if the genetic diversity of HA and NA were linked. Using time-scaled Bayesian phylodynamic analyses, the relationships of paired swine N2 with H1 or H3 from 2009 to 2018 were evaluated. These data demonstrated increased relative genetic diversity within the major N2 clades circulating in swine in the USA (N2.1998 between 2014 and 2017 and N2.2002 between 2010 and 2016). Preferential pairing was observed among specific NA and HA genetic clades. Gene reassortment between cocirculating influenza A strains resulted in novel pairings that persisted. The changes in genetic diversity in the NA gene were quantified using Bayesian phylodynamic analyses, and increases in diversity were observed subsequent to novel NA–HA reassortment events. The rate of evolution among NA–N2 clades and HA–H1 and HA–H3 clades were similar. Bayesian phylodynamic analyses demonstrated strong spatial patterns in N2 genetic diversity, but frequent interstate movement of rare N2 clades provided opportunity for reassortment and emergence of new N2–HA pairings. The frequent regional movement of pigs and their influenza viruses is an explanation for the documented patterns of reassortment and subsequent changes in gene diversity. The reassortment and evolution of NA and linked HA evolution may result in antigenic drift of both major surface glycoproteins, reducing vaccine efficacy, with subsequent impact on animal health.},
doi = {10.1093/ve/veab090},
journal = {Virus Evolution},
number = 2,
volume = 7,
place = {United Kingdom},
year = {Fri Oct 08 00:00:00 EDT 2021},
month = {Fri Oct 08 00:00:00 EDT 2021}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1093/ve/veab090
https://doi.org/10.1093/ve/veab090
Other availability
Search WorldCat to find libraries that may hold this journal
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms
journal, May 2018
- Kumar, Sudhir; Stecher, Glen; Li, Michael
- Molecular Biology and Evolution, Vol. 35, Issue 6
Guidelines for Identifying Homologous Recombination Events in Influenza A Virus
journal, May 2010
- Boni, Maciej F.; de Jong, Menno D.; van Doorn, H. Rogier
- PLoS ONE, Vol. 5, Issue 5
Fitness costs limit influenza A virus hemagglutinin glycosylation as an immune evasion strategy
journal, November 2011
- Das, S. R.; Hensley, S. E.; David, A.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 51
A Phylogeny-Based Global Nomenclature System and Automated Annotation Tool for H1 Hemagglutinin Genes from Swine Influenza A Viruses
journal, December 2016
- Anderson, Tavis K.; Macken, Catherine A.; Lewis, Nicola S.
- mSphere, Vol. 1, Issue 6
Bayesian estimation supersedes the t test.
journal, January 2013
- Kruschke, John K.
- Journal of Experimental Psychology: General, Vol. 142, Issue 2
BEAGLE: An Application Programming Interface and High-Performance Computing Library for Statistical Phylogenetics
journal, October 2011
- Ayres, Daniel L.; Darling, Aaron; Zwickl, Derrick J.
- Systematic Biology, Vol. 61, Issue 1
dendextend: an R package for visualizing, adjusting and comparing trees of hierarchical clustering
journal, July 2015
- Galili, Tal
- Bioinformatics, Vol. 31, Issue 22
Emergence of a Novel Swine-Origin Influenza A (H1N1) Virus in Humans
journal, June 2009
- ,
- New England Journal of Medicine, Vol. 360, Issue 25, p. 2605-2615
Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic
journal, June 2009
- Smith, Gavin J. D.; Vijaykrishna, Dhanasekaran; Bahl, Justin
- Nature, Vol. 459, Issue 7250
Optimal Use of Vaccines for Control of Influenza A Virus in Swine
journal, January 2015
- Sandbulte, Matthew; Spickler, Anna; Zaabel, Pamela
- Vaccines, Vol. 3, Issue 1
Bayesian Phylogenetics with BEAUti and the BEAST 1.7
journal, February 2012
- Drummond, Alexei J.; Suchard, Marc A.; Xie, Dong
- Molecular Biology and Evolution, Vol. 29, Issue 8
Effect of Neuraminidase Antibody on hong kong Influenza
journal, March 1973
- Monto, ArnoldS.; Kendal, AlanP.
- The Lancet, Vol. 301, Issue 7804
Relaxed Phylogenetics and Dating with Confidence
journal, March 2006
- Drummond, Alexei J.; Ho, Simon Y. W.; Phillips, Matthew J.
- PLoS Biology, Vol. 4, Issue 5
Influenza A(H3N2) Virus in Swine at Agricultural Fairs and Transmission to Humans, Michigan and Ohio, USA, 2016
journal, September 2017
- Bowman, Andrew S.; Walia, Rasna R.; Nolting, Jacqueline M.
- Emerging Infectious Diseases, Vol. 23, Issue 9
octoFLU: Automated Classification for the Evolutionary Origin of Influenza A Virus Gene Sequences Detected in U.S. Swine
journal, August 2019
- Chang, Jennifer; Anderson, Tavis K.; Zeller, Michael A.
- Microbiology Resource Announcements, Vol. 8, Issue 32
SpreaD3: Interactive Visualization of Spatiotemporal History and Trait Evolutionary Processes
journal, April 2016
- Bielejec, Filip; Baele, Guy; Vrancken, Bram
- Molecular Biology and Evolution, Vol. 33, Issue 8
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
journal, March 2010
- Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P.
- PLoS ONE, Vol. 5, Issue 3
Capsular Sialic Acid of Streptococcus suis Serotype 2 Binds to Swine Influenza Virus and Enhances Bacterial Interactions with Virus-Infected Tracheal Epithelial Cells
journal, September 2013
- Wang, Yingchao; Gagnon, Carl A.; Savard, Christian
- Infection and Immunity, Vol. 81, Issue 12
Influenza A virus vaccines for swine
journal, July 2017
- Vincent, Amy L.; Perez, Daniel R.; Rajao, Daniela
- Veterinary Microbiology, Vol. 206
Molecular evolution of the hemagglutinin and neuraminidase genes of pandemic (H1N1) 2009 influenza viruses in Sendai, Japan, during 2009–2011
journal, September 2013
- Khandaker, Irona; Suzuki, Akira; Kamigaki, Taro
- Virus Genes, Vol. 47, Issue 3
Genetic Reassortment of Avian, Swine, and Human Influenza A Viruses in American Pigs
journal, October 1999
- Zhou, Nan Nan; Senne, Dennis A.; Landgraf, John S.
- Journal of Virology, Vol. 73, Issue 10
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability
journal, January 2013
- Katoh, K.; Standley, D. M.
- Molecular Biology and Evolution, Vol. 30, Issue 4
Balanced Hemagglutinin and Neuraminidase Activities Are Critical for Efficient Replication of Influenza A Virus
journal, July 2000
- Mitnaul, Lyndon J.; Matrosovich, Mikhail N.; Castrucci, Maria R.
- Journal of Virology, Vol. 74, Issue 13
BEAST 2: A Software Platform for Bayesian Evolutionary Analysis
journal, April 2014
- Bouckaert, Remco; Heled, Joseph; Kühnert, Denise
- PLoS Computational Biology, Vol. 10, Issue 4
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014
- Stamatakis, Alexandros
- Bioinformatics, Vol. 30, Issue 9
Not So Different After All: A Comparison of Methods for Detecting Amino Acid Sites Under Selection
journal, February 2005
- Kosakovsky Pond, Sergei L.; Frost, Simon D. W.
- Molecular Biology and Evolution, Vol. 22, Issue 5
Phylodynamics of H1N1/2009 influenza reveals the transition from host adaptation to immune-driven selection
journal, August 2015
- Su, Yvonne C. F.; Bahl, Justin; Joseph, Udayan
- Nature Communications, Vol. 6, Issue 1
Characterization of a newly emerged genetic cluster of H1N1 and H1N2 swine influenza virus in the United States
journal, July 2009
- Vincent, Amy L.; Ma, Wenjun; Lager, Kelly M.
- Virus Genes, Vol. 39, Issue 2
ISU FLUture: a veterinary diagnostic laboratory web-based platform to monitor the temporal genetic patterns of Influenza A virus in swine
journal, November 2018
- Zeller, Michael A.; Anderson, Tavis K.; Walia, Rasna W.
- BMC Bioinformatics, Vol. 19, Issue 1
The Molecular Determinants of Antibody Recognition and Antigenic Drift in the H3 Hemagglutinin of Swine Influenza A Virus
journal, July 2016
- Abente, Eugenio J.; Santos, Jefferson; Lewis, Nicola S.
- Journal of Virology, Vol. 90, Issue 18
Failure of protection and enhanced pneumonia with a US H1N2 swine influenza virus in pigs vaccinated with an inactivated classical swine H1N1 vaccine
journal, January 2008
- Vincent, Amy L.; Lager, Kelly M.; Janke, Bruce H.
- Veterinary Microbiology, Vol. 126, Issue 4
Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: Approximate methods
journal, September 1994
- Yang, Ziheng
- Journal of Molecular Evolution, Vol. 39, Issue 3
Spatial Dynamics of Human-Origin H1 Influenza A Virus in North American Swine
journal, June 2011
- Nelson, Martha I.; Lemey, Philippe; Tan, Yi
- PLoS Pathogens, Vol. 7, Issue 6
Influenza Research Database: An integrated bioinformatics resource for influenza virus research
journal, September 2016
- Zhang, Yun; Aevermann, Brian D.; Anderson, Tavis K.
- Nucleic Acids Research, Vol. 45, Issue D1
Neuraminidase inhibiting antibody responses in pigs differ between influenza A virus N2 lineages and by vaccine type
journal, July 2016
- Sandbulte, Matthew R.; Gauger, Phillip C.; Kitikoon, Pravina
- Vaccine, Vol. 34, Issue 33
Molecular footprints of selective pressure in the neuraminidase gene of currently circulating human influenza subtypes and lineages
journal, September 2018
- Correia, Vanessa; Abecasis, Ana B.; Rebelo-de-Andrade, Helena
- Virology, Vol. 522
Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen)
journal, January 2016
- Rambaut, Andrew; Lam, Tommy T.; Max Carvalho, Luiz
- Virus Evolution, Vol. 2, Issue 1
The genomic evolution of H1 influenza A viruses from swine detected in the United States between 2009 and 2016
journal, August 2017
- Gao, Shibo; Anderson, Tavis K.; Walia, Rasna R.
- Journal of General Virology, Vol. 98, Issue 8
Selective Bottlenecks Shape Evolutionary Pathways Taken during Mammalian Adaptation of a 1918-like Avian Influenza Virus
journal, February 2016
- Moncla, Louise H.; Zhong, Gongxun; Nelson, Chase W.
- Cell Host & Microbe, Vol. 19, Issue 2
Deep Sequencing Reveals Potential Antigenic Variants at Low Frequencies in Influenza A Virus-Infected Humans
journal, April 2016
- Dinis, Jorge M.; Florek, Nicholas W.; Fatola, Omolayo O.
- Journal of Virology, Vol. 90, Issue 7
Estimating Mutation Parameters, Population History and Genealogy Simultaneously From Temporally Spaced Sequence Data
journal, July 2002
- Drummond, Alexei J.; Nicholls, Geoff K.; Rodrigo, Allen G.
- Genetics, Vol. 161, Issue 3
Genomewide Analysis of Reassortment and Evolution of Human Influenza A(H3N2) Viruses Circulating between 1968 and 2011
journal, December 2013
- Westgeest, K. B.; Russell, C. A.; Lin, X.
- Journal of Virology, Vol. 88, Issue 5
Long-term evolution and transmission dynamics of swine influenza A virus
journal, May 2011
- Vijaykrishna, Dhanasekaran; Smith, Gavin J. D.; Pybus, Oliver G.
- Nature, Vol. 473, Issue 7348
Nextstrain: real-time tracking of pathogen evolution
journal, May 2018
- Hadfield, James; Megill, Colin; Bell, Sidney M.
- Bioinformatics, Vol. 34, Issue 23
Complete Genome Sequences of Two Novel Human-Like H3N2 Influenza A Viruses, A/swine/Oklahoma/65980/2017 (H3N2) and A/Swine/Oklahoma/65260/2017 (H3N2), Detected in Swine in the United States
journal, November 2018
- Zeller, Michael A.; Li, Ganwu; Harmon, Karen M.
- Microbiology Resource Announcements, Vol. 7, Issue 20
Sweep Dynamics (SD) plots: Computational identification of selective sweeps to monitor the adaptation of influenza A viruses
journal, January 2018
- Klingen, Thorsten R.; Reimering, Susanne; Loers, Jens
- Scientific Reports, Vol. 8, Issue 1
Evolutionary changes in influenza B are not primarily governed by antibody selection.
journal, May 1990
- Air, G. M.; Gibbs, A. J.; Laver, W. G.
- Proceedings of the National Academy of Sciences, Vol. 87, Issue 10
Hemagglutinin Receptor Binding Avidity Drives Influenza A Virus Antigenic Drift
journal, October 2009
- Hensley, Scott E.; Das, Suman R.; Bailey, Adam L.
- Science, Vol. 326, Issue 5953
Smooth Skyride through a Rough Skyline: Bayesian Coalescent-Based Inference of Population Dynamics
journal, April 2008
- Minin, V. N.; Bloomquist, E. W.; Suchard, M. A.
- Molecular Biology and Evolution, Vol. 25, Issue 7
Intrasubtype Reassortments Cause Adaptive Amino Acid Replacements in H3N2 Influenza Genes
journal, January 2014
- Neverov, Alexey D.; Lezhnina, Ksenia V.; Kondrashov, Alexey S.
- PLoS Genetics, Vol. 10, Issue 1