title: A Phylogeny-Based Global Nomenclature System and Automated Annotation Tool for H1 Hemagglutinin Genes from Swine Influenza A Viruses.
abstract: The H1 subtype of influenza A viruses (IAVs) has been circulating in swine since the 1918 human influenza pandemic. Over time, and aided by further introductions from nonswine hosts, swine H1 viruses have diversified into three genetic lineages. Due to limited global data, these H1 lineages were named based on colloquial context, leading to a proliferation of inconsistent regional naming conventions. In this study, we propose rigorous phylogenetic criteria to establish a globally consistent nomenclature of swine H1 virus hemagglutinin (HA) evolution. These criteria applied to a data set of 7,070 H1 HA sequences led to 28 distinct clades as the basis for the nomenclature. We developed and implemented a web-accessible annotation tool that can assign these biologically informative categories to new sequence data. The annotation tool assigned the combined data set of 7,070 H1 sequences to the correct clade more than 99% of the time. Our analyses indicated that 87% of the swine H1 viruses from 2010 to the present had HAs that belonged to 7 contemporary cocirculating clades. Our nomenclature and web-accessible classification tool provide an accurate method for researchers, diagnosticians, and health officials to assign clade designations to HA sequences. The tool can be updated readily to track evolving nomenclature as new clades emerge, ensuring continued relevance. A common global nomenclature facilitates comparisons of IAVs infecting humans and pigs, within and between regions, and can provide insight into the diversity of swine H1 influenza virus and its impact on vaccine strain selection, diagnostic reagents, and test performance, thereby simplifying communication of such data.IMPORTANCEA fundamental goal in the biological sciences is the definition of groups of organisms based on evolutionary history and the naming of those groups. For influenza A viruses (IAVs) in swine, understanding the hemagglutinin (HA) genetic lineage of a circulating strain aids in vaccine antigen selection and allows for inferences about vaccine efficacy. Previous reporting of H1 virus HA in swine relied on colloquial names, frequently with incriminating and stigmatizing geographic toponyms, making comparisons between studies challenging. To overcome this, we developed an adaptable nomenclature using measurable criteria for historical and contemporary evolutionary patterns of H1 global swine IAVs. We also developed a web-accessible tool that classifies viruses according to this nomenclature. This classification system will aid agricultural production and pandemic preparedness through the identification of important changes in swine IAVs and provides terminology enabling discussion of swine IAVs in a common context among animal and human health initiatives.
authors.affiliation: Virus and Prion Research Unit, National Animal Disease Center, USDA-ARS, Ames, Iowa, USA.
authors.forename: Tavis K
authors.identifier: 0000-0002-3138-5535
authors.initials: TK
authors.lastname: Anderson
authors.affiliation: Bioinformatics Institute, University of Auckland, Auckland, New Zealand.
authors.forename: Catherine A
authors.initials: CA
authors.lastname: Macken
authors.affiliation: Department of Zoology, University of Cambridge, Cambridge, United Kingdom.
authors.forename: Nicola S
authors.initials: NS
authors.lastname: Lewis
authors.affiliation: J. Craig Venter Institute, La Jolla, California, USA; Department of Pathology, University of California, San Diego, California, USA.
authors.forename: Richard H
authors.identifier: 0000-0003-1355-892X
authors.initials: RH
authors.lastname: Scheuermann
authors.affiliation: Laboratory of Virology, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium.
authors.forename: Kristien
authors.initials: K
authors.lastname: Van Reeth
authors.affiliation: Animal and Plant Health Agency, Weybridge, United Kingdom.
authors.forename: Ian H
authors.initials: IH
authors.lastname: Brown
authors.affiliation: National Veterinary Services Laboratories, USDA-APHIS, Ames, Iowa, USA.
authors.forename: Sabrina L
authors.initials: SL
authors.lastname: Swenson
authors.affiliation: ANSES, Ploufragan-Plouzané Laboratory, Swine Virology Immunology Unit, Ploufragan, France.
authors.forename: Gaëlle
authors.initials: G
authors.lastname: Simon
authors.affiliation: Division of Transboundary Animal Disease, National Institute of Animal Health, National Agriculture and Food Research Organization, Ibaraki, Japan.
authors.forename: Takehiko
authors.initials: T
authors.lastname: Saito
authors.affiliation: Canadian Food Inspection Agency, National Centre for Foreign Animal Disease, Winnipeg, Manitoba, Canada.
authors.forename: Yohannes
authors.initials: Y
authors.lastname: Berhane
authors.affiliation: Embrapa Swine and Poultry, Animal Health and Genetic Laboratory, Concórdia, SC, Brazil.
authors.forename: Janice
authors.initials: J
authors.lastname: Ciacci-Zanella
authors.affiliation: Instituto de Patobiología, CICVyA INTA, Hurlingham, Buenos Aires, Argentina.
authors.forename: Ariel
authors.initials: A
authors.lastname: Pereda
authors.affiliation: Influenza Division, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, USA.
authors.forename: C Todd
authors.initials: CT
authors.lastname: Davis
authors.affiliation: Influenza Division, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, USA.
authors.forename: Ruben O
authors.initials: RO
authors.lastname: Donis
authors.affiliation: Department of Infectious Diseases, St. Jude Children's Research Hospital, Memphis, Tennessee, USA.
authors.forename: Richard J
authors.initials: RJ
authors.lastname: Webby
authors.affiliation: Virus and Prion Research Unit, National Animal Disease Center, USDA-ARS, Ames, Iowa, USA.
authors.forename: Amy L
authors.initials: AL
authors.lastname: Vincent
keywords: H1N1; H1N2; influenza A virus; molecular epidemiology; nomenclature; swine; virus evolution