Skip to main content
Top
Published in: Archives of Virology 7/2020

01-07-2020 | Influenza Virus | Original Article

Historical origins and zoonotic potential of avian influenza virus H9N2 in Tunisia revealed by Bayesian analysis and molecular characterization

Authors: Marwa Arbi, Oussema Souiai, Natalia Rego, Imen Larbi, Hugo Naya, Abdeljelil Ghram, Mehdi Houimel

Published in: Archives of Virology | Issue 7/2020

Login to get access

Abstract

During 2009–2012, several outbreaks of avian influenza virus H9N2 were reported in Tunisian poultry. The circulating strains carried in their hemagglutinins the human-like marker 226L, which is known to be important for avian-to-human viral transmission. To investigate the origins and zoonotic potential of the Tunisian H9N2 viruses, five new isolates were identified during 2012–2016 and their whole genomes were sequenced. Bayesian-based phylogeny showed that the HA, NA, M and NP segments belong to the G1-like lineage. The PB1, PB2, PA and NS segments appeared to have undergone multiple intersubtype reassortments and to be only distantly related to all of the Eurasian lineages (G1-like, Y280-like and Korean-like). The spatiotemporal dynamic of virus spread revealed that the H9N2 virus was transferred to Tunisia from the UAE through Asian and European pathways. As indicated by Bayesian analysis of host traits, ducks and terrestrial birds played an important role in virus transmission to Tunisia. The subtype phylodynamics showed that the history of the PB1 and PB2 segments was marked by intersubtype reassortments with H4N6, H10N4 and H2N2 subtypes. Most of these transitions between locations, hosts and subtypes were statistically supported (BF > 3) and not influenced by sampling bias. Evidence of genetic evolution was observed in the predicted amino acid sequences of the viral proteins of recent Tunisian H9N2 viruses, which were characterized by the acquisition of new mutations involved in virus adaptation to avian and mammalian hosts and amantadine resistance. This study is the first comprehensive analysis of the evolutionary history of Tunisian H9N2 viruses and highlights the zoonotic risk associated with their circulation in poultry, indicating the need for continuous surveillance of their molecular evolution.
Appendix
Available only for authorised users
Literature
4.
go back to reference Yoon SW, Webby RJ, Webster RG (2014) Evolution and ecology of influenza A viruses. Curr Top Microbiol Immunol 385:359–375PubMed Yoon SW, Webby RJ, Webster RG (2014) Evolution and ecology of influenza A viruses. Curr Top Microbiol Immunol 385:359–375PubMed
5.
go back to reference Homme PJ, Easterday BC (1970) Avian influenza virus infections. I. Characteristics of influenza A/Turkey/ Wisconsin/1966 virus. Avian Dis 14(1):66–74PubMed Homme PJ, Easterday BC (1970) Avian influenza virus infections. I. Characteristics of influenza A/Turkey/ Wisconsin/1966 virus. Avian Dis 14(1):66–74PubMed
6.
go back to reference Shortridge KF (1992) Pandemic influenza: a zoonosis? Semin Respir Infect 7(1):11–25PubMed Shortridge KF (1992) Pandemic influenza: a zoonosis? Semin Respir Infect 7(1):11–25PubMed
9.
go back to reference Lee CW, Song CS, Lee YJ, Mo IP, Garcia M, Suarez DL, Kim SJ (2000) Sequence analysis of the hemagglutinin gene of H9N2 Korean avian influenza viruses and assessment of the pathogenic potential of isolate MS96. Avian Dis 44:527–535PubMed Lee CW, Song CS, Lee YJ, Mo IP, Garcia M, Suarez DL, Kim SJ (2000) Sequence analysis of the hemagglutinin gene of H9N2 Korean avian influenza viruses and assessment of the pathogenic potential of isolate MS96. Avian Dis 44:527–535PubMed
12.
go back to reference Nagy A, Mettenleiter TC, Abdelwhab EM (2017) A brief summary of the epidemiology and genetic relatedness of avian influenza H9N2 virus in birds and mammals in the Middle East and North Africa. Epidemiol Infect 145:3320–3333PubMed Nagy A, Mettenleiter TC, Abdelwhab EM (2017) A brief summary of the epidemiology and genetic relatedness of avian influenza H9N2 virus in birds and mammals in the Middle East and North Africa. Epidemiol Infect 145:3320–3333PubMed
18.
go back to reference Zhang K, Zhang Z, Yu Z et al (2013) Domestic cats and dogs are susceptible to H9N2 avian influenza virus. Virus Res 175(1):52–57PubMed Zhang K, Zhang Z, Yu Z et al (2013) Domestic cats and dogs are susceptible to H9N2 avian influenza virus. Virus Res 175(1):52–57PubMed
22.
go back to reference Tombari W, Paul M, Bettaieb J, Larbi I, Nsiri J, Elbehi I, Gribaa L, Ghram A (2013) Risk factors and characteristics of low pathogenic avian influenza virus isolated from commercial poultry in Tunisia. PLoS One 8(1):e53524PubMedPubMedCentral Tombari W, Paul M, Bettaieb J, Larbi I, Nsiri J, Elbehi I, Gribaa L, Ghram A (2013) Risk factors and characteristics of low pathogenic avian influenza virus isolated from commercial poultry in Tunisia. PLoS One 8(1):e53524PubMedPubMedCentral
23.
go back to reference Tombari W, Nsiri Larbi I, Guerin JL, Ghram A (2011) Genetic evolution of low pathogenecity H9N2 Avian influenza viruses in Tunisia: acquisition of new mutations. Virol J 8:467PubMedPubMedCentral Tombari W, Nsiri Larbi I, Guerin JL, Ghram A (2011) Genetic evolution of low pathogenecity H9N2 Avian influenza viruses in Tunisia: acquisition of new mutations. Virol J 8:467PubMedPubMedCentral
24.
go back to reference Aouini R, Laamiri N, Ghram A (2016) Novel gene mutations in Tunisian isolate of avian H9N2 influenza virus. J Vet Sci Technol. 8:1 Aouini R, Laamiri N, Ghram A (2016) Novel gene mutations in Tunisian isolate of avian H9N2 influenza virus. J Vet Sci Technol. 8:1
30.
go back to reference Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis for Windows 95/98/NT. Nucleic Acids Symp 41:95–98 Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis for Windows 95/98/NT. Nucleic Acids Symp 41:95–98
31.
go back to reference Guindon S, Gascuel O (2003) A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704PubMed Guindon S, Gascuel O (2003) A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704PubMed
32.
go back to reference Rambaut A, Lam TT, Max Carvalho L, Pybus OG (2016) Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evol 2(1):7 Rambaut A, Lam TT, Max Carvalho L, Pybus OG (2016) Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evol 2(1):7
34.
go back to reference Baele G, Li WLS, Drummond AJ, Suchard MA, Lemey P (2013) Accurate model selection of relaxed molecular clocks in Bayesian phylogenetics. Mol Biol Evol 30(2):239–243PubMed Baele G, Li WLS, Drummond AJ, Suchard MA, Lemey P (2013) Accurate model selection of relaxed molecular clocks in Bayesian phylogenetics. Mol Biol Evol 30(2):239–243PubMed
38.
go back to reference Hicks JT, Dimitrov KM, Afonso CL et al. (2019) Global phylodynamic analysis of avian paramyxovirus-1 provides evidence of inter-host transmission and intercontinental spatial diffusion. BMC Evol Biol 19(108). Hicks JT, Dimitrov KM, Afonso CL et al. (2019) Global phylodynamic analysis of avian paramyxovirus-1 provides evidence of inter-host transmission and intercontinental spatial diffusion. BMC Evol Biol 19(108).
39.
go back to reference DeLano WL (2002) Pymol: an open-source molecular graphics tool. CCP4 Newsl Protein Crystallogr 40:82–92. DeLano WL (2002) Pymol: an open-source molecular graphics tool. CCP4 Newsl Protein Crystallogr 40:82–92.
40.
go back to reference Li C, Yu K, Tian G, Yu D, Liu L, Jing B, Ping J, Chen H (2005) Evolution of H9N2 influenza viruses from domestic poultry in Mainland China. Virology 340(1):70–83PubMed Li C, Yu K, Tian G, Yu D, Liu L, Jing B, Ping J, Chen H (2005) Evolution of H9N2 influenza viruses from domestic poultry in Mainland China. Virology 340(1):70–83PubMed
41.
go back to reference Gabriel G, Abram M, Keiner B, Wagner R, Klenk HD, Stech J (2007) Differential polymerase activity in avian and mammalian cells determines host range of influenza virus. J Virol 81:9601–9604PubMedPubMedCentral Gabriel G, Abram M, Keiner B, Wagner R, Klenk HD, Stech J (2007) Differential polymerase activity in avian and mammalian cells determines host range of influenza virus. J Virol 81:9601–9604PubMedPubMedCentral
42.
go back to reference Hulse-Post DJ, Franks J, Boyd K, Salomon R, Hoffmann E, Yen HL et al (2007) Molecular changes in the polymerase genes (PA and PB1) associated with high pathogenicity of H5N1 influenza virus in mallard ducks. J Virol 81:8515–8524PubMedPubMedCentral Hulse-Post DJ, Franks J, Boyd K, Salomon R, Hoffmann E, Yen HL et al (2007) Molecular changes in the polymerase genes (PA and PB1) associated with high pathogenicity of H5N1 influenza virus in mallard ducks. J Virol 81:8515–8524PubMedPubMedCentral
43.
go back to reference Liu Q, Lu L, Sun Z, Chen GW, Wen Y, Jiang S (2013) Genomic signature and protein sequence analysis of a novel influenza A (H7N9) virus that causes an outbreak in humans in China. Microbes Infect 15:432–439PubMed Liu Q, Lu L, Sun Z, Chen GW, Wen Y, Jiang S (2013) Genomic signature and protein sequence analysis of a novel influenza A (H7N9) virus that causes an outbreak in humans in China. Microbes Infect 15:432–439PubMed
44.
go back to reference Shaw M, Cooper L, Xu X, Thompson W, Krauss S, Guan Y, Zhou N, Klimov A, Cox N, Webster R, Lim W, Shortridge K, Subbarao K (2002) Molecular changes associated with the transmission of avian influenza a H5N1 and H9N2 viruses to humans. J Med Virol 66:107–114PubMed Shaw M, Cooper L, Xu X, Thompson W, Krauss S, Guan Y, Zhou N, Klimov A, Cox N, Webster R, Lim W, Shortridge K, Subbarao K (2002) Molecular changes associated with the transmission of avian influenza a H5N1 and H9N2 viruses to humans. J Med Virol 66:107–114PubMed
47.
go back to reference Ilyushina NA, Govorkova EA, Webster RG (2005) Detection of amantadine-resistant variants among avian influenza viruses isolated in North America and Asia. Virology 341:102–106PubMed Ilyushina NA, Govorkova EA, Webster RG (2005) Detection of amantadine-resistant variants among avian influenza viruses isolated in North America and Asia. Virology 341:102–106PubMed
54.
go back to reference Gao H, Xu G, Sun Y, Qi L, Wang J, Kong W et al (2015) PA-X is a virulence factor in avian H9N2 influenza virus. J Gen Virol 96:2587–2594PubMed Gao H, Xu G, Sun Y, Qi L, Wang J, Kong W et al (2015) PA-X is a virulence factor in avian H9N2 influenza virus. J Gen Virol 96:2587–2594PubMed
61.
go back to reference Jegede A, Fu Q, Berhane Y, Lin M, Kumar A, Guan J (2018) H9N2 avian influenza virus retained low pathogenicity after serial passage in chickens Jegede A, Fu Q, Berhane Y, Lin M, Kumar A, Guan J (2018) H9N2 avian influenza virus retained low pathogenicity after serial passage in chickens
63.
go back to reference Teng Q, Xu D, Shen W et al (2016) A single mutation at position 190 in hemagglutinin enhances binding affinity for human type sialic acid receptor and replication of H9N2 Avian influenza virus in mice. J Virol 90:21 Teng Q, Xu D, Shen W et al (2016) A single mutation at position 190 in hemagglutinin enhances binding affinity for human type sialic acid receptor and replication of H9N2 Avian influenza virus in mice. J Virol 90:21
64.
go back to reference Matrosovich MN, Krauss S, Webster RG (2001) H9N2 influenza A viruses from poultry in Asia have human virus-like receptor specificity. Virology 281:156–162PubMed Matrosovich MN, Krauss S, Webster RG (2001) H9N2 influenza A viruses from poultry in Asia have human virus-like receptor specificity. Virology 281:156–162PubMed
66.
go back to reference Yamaji R, Yamada S, Le MQ et al (2015) Identification of PB2 mutations responsible for the efficient replication of H5N1 influenza viruses in human lung epithelial cells. J Virol 89:7 Yamaji R, Yamada S, Le MQ et al (2015) Identification of PB2 mutations responsible for the efficient replication of H5N1 influenza viruses in human lung epithelial cells. J Virol 89:7
67.
go back to reference Vigerust DJ, Shepherd VL (2007) Virus glycosylation: role in virulence and immune interactions. Trends Microbiol 15:5 Vigerust DJ, Shepherd VL (2007) Virus glycosylation: role in virulence and immune interactions. Trends Microbiol 15:5
68.
go back to reference Sun S, Wang Q, Zhao F, Chen W, Li Z (2011) Glycosylation Site Alteration in the Evolution of Influenza A (H1N1) Viruses. PLoS One 6(7):e22844PubMedPubMedCentral Sun S, Wang Q, Zhao F, Chen W, Li Z (2011) Glycosylation Site Alteration in the Evolution of Influenza A (H1N1) Viruses. PLoS One 6(7):e22844PubMedPubMedCentral
Metadata
Title
Historical origins and zoonotic potential of avian influenza virus H9N2 in Tunisia revealed by Bayesian analysis and molecular characterization
Authors
Marwa Arbi
Oussema Souiai
Natalia Rego
Imen Larbi
Hugo Naya
Abdeljelil Ghram
Mehdi Houimel
Publication date
01-07-2020
Publisher
Springer Vienna
Keyword
Influenza Virus
Published in
Archives of Virology / Issue 7/2020
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-020-04624-4

Other articles of this Issue 7/2020

Archives of Virology 7/2020 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.