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Co-infection of chickens with H9N2 and H7N9 avian influenza viruses leads to emergence of reassortant H9N9 virus with increased fitness for poultry and enhanced zoonotic potential

View ORCID ProfileSushant Bhat, View ORCID ProfileJoe James, Jean-Remy Sadeyen, Sahar Mahmood, Holly J Everest, View ORCID ProfilePengxiang Chang, Sarah Walsh, Alexander MP Byrne, Benjamin Mollett, Fabian Lean, View ORCID ProfileJoshua E. Sealy, View ORCID ProfileHolly Shelton, View ORCID ProfileMarek J Slomka, View ORCID ProfileSharon M Brookes, View ORCID ProfileMunir Iqbal
doi: https://doi.org/10.1101/2021.04.05.438444
Sushant Bhat
1Avian Influenza Group, The Pirbright Institute, Woking GU24 0NF, UK
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Joe James
2Virology Department, Animal & Plant Health Agency, Weybridge KT15 3NB, UK
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Jean-Remy Sadeyen
1Avian Influenza Group, The Pirbright Institute, Woking GU24 0NF, UK
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Sahar Mahmood
2Virology Department, Animal & Plant Health Agency, Weybridge KT15 3NB, UK
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Holly J Everest
2Virology Department, Animal & Plant Health Agency, Weybridge KT15 3NB, UK
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Pengxiang Chang
1Avian Influenza Group, The Pirbright Institute, Woking GU24 0NF, UK
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  • ORCID record for Pengxiang Chang
Sarah Walsh
2Virology Department, Animal & Plant Health Agency, Weybridge KT15 3NB, UK
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Alexander MP Byrne
2Virology Department, Animal & Plant Health Agency, Weybridge KT15 3NB, UK
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Benjamin Mollett
2Virology Department, Animal & Plant Health Agency, Weybridge KT15 3NB, UK
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Fabian Lean
2Virology Department, Animal & Plant Health Agency, Weybridge KT15 3NB, UK
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Joshua E. Sealy
1Avian Influenza Group, The Pirbright Institute, Woking GU24 0NF, UK
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  • ORCID record for Joshua E. Sealy
Holly Shelton
1Avian Influenza Group, The Pirbright Institute, Woking GU24 0NF, UK
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Marek J Slomka
2Virology Department, Animal & Plant Health Agency, Weybridge KT15 3NB, UK
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Sharon M Brookes
2Virology Department, Animal & Plant Health Agency, Weybridge KT15 3NB, UK
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Munir Iqbal
1Avian Influenza Group, The Pirbright Institute, Woking GU24 0NF, UK
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  • For correspondence: munir.iqbal@pirbright.ac.uk dr.muniriqbal@gmail.com
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SUMMARY

An H7N9 low pathogenicity avian influenza virus (LPAIV) emerged through genetic reassortment between H9N2 and other LPAIVs circulating in birds in China. This virus causes inapparent clinical disease in chickens, but zoonotic transmission results in severe and fatal disease in humans. We evaluated the consequences of reassortment between the H7N9 and the contemporary H9N2 viruses of G1 lineage that are enzootic in poultry across the Indian sub-continent and the Middle East. Co-infection of chickens with these viruses resulted in emergence of novel reassortant H9N9 viruses carrying genes derived from both H9N2 and H7N9 viruses. These reassortant H9N9 viruses showed significantly increased replication fitness, enhanced pathogenicity in chicken embryos and the potential to transmit via contact among ferrets. Our study highlights that the co-circulation of H7N9 and H9N2 viruses could represent a threat for the generation of novel reassortant viruses with greater virulence in poultry and an increased zoonotic potential.

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In Brief H9N2 viruses have a high propensity to reassort with other avian influenza viruses. We found that co-infection of chickens with H9N2 and H7N9 led to the emergence of reassortant viruses including the H9N9 subtype. Some reassortant H9N9 viruses exhibited increased replication fitness, increased pathogenicity in the chicken embryo, greater avidity for human and avian cell receptors, lower pH fusion and contact-transmission to ferrets. This study demonstrated the ability of viruses that already exist in nature to exchange genetic material, highlighting the potential emergence of viruses from these subtypes with increased zoonotic potential. There are nine H9 influenza A subtypes carrying different neuraminidase (NA) genes, including H9N9 viruses, while they are not common they do exist in nature as wildtypes (CDC).

Highlights

  • Co-infection of chickens with H7N9 and H9N2 led to emergence of reassortant H9N9 viruses

  • Reassortant H9N9 viruses had an increased replication rate in avian and human cells

  • Reassortant H9N9 viruses had a lower pH fusion and significantly higher receptor binding to α 2,3 sialoglycans

  • Reassortant H9N9 replicated in ferrets at similar levels compared to H7N9 and transmitted via direct contact

  • Ferrets exposed to reassortant H9N9 by aerosol contact were also found to be seropositive

  • Experimental simulation of events that may occur naturally with circulating viruses has demonstrated the risk of emergence of viruses with increased zoonotic potential.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted April 05, 2021.
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Co-infection of chickens with H9N2 and H7N9 avian influenza viruses leads to emergence of reassortant H9N9 virus with increased fitness for poultry and enhanced zoonotic potential
Sushant Bhat, Joe James, Jean-Remy Sadeyen, Sahar Mahmood, Holly J Everest, Pengxiang Chang, Sarah Walsh, Alexander MP Byrne, Benjamin Mollett, Fabian Lean, Joshua E. Sealy, Holly Shelton, Marek J Slomka, Sharon M Brookes, Munir Iqbal
bioRxiv 2021.04.05.438444; doi: https://doi.org/10.1101/2021.04.05.438444
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Co-infection of chickens with H9N2 and H7N9 avian influenza viruses leads to emergence of reassortant H9N9 virus with increased fitness for poultry and enhanced zoonotic potential
Sushant Bhat, Joe James, Jean-Remy Sadeyen, Sahar Mahmood, Holly J Everest, Pengxiang Chang, Sarah Walsh, Alexander MP Byrne, Benjamin Mollett, Fabian Lean, Joshua E. Sealy, Holly Shelton, Marek J Slomka, Sharon M Brookes, Munir Iqbal
bioRxiv 2021.04.05.438444; doi: https://doi.org/10.1101/2021.04.05.438444

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