Influenza A virus reassortment is strain dependent.

RNA viruses can exchange genetic material during coinfection, an interaction that creates novel strains with implications for viral evolution and public health. Influenza A viral genetic exchange can occur when genome segments from distinct strains reassort in coinfected cells. Predicting potential...

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Main Authors: Kishana Y Taylor, Ilechukwu Agu, Ivy José, Sari Mäntynen, A J Campbell, Courtney Mattson, Tsui-Wen Chou, Bin Zhou, David Gresham, Elodie Ghedin, Samuel L Díaz Muñoz
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2023-03-01
Series:PLoS Pathogens
Online Access:https://doi.org/10.1371/journal.ppat.1011155
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author Kishana Y Taylor
Ilechukwu Agu
Ivy José
Sari Mäntynen
A J Campbell
Courtney Mattson
Tsui-Wen Chou
Bin Zhou
David Gresham
Elodie Ghedin
Samuel L Díaz Muñoz
author_facet Kishana Y Taylor
Ilechukwu Agu
Ivy José
Sari Mäntynen
A J Campbell
Courtney Mattson
Tsui-Wen Chou
Bin Zhou
David Gresham
Elodie Ghedin
Samuel L Díaz Muñoz
author_sort Kishana Y Taylor
collection DOAJ
description RNA viruses can exchange genetic material during coinfection, an interaction that creates novel strains with implications for viral evolution and public health. Influenza A viral genetic exchange can occur when genome segments from distinct strains reassort in coinfected cells. Predicting potential genomic reassortment between influenza strains has been a long-standing goal. Experimental coinfection studies have shed light on factors that limit or promote reassortment. However, determining the reassortment potential between diverse Influenza A strains has remained elusive. To address this challenge, we developed a high throughput genotyping approach to quantify reassortment among a diverse panel of human influenza virus strains encompassing two pandemics (swine and avian origin), three specific epidemics, and both circulating human subtypes A/H1N1 and A/H3N2. We found that reassortment frequency (the proportion of reassortants generated) is an emergent property of specific pairs of strains where strain identity is a predictor of reassortment frequency. We detect little evidence that antigenic subtype drives reassortment as intersubtype (H1N1xH3N2) and intrasubtype reassortment frequencies were, on average, similar. Instead, our data suggest that certain strains bias the reassortment frequency up or down, independently of the coinfecting partner. We observe that viral productivity is also an emergent property of coinfections, but uncorrelated to reassortment frequency; thus viral productivity is a separate factor affecting the total number of reassortants produced. Assortment of individual segments among progeny and pairwise segment combinations within progeny generally favored homologous combinations. These outcomes were not related to strain similarity or shared subtype but reassortment frequency was closely correlated to the proportion of both unique genotypes and of progeny with heterologous pairwise segment combinations. We provide experimental evidence that viral genetic exchange is potentially an individual social trait subject to natural selection, which implies the propensity for reassortment is not evenly shared among strains. This study highlights the need for research incorporating diverse strains to discover the traits that shift the reassortment potential to realize the goal of predicting influenza virus evolution resulting from segment exchange.
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spelling doaj.art-aa4330c7fc2841db9856e7a9fea3756d2023-04-12T05:31:31ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742023-03-01193e101115510.1371/journal.ppat.1011155Influenza A virus reassortment is strain dependent.Kishana Y TaylorIlechukwu AguIvy JoséSari MäntynenA J CampbellCourtney MattsonTsui-Wen ChouBin ZhouDavid GreshamElodie GhedinSamuel L Díaz MuñozRNA viruses can exchange genetic material during coinfection, an interaction that creates novel strains with implications for viral evolution and public health. Influenza A viral genetic exchange can occur when genome segments from distinct strains reassort in coinfected cells. Predicting potential genomic reassortment between influenza strains has been a long-standing goal. Experimental coinfection studies have shed light on factors that limit or promote reassortment. However, determining the reassortment potential between diverse Influenza A strains has remained elusive. To address this challenge, we developed a high throughput genotyping approach to quantify reassortment among a diverse panel of human influenza virus strains encompassing two pandemics (swine and avian origin), three specific epidemics, and both circulating human subtypes A/H1N1 and A/H3N2. We found that reassortment frequency (the proportion of reassortants generated) is an emergent property of specific pairs of strains where strain identity is a predictor of reassortment frequency. We detect little evidence that antigenic subtype drives reassortment as intersubtype (H1N1xH3N2) and intrasubtype reassortment frequencies were, on average, similar. Instead, our data suggest that certain strains bias the reassortment frequency up or down, independently of the coinfecting partner. We observe that viral productivity is also an emergent property of coinfections, but uncorrelated to reassortment frequency; thus viral productivity is a separate factor affecting the total number of reassortants produced. Assortment of individual segments among progeny and pairwise segment combinations within progeny generally favored homologous combinations. These outcomes were not related to strain similarity or shared subtype but reassortment frequency was closely correlated to the proportion of both unique genotypes and of progeny with heterologous pairwise segment combinations. We provide experimental evidence that viral genetic exchange is potentially an individual social trait subject to natural selection, which implies the propensity for reassortment is not evenly shared among strains. This study highlights the need for research incorporating diverse strains to discover the traits that shift the reassortment potential to realize the goal of predicting influenza virus evolution resulting from segment exchange.https://doi.org/10.1371/journal.ppat.1011155
spellingShingle Kishana Y Taylor
Ilechukwu Agu
Ivy José
Sari Mäntynen
A J Campbell
Courtney Mattson
Tsui-Wen Chou
Bin Zhou
David Gresham
Elodie Ghedin
Samuel L Díaz Muñoz
Influenza A virus reassortment is strain dependent.
PLoS Pathogens
title Influenza A virus reassortment is strain dependent.
title_full Influenza A virus reassortment is strain dependent.
title_fullStr Influenza A virus reassortment is strain dependent.
title_full_unstemmed Influenza A virus reassortment is strain dependent.
title_short Influenza A virus reassortment is strain dependent.
title_sort influenza a virus reassortment is strain dependent
url https://doi.org/10.1371/journal.ppat.1011155
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