Influenza A Virus Transmission Bottlenecks Are Defined by Infection Route and Recipient Host

Despite its global relevance, our understanding of how influenza A virus transmission impacts the overall population dynamics of this RNA virus remains incomplete. To define this dynamic, we inserted neutral barcodes into the influenza A virus genome to generate a population of viruses that can be i...

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Published inCell host & microbe Vol. 16; no. 5; pp. 691 - 700
Main Authors Varble, Andrew, Albrecht, Randy A., Backes, Simone, Crumiller, Marshall, Bouvier, Nicole M., Sachs, David, García-Sastre, Adolfo, tenOever, Benjamin R.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 12.11.2014
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Abstract Despite its global relevance, our understanding of how influenza A virus transmission impacts the overall population dynamics of this RNA virus remains incomplete. To define this dynamic, we inserted neutral barcodes into the influenza A virus genome to generate a population of viruses that can be individually tracked during transmission events. We find that physiological bottlenecks differ dramatically based on the infection route and level of adaptation required for efficient replication. Strong genetic pressures are responsible for bottlenecks during adaptation across different host species, whereas transmission between susceptible hosts results in bottlenecks that are not genetically driven and occur at the level of the recipient. Additionally, the infection route significantly influences the bottleneck stringency, with aerosol transmission imposing greater selection than direct contact. These transmission constraints have implications in understanding the global migration of virus populations and provide a clearer perspective on the emergence of pandemic strains. [Display omitted] •Influenza A virus transmission involves sequence-dependent and -independent bottlenecks•The transmission route affects bottleneck stringency and initial virus population diversity•Virus population selection during transmission occurs at the level of recipient The biology of virus transmission impacts geographical spread and genetic diversity. By examining influenza A virus populations during different transmission events, Varble et al. find that bottlenecks differ based on the level of adaptation required for virus replication and the infection route.
AbstractList Despite its global relevance, our understanding of how influenza A virus transmission impacts the overall population dynamics of this RNA virus remains incomplete. To define this dynamic, we inserted neutral barcodes into the influenza A virus genome to generate a population of viruses that can be individually tracked during transmission events. We find that physiological bottlenecks differ dramatically based on the infection route and level of adaptation required for efficient replication. Strong genetic pressures are responsible for bottlenecks during adaptation across different host species, whereas transmission between susceptible hosts results in bottlenecks that are not genetically driven and occur at the level of the recipient. Additionally, the infection route significantly influences the bottleneck stringency, with aerosol transmission imposing greater selection than direct contact. These transmission constraints have implications in understanding the global migration of virus populations and provide a clearer perspective on the emergence of pandemic strains.Despite its global relevance, our understanding of how influenza A virus transmission impacts the overall population dynamics of this RNA virus remains incomplete. To define this dynamic, we inserted neutral barcodes into the influenza A virus genome to generate a population of viruses that can be individually tracked during transmission events. We find that physiological bottlenecks differ dramatically based on the infection route and level of adaptation required for efficient replication. Strong genetic pressures are responsible for bottlenecks during adaptation across different host species, whereas transmission between susceptible hosts results in bottlenecks that are not genetically driven and occur at the level of the recipient. Additionally, the infection route significantly influences the bottleneck stringency, with aerosol transmission imposing greater selection than direct contact. These transmission constraints have implications in understanding the global migration of virus populations and provide a clearer perspective on the emergence of pandemic strains.
Despite its global relevance, our understanding of how influenza A virus transmission impacts the overall population dynamics of this RNA virus remains incomplete. To define this dynamic, we inserted neutral barcodes into the influenza A virus genome to generate a population of viruses that can be individually tracked during transmission events. We find that physiological bottlenecks differ dramatically based on the infection route and level of adaptation required for efficient replication. Strong genetic pressures are responsible for bottlenecks during adaptation across different host species, whereas transmission between susceptible hosts results in bottlenecks that are not genetically driven and occur at the level of the recipient. Additionally, the infection route significantly influences the bottleneck stringency, with aerosol transmission imposing greater selection than direct contact. These transmission constraints have implications in understanding the global migration of virus populations and provide a clearer perspective on the emergence of pandemic strains. [Display omitted] •Influenza A virus transmission involves sequence-dependent and -independent bottlenecks•The transmission route affects bottleneck stringency and initial virus population diversity•Virus population selection during transmission occurs at the level of recipient The biology of virus transmission impacts geographical spread and genetic diversity. By examining influenza A virus populations during different transmission events, Varble et al. find that bottlenecks differ based on the level of adaptation required for virus replication and the infection route.
Despite its global relevance, our understanding of how influenza A virus transmission impacts the overall population dynamics of this RNA virus remains incomplete. To define this dynamic, we inserted neutral barcodes into the influenza A virus genome to generate a population of viruses that can be individually tracked during transmission events. We find that physiological bottlenecks differ dramatically based on the infection route and level of adaptation required for efficient replication. Strong genetic pressures are responsible for bottlenecks during adaptation across different host species, whereas transmission between susceptible hosts results in bottlenecks that are not genetically driven and occur at the level of the recipient. Additionally, the infection route significantly influences the bottleneck stringency, with aerosol transmission imposing greater selection than direct contact. These transmission constraints have implications in understanding the global migration of virus populations and provide a clearer perspective into the emergence of pandemic strains.
Despite its global relevance, our understanding of how influenza A virus transmission impacts the overall population dynamics of this RNA virus remains incomplete. To define this dynamic, we inserted neutral barcodes into the influenza A virus genome to generate a population of viruses that can be individually tracked during transmission events. We find that physiological bottlenecks differ dramatically based on the infection route and level of adaptation required for efficient replication. Strong genetic pressures are responsible for bottlenecks during adaptation across different host species, whereas transmission between susceptible hosts results in bottlenecks that are not genetically driven and occur at the level of the recipient. Additionally, the infection route significantly influences the bottleneck stringency, with aerosol transmission imposing greater selection than direct contact. These transmission constraints have implications in understanding the global migration of virus populations and provide a clearer perspective on the emergence of pandemic strains.
Author Albrecht, Randy A.
García-Sastre, Adolfo
Crumiller, Marshall
Backes, Simone
Sachs, David
tenOever, Benjamin R.
Bouvier, Nicole M.
Varble, Andrew
AuthorAffiliation 5 Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, New York, 10029 USA
1 Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, New York, 10029 USA
3 The Laboratory of Biophysics, The Rockefeller University, New York, NY, 10065 USA
2 Global Health and Emerging Pathogens Institute, Icahn School of Medicine at Mount Sinai, New York, New York, 10029 USA
4 Department of Medicine, Division of Infectious Diseases, Icahn School of Medicine at Mount Sinai, New York, New York, 10029 USA
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– name: 4 Department of Medicine, Division of Infectious Diseases, Icahn School of Medicine at Mount Sinai, New York, New York, 10029 USA
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Snippet Despite its global relevance, our understanding of how influenza A virus transmission impacts the overall population dynamics of this RNA virus remains...
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SubjectTerms Animals
Cell Line, Tumor
Disease Transmission, Infectious - veterinary
DNA Barcoding, Taxonomic
Dogs
Ferrets
Genome, Viral
Guinea Pigs
High-Throughput Nucleotide Sequencing
Host-Pathogen Interactions
Humans
Influenza A virus - genetics
Influenza A virus - pathogenicity
Influenza, Human - transmission
Madin Darby Canine Kidney Cells
Male
Orthomyxoviridae Infections - transmission
Title Influenza A Virus Transmission Bottlenecks Are Defined by Infection Route and Recipient Host
URI https://dx.doi.org/10.1016/j.chom.2014.09.020
https://www.ncbi.nlm.nih.gov/pubmed/25456074
https://www.proquest.com/docview/1640332293
https://pubmed.ncbi.nlm.nih.gov/PMC4272616
Volume 16
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