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Incomplete influenza A virus genomes occur frequently but are readily complemented during localized viral spread

Author

Listed:
  • Nathan T. Jacobs

    (Emory University School of Medicine)

  • Nina O. Onuoha

    (Emory University School of Medicine)

  • Alice Antia

    (Emory University School of Medicine)

  • John Steel

    (Emory University School of Medicine
    Influenza Division, Centers for Disease Control and Prevention)

  • Rustom Antia

    (Emory University)

  • Anice C. Lowen

    (Emory University School of Medicine
    Emory University School of Medicine)

Abstract

Segmentation of viral genomes into multiple RNAs creates the potential for replication of incomplete viral genomes (IVGs). Here we use a single-cell approach to quantify influenza A virus IVGs and examine their fitness implications. We find that each segment of influenza A/Panama/2007/99 (H3N2) virus has a 58% probability of being replicated in a cell infected with a single virion. Theoretical methods predict that IVGs carry high costs in a well-mixed system, as 3.6 virions are required for replication of a full genome. Spatial structure is predicted to mitigate these costs, however, and experimental manipulations of spatial structure indicate that local spread facilitates complementation. A virus entirely dependent on co-infection was used to assess relevance of IVGs in vivo. This virus grows robustly in guinea pigs, but is less infectious and does not transmit. Thus, co-infection allows IVGs to contribute to within-host spread, but complete genomes may be critical for transmission.

Suggested Citation

  • Nathan T. Jacobs & Nina O. Onuoha & Alice Antia & John Steel & Rustom Antia & Anice C. Lowen, 2019. "Incomplete influenza A virus genomes occur frequently but are readily complemented during localized viral spread," Nature Communications, Nature, vol. 10(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-11428-x
    DOI: 10.1038/s41467-019-11428-x
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    Cited by:

    1. Katherine A. Amato & Luis A. Haddock & Katarina M. Braun & Victoria Meliopoulos & Brandi Livingston & Rebekah Honce & Grace A. Schaack & Emma Boehm & Christina A. Higgins & Gabrielle L. Barry & Katia , 2022. "Influenza A virus undergoes compartmentalized replication in vivo dominated by stochastic bottlenecks," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Ketaki Ganti & Anish Bagga & Silvia Carnaccini & Lucas M. Ferreri & Ginger Geiger & C. Joaquin Caceres & Brittany Seibert & Yonghai Li & Liping Wang & Taeyong Kwon & Yuhao Li & Igor Morozov & Wenjun M, 2022. "Influenza A virus reassortment in mammals gives rise to genetically distinct within-host subpopulations," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    3. Asher Leeks & Stuart A. West & Melanie Ghoul, 2021. "The evolution of cheating in viruses," Nature Communications, Nature, vol. 12(1), pages 1-14, December.

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