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Towards an integrative view of virus phenotypes

Nature Reviews Microbiology volume 20, pages 83–94 (2022)Cite this article

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Abstract

Understanding how phenotypes emerge from genotypes is a foundational goal in biology. As challenging as this task is when considering cellular life, it is further complicated in the case of viruses. During replication, a virus as a discrete entity (the virion) disappears and manifests itself as a metabolic amalgam between the virus and the host (the virocell). Identifying traits that unambiguously constitute a virus’s phenotype is straightforward for the virion, less so for the virocell. Here, we present a framework for categorizing virus phenotypes that encompasses both virion and virocell stages and considers functional and performance traits of viruses in the context of fitness. Such an integrated view of virus phenotype is necessary for comprehensive interpretation of viral genome sequences and will advance our understanding of viral evolution and ecology.

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Fig. 1: Phenotypes and traits during the virus life cycle.
Fig. 2: How the performance trait of burst size may arise from the interactions of multiple functional traits and the environment.
Fig. 3: Phenotypic plasticity of a virus due to temperature.
Fig. 4: Reproduction strategies and pathways of replication inside host cells.

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Acknowledgements

This Review was inspired by discussions at a workshop supported by the US National Science Foundation under grant no. 1736030, and by the Delaware INBRE programme, with a grant from the US National Institute of General Medical Sciences (P20 GM103446) from the US National Institutes of Health and the State of Delaware.

Author information

Authors and Affiliations

  1. School of Biological Sciences, University of Nebraska-Lincoln, Lincoln, NE, USA

    John P. DeLong & Miranda E. Salsbery

  2. Tropical Biological Research Unit, College of Science, University of Baghdad, Baghdad, Iraq

    Maitham A. Al-Sammak

  3. Nebraska Center for Virology, University of Nebraska-Lincoln, Lincoln, NE, USA

    Maitham A. Al-Sammak, Zeina T. Al-Ameeli, David D. Dunigan & James L. Van Etten

  4. Medical Technical Institutes, Middle Technical University, Baghdad, Iraq

    Zeina T. Al-Ameeli

  5. Department of Plant Pathology, University of Nebraska-Lincoln, Lincoln, NE, USA

    David D. Dunigan & James L. Van Etten

  6. Department of Oceanography, University of Hawaiʻi at Mānoa, Honolulu, HI, USA

    Kyle F. Edwards, Christopher R. Schvarcz & Grieg F. Steward

  7. Department of Plant and Soil Sciences, University of Delaware, Newark, DE, USA

    Jeffry J. Fuhrmann, Kona Haramoto, Amelia O. Harrison, Shawn W. Polson & K. Eric Wommack

  8. Department of Biological Sciences, University of Delaware, Newark, DE, USA

    Jeffry J. Fuhrmann, Jason P. Gleghorn, Hanqun Li, Shawn W. Polson & K. Eric Wommack

  9. Department of Biomedical Engineering, University of Delaware, Newark, DE, USA

    Jason P. Gleghorn & Jasmine Shirazi

  10. Delaware Biotechnology Institute, University of Delaware, Newark, DE, USA

    Hanqun Li, Kona Haramoto, Amelia O. Harrison, Ryan M. Moore, Shawn W. Polson, Barbra D. Ferrell & K. Eric Wommack

  11. Department of Biology and Marine Biology, Roger Williams University, Bristol, RI, USA

    Marcia F. Marston

  12. Center for Bioinformatics and Computational Biology, University of Delaware, Newark, DE, USA

    Ryan M. Moore, Shawn W. Polson & Barbra D. Ferrell

Authors
  1. John P. DeLong
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  2. Maitham A. Al-Sammak
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  3. Zeina T. Al-Ameeli
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  4. David D. Dunigan
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  5. Kyle F. Edwards
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  6. Jeffry J. Fuhrmann
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  7. Jason P. Gleghorn
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  8. Hanqun Li
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  9. Kona Haramoto
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  10. Amelia O. Harrison
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  11. Marcia F. Marston
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  12. Ryan M. Moore
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  13. Shawn W. Polson
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  14. Barbra D. Ferrell
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  15. Miranda E. Salsbery
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  16. Christopher R. Schvarcz
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  17. Jasmine Shirazi
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  18. Grieg F. Steward
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  19. James L. Van Etten
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  20. K. Eric Wommack
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Contributions

Z.T.A.-A., M.A.A.-S., D.D.D., J.P.D., K.F.E., B.D.F., J.J.F., J.P.G., A.O.H., K.H., H.L., M.F.M., R.M.M., S.W.P., M.E.S., J.S. and K.E.W. researched data for the article, D.D.D., J.P.D., K.F.E., J.P.G., M.F.M., C.R.S. and K.E.W. contributed substantially to discussion of the content, D.D.D., J.P.D., K.F.E., J.J.F., J.P.G., M.F.M., S.W.P., C.R.S., G.F.S., J.L.V.E. and K.E.W. wrote the manuscript and D.D.D., J.P.D., K.F.E., J.J.F., J.P.G., M.F.M., S.W.P., C.R.S. and K.E.W. reviewed or edited the manuscript before submission.

Corresponding authors

Correspondence to John P. DeLong or K. Eric Wommack.

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Competing interests

The authors declare no competing interests.

Additional information

Peer review information

Nature Reviews Microbiology thanks H. Ogata, who co-reviewed with H. Endo, S. Roux and the other, anonymous, reviewer for their contribution to the peer review of this work.

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Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Glossary

Reassortment

When genome segments from different infecting viruses combine to form a new viral genome.

Episome

A length of viral genome occurring within a host cell.

T number

The number of sides of a virion.

Segmented

A genome separated into different parts and not physically connected.

Monopartite

Referring to a virus with a non-segmented genome.

Bipartite

Referring to a virus with a genome segmented into two parts.

Multiplicity of infection

The ratio of infecting viruses to hosts.

G+C content

The proportion of all the nucleotides that are guanine or cytosine.

Interferons

Host proteins that can inhibit virus reproduction.

Restriction–modification systems

A tool for breaking up foreign DNA within host cells.

CRISPR–Cas immunity

Genetic sequences that can be used to identify and destroy foreign genomes.

Plasmodesmata

Cytoplasmic connections between neighbouring plant cells.

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DeLong, J.P., Al-Sammak, M.A., Al-Ameeli, Z.T. et al. Towards an integrative view of virus phenotypes. Nat Rev Microbiol 20, 83–94 (2022). https://doi.org/10.1038/s41579-021-00612-w

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