The contrasting phylodynamics of human influenza B viruses

  1. Dhanasekaran Vijaykrishna  Is a corresponding author
  2. Edward C Holmes
  3. Udayan Joseph
  4. Mathieu Fourment
  5. Yvonne C F Su
  6. Rebecca Halpin
  7. Raphael T C Lee
  8. Yi-Mo Deng
  9. Vithiagaran Gunalan
  10. Xudong Lin
  11. Timothy B Stockwell
  12. Nadia B Fedorova
  13. Bin Zhou
  14. Natalie Spirason
  15. Denise Kühnert
  16. Veronika Boskova
  17. Tanja Stadler
  18. Anna-Maria Costa
  19. Dominic E Dwyer
  20. Q Sue Huang
  21. Lance C Jennings
  22. William Rawlinson
  23. Sheena G Sullivan
  24. Aeron C Hurt
  25. Sebastian Maurer-Stroh
  26. David E Wentworth
  27. Gavin J D Smith
  28. Ian Barr
  1. Duke-NUS Graduate Medical School, Singapore
  2. University of Sydney, Australia
  3. J Craig Venter Institute, United States
  4. Agency for Science, Technology and Research, Singapore
  5. Peter Doherty Institute for Infection and Immunity, Australia
  6. Eidgenössische Technische Hochschule Zürich, Switzerland
  7. Royal Children's Hospital, Australia
  8. Westmead Hospital, Australia
  9. National Centre for Biosecurity and Infectious Disease, New Zealand
  10. Canterbury Health Laboratories, New Zealand
  11. Prince of Wales Hospital, Australia
  12. Peter Doherty Institute for Infection and Immunity, United States

Abstract

A complex interplay of viral, host and ecological factors shape the spatio-temporal incidence and evolution of human influenza viruses. Although considerable attention has been paid to influenza A viruses, a lack of equivalent data means that an integrated evolutionary and epidemiological framework has until now not been available for influenza B viruses, despite their significant disease burden. Through the analysis of over 900 full genomes from an epidemiological collection of more than 26,000 strains from Australia and New Zealand, we reveal fundamental differences in the phylodynamics of the two co-circulating lineages of influenza B virus (Victoria and Yamagata), showing that their individual dynamics are determined by a complex relationship between virus transmission, age of infection and receptor binding preference. In sum, this work identifies new factors that are important determinants of influenza B evolution and epidemiology.

Article and author information

Author details

  1. Dhanasekaran Vijaykrishna

    Duke-NUS Graduate Medical School, Singapore, Singapore
    For correspondence
    vijay.dhanasekaran@duke-nus.edu.sg
    Competing interests
    The authors declare that no competing interests exist.
  2. Edward C Holmes

    Marie Bashir Institute for Infectious Diseases and Biosecurity, University of Sydney, Sydney, Australia
    Competing interests
    The authors declare that no competing interests exist.
  3. Udayan Joseph

    Duke-NUS Graduate Medical School, Singapore, Singapore
    Competing interests
    The authors declare that no competing interests exist.
  4. Mathieu Fourment

    Marie Bashir Institute for Infectious Diseases and Biosecurity, University of Sydney, Sydney, Australia
    Competing interests
    The authors declare that no competing interests exist.
  5. Yvonne C F Su

    Duke-NUS Graduate Medical School, Singapore, Singapore
    Competing interests
    The authors declare that no competing interests exist.
  6. Rebecca Halpin

    J Craig Venter Institute, Rockville, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Raphael T C Lee

    Bioinformatics Institute, Agency for Science, Technology and Research, Singapore, Singapore
    Competing interests
    The authors declare that no competing interests exist.
  8. Yi-Mo Deng

    World Health Organisation Collaborating Centre for Reference and Research on Influenza, Peter Doherty Institute for Infection and Immunity, Melbourne, Australia
    Competing interests
    The authors declare that no competing interests exist.
  9. Vithiagaran Gunalan

    Bioinformatics Institute, Agency for Science, Technology and Research, Singapore, Singapore
    Competing interests
    The authors declare that no competing interests exist.
  10. Xudong Lin

    J Craig Venter Institute, Rockville, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Timothy B Stockwell

    J Craig Venter Institute, Rockville, United States
    Competing interests
    The authors declare that no competing interests exist.
  12. Nadia B Fedorova

    J Craig Venter Institute, Rockville, United States
    Competing interests
    The authors declare that no competing interests exist.
  13. Bin Zhou

    J Craig Venter Institute, Rockville, United States
    Competing interests
    The authors declare that no competing interests exist.
  14. Natalie Spirason

    World Health Organisation Collaborating Centre for Reference and Research on Influenza, Peter Doherty Institute for Infection and Immunity, Melbourne, Australia
    Competing interests
    The authors declare that no competing interests exist.
  15. Denise Kühnert

    Department of Environmental Systems Science, Eidgenössische Technische Hochschule Zürich, Zürich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  16. Veronika Boskova

    Department of Biosystems Science and Engineering, Eidgenössische Technische Hochschule Zürich, Basel, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  17. Tanja Stadler

    Department of Biosystems Science and Engineering, Eidgenössische Technische Hochschule Zürich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  18. Anna-Maria Costa

    Royal Children's Hospital, Parkville, Australia
    Competing interests
    The authors declare that no competing interests exist.
  19. Dominic E Dwyer

    Centre for Infectious Diseases and Microbiology Laboratory Services, Westmead Hospital, Westmead, Australia
    Competing interests
    The authors declare that no competing interests exist.
  20. Q Sue Huang

    Institute of Environmental Science and Research, National Centre for Biosecurity and Infectious Disease, Upper Hutt, New Zealand
    Competing interests
    The authors declare that no competing interests exist.
  21. Lance C Jennings

    Microbiology Department, Canterbury Health Laboratories, Christchurch, New Zealand
    Competing interests
    The authors declare that no competing interests exist.
  22. William Rawlinson

    Virology Division, SEALS Microbiology, Prince of Wales Hospital, Sydney, Australia
    Competing interests
    The authors declare that no competing interests exist.
  23. Sheena G Sullivan

    World Health Organisation Collaborating Centre for Reference and Research on Influenza, Peter Doherty Institute for Infection and Immunity, Melbourne, Australia
    Competing interests
    The authors declare that no competing interests exist.
  24. Aeron C Hurt

    World Health Organisation Collaborating Centre for Reference and Research on Influenza, Peter Doherty Institute for Infection and Immunity, Melbourne, Australia
    Competing interests
    The authors declare that no competing interests exist.
  25. Sebastian Maurer-Stroh

    Bioinformatics Institute, Agency for Science, Technology and Research, Singapore, Singapore
    Competing interests
    The authors declare that no competing interests exist.
  26. David E Wentworth

    J Craig Venter Institute, Rockville, United States
    Competing interests
    The authors declare that no competing interests exist.
  27. Gavin J D Smith

    Duke-NUS Graduate Medical School, Singapore, Singapore
    Competing interests
    The authors declare that no competing interests exist.
  28. Ian Barr

    World Health Organisation Collaborating Centre for Reference and Research on Influenza, Peter Doherty Institute for Infection and Immunity, Melbourne, United States
    Competing interests
    The authors declare that no competing interests exist.

Copyright

© 2015, Vijaykrishna et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 6,114
    views
  • 1,048
    downloads
  • 183
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Dhanasekaran Vijaykrishna
  2. Edward C Holmes
  3. Udayan Joseph
  4. Mathieu Fourment
  5. Yvonne C F Su
  6. Rebecca Halpin
  7. Raphael T C Lee
  8. Yi-Mo Deng
  9. Vithiagaran Gunalan
  10. Xudong Lin
  11. Timothy B Stockwell
  12. Nadia B Fedorova
  13. Bin Zhou
  14. Natalie Spirason
  15. Denise Kühnert
  16. Veronika Boskova
  17. Tanja Stadler
  18. Anna-Maria Costa
  19. Dominic E Dwyer
  20. Q Sue Huang
  21. Lance C Jennings
  22. William Rawlinson
  23. Sheena G Sullivan
  24. Aeron C Hurt
  25. Sebastian Maurer-Stroh
  26. David E Wentworth
  27. Gavin J D Smith
  28. Ian Barr
(2015)
The contrasting phylodynamics of human influenza B viruses
eLife 4:e05055.
https://doi.org/10.7554/eLife.05055

Share this article

https://doi.org/10.7554/eLife.05055

Further reading

    1. Evolutionary Biology
    Ljiljana Mihajlovic, Bharat Ravi Iyengar ... Yolanda Schaerli
    Research Article

    Gene duplication drives evolution by providing raw material for proteins with novel functions. An influential hypothesis by Ohno (1970) posits that gene duplication helps genes tolerate new mutations and thus facilitates the evolution of new phenotypes. Competing hypotheses argue that deleterious mutations will usually inactivate gene duplicates too rapidly for Ohno’s hypothesis to work. We experimentally tested Ohno’s hypothesis by evolving one or exactly two copies of a gene encoding a fluorescent protein in Escherichia coli through several rounds of mutation and selection. We analyzed the genotypic and phenotypic evolutionary dynamics of the evolving populations through high-throughput DNA sequencing, biochemical assays, and engineering of selected variants. In support of Ohno’s hypothesis, populations carrying two gene copies displayed higher mutational robustness than those carrying a single gene copy. Consequently, the double-copy populations experienced relaxed purifying selection, evolved higher phenotypic and genetic diversity, carried more mutations and accumulated combinations of key beneficial mutations earlier. However, their phenotypic evolution was not accelerated, possibly because one gene copy rapidly became inactivated by deleterious mutations. Our work provides an experimental platform to test models of evolution by gene duplication, and it supports alternatives to Ohno’s hypothesis that point to the importance of gene dosage.

    1. Cell Biology
    2. Evolutionary Biology
    Paul Richard J Yulo, Nicolas Desprat ... Heather L Hendrickson
    Research Article

    Maintenance of rod-shape in bacterial cells depends on the actin-like protein MreB. Deletion of mreB from Pseudomonas fluorescens SBW25 results in viable spherical cells of variable volume and reduced fitness. Using a combination of time-resolved microscopy and biochemical assay of peptidoglycan synthesis, we show that reduced fitness is a consequence of perturbed cell size homeostasis that arises primarily from differential growth of daughter cells. A 1000-generation selection experiment resulted in rapid restoration of fitness with derived cells retaining spherical shape. Mutations in the peptidoglycan synthesis protein Pbp1A were identified as the main route for evolutionary rescue with genetic reconstructions demonstrating causality. Compensatory pbp1A mutations that targeted transpeptidase activity enhanced homogeneity of cell wall synthesis on lateral surfaces and restored cell size homeostasis. Mechanistic explanations require enhanced understanding of why deletion of mreB causes heterogeneity in cell wall synthesis. We conclude by presenting two testable hypotheses, one of which posits that heterogeneity stems from non-functional cell wall synthesis machinery, while the second posits that the machinery is functional, albeit stalled. Overall, our data provide support for the second hypothesis and draw attention to the importance of balance between transpeptidase and glycosyltransferase functions of peptidoglycan building enzymes for cell shape determination.