LINE-1 retrotransposons facilitate horizontal gene transfer into poxviruses

  1. M Julhasur Rahman
  2. Sherry L Haller
  3. Ana M M Stoian
  4. Jie Li
  5. Greg Brennan
  6. Stefan Rothenburg  Is a corresponding author
  1. University of California, Davis, United States
  2. The University of Texas Medical Branch at Galveston, United States

Abstract

There is ample phylogenetic evidence that many critical virus functions, like immune evasion, evolved by the acquisition of genes from their hosts through horizontal gene transfer (HGT). However, the lack of an experimental system has prevented a mechanistic understanding of this process. We developed a model to elucidate the mechanisms of HGT into vaccinia virus, the prototypic poxvirus. All identified gene capture events showed signatures of long interspersed nuclear element-1 (LINE-1)-mediated retrotransposition, including spliced-out introns, polyadenylated tails, and target site duplications. In one case, the acquired gene integrated together with a polyadenylated host U2 small nuclear RNA. Integrations occurred across the genome, in some cases knocking out essential viral genes. These essential gene knockouts were rescued through a process of complementation by the parent virus followed by non-homologous recombination during serial passaging to generate a single, replication-competent virus. This work links multiple evolutionary mechanisms into one adaptive cascade and identifies host retrotransposons as major drivers for virus evolution.

Data availability

Sequencing data have been deposited in ArrayExpress under accession code E-MTAB-9682.

The following data sets were generated

Article and author information

Author details

  1. M Julhasur Rahman

    Department of Medial Microbiology and Immunology, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Sherry L Haller

    Center for Biodefense and Emerging Infectious Diseases, The University of Texas Medical Branch at Galveston, Galveston, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Ana M M Stoian

    Department of Medial Microbiology and Immunology, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Jie Li

    Genome Center, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Greg Brennan

    Department of Medial Microbiology and Immunology, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4339-9045
  6. Stefan Rothenburg

    Department of Medical Microbiology and Immunology, University of California, Davis, Davis, United States
    For correspondence
    rothenburg@ucdavis.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2525-8230

Funding

National Institute of Allergy and Infectious Diseases (AI146915)

  • Stefan Rothenburg

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Karla Kirkegaard, Stanford University School of Medicine, United States

Version history

  1. Received: September 22, 2020
  2. Preprint posted: October 26, 2020 (view preprint)
  3. Accepted: September 6, 2022
  4. Accepted Manuscript published: September 7, 2022 (version 1)
  5. Version of Record published: October 18, 2022 (version 2)

Copyright

© 2022, Rahman 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.

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  1. M Julhasur Rahman
  2. Sherry L Haller
  3. Ana M M Stoian
  4. Jie Li
  5. Greg Brennan
  6. Stefan Rothenburg
(2022)
LINE-1 retrotransposons facilitate horizontal gene transfer into poxviruses
eLife 11:e63327.
https://doi.org/10.7554/eLife.63327

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https://doi.org/10.7554/eLife.63327