Abstract

Horizontal gene transfer (HGT) provides a major source of genetic variation. Many viruses, including poxviruses, encode genes with crucial functions directly gained by gene transfer from hosts. The mechanism of transfer to poxvirus genomes is unknown. Using genome analysis and experimental screens of infected cells, we discovered a central role for Long Interspersed Nuclear Element-1 (LINE-1) retrotransposition in HGT to virus genomes. The process recapitulates processed pseudogene generation, but with host messenger RNA directed into virus genomes. Intriguingly, hallmark features of retrotransposition appear to favor virus adaption through rapid duplication of captured host genes on arrival. Our study reveals a previously unrecognized conduit of genetic traffic with fundamental implications for the evolution of many virus classes and their hosts.

Data availability

Sequencing data have been deposited in the NCBI SRA database under project code PRJNA614958.All data generated or analyses during this study are included in the manuscript and supplemental files.

The following data sets were generated

Article and author information

Author details

  1. Sarah M Fixsen

    Department of Human Genetics, University of Utah, Salt Lake City, United States
    Competing interests
    No competing interests declared.
  2. Kelsey R Cone

    Department of Human Genetics, University of Utah, Salt Lake City, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4547-7174
  3. Stephen A Goldstein

    Department of Human Genetics, University of Utah, Salt Lake City, United States
    Competing interests
    No competing interests declared.
  4. Thomas A Sasani

    Department of Human Genetics, University of Utah, Salt Lake City, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2317-1374
  5. Aaron R Quinlan

    Department of Human Genetics, University of Utah, Salt Lake City, United States
    Competing interests
    No competing interests declared.
  6. Stefan Rothenburg

    Department of Medical Microbiology and Immunology, University of California, Davis, Davis, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2525-8230
  7. Nels C Elde

    Department of Human Genetics, University of Utah, Salt Lake City, United States
    For correspondence
    nelde@genetics.utah.edu
    Competing interests
    Nels C Elde, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0426-1377

Funding

National Institutes of Health (R35GM134936)

  • Nels C Elde

National Institutes of Health (T32GM007464)

  • Sarah M Fixsen
  • Thomas A Sasani

National Institutes of Health (T32AI055434)

  • Kelsey R Cone

Burroughs Wellcome Fund (1015462)

  • Nels C Elde

University of Utah (HA and Edna Benning Presidential Endowed Chair)

  • Nels C Elde

National Institutes of Health (R01AI146915)

  • 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 27, 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, Fixsen 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. Sarah M Fixsen
  2. Kelsey R Cone
  3. Stephen A Goldstein
  4. Thomas A Sasani
  5. Aaron R Quinlan
  6. Stefan Rothenburg
  7. Nels C Elde
(2022)
Poxviruses capture host genes by LINE-1 retrotransposition
eLife 11:e63332.
https://doi.org/10.7554/eLife.63332

Share this article

https://doi.org/10.7554/eLife.63332

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