1. Evolutionary Biology
  2. Microbiology and Infectious Disease

Poxviruses capture host genes by LINE-1 retrotransposition

  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  Is a corresponding author
  1. University of Utah, United States
  2. University of California, Davis, United States
https://doi.org/10.7554/eLife.63332
Share this article
Cite this article
  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
  2. Download BibTeX
  3. Download .RIS

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.

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.

Metrics

  • 1,987
    views
  • 453
    downloads
  • 20
    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. 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

Categories and tags

Research organisms

Further reading

    1. Microbiology and Infectious Disease

    LINE-1 retrotransposons facilitate horizontal gene transfer into poxviruses

    M Julhasur Rahman, Sherry L Haller ... Stefan Rothenburg
    Research Article Updated

    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 nonhomologous 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.

    1. Evolutionary Biology
    2. Microbiology and Infectious Disease

    Evolution: A life LINE for large viruses

    Eugene V Koonin, Mart Krupovic
    Insight

    As long suspected, poxviruses capture host genes through a reverse-transcription process now shown to be mediated by retrotransposons.

    1. Evolutionary Biology

    The population genetics of convergent adaptation in maize and teosinte is not locally restricted

    Silas Tittes, Anne Lorant ... Jeffrey Ross-Ibarra
    Research Article

    What is the genetic architecture of local adaptation and what is the geographic scale over which it operates? We investigated patterns of local and convergent adaptation in five sympatric population pairs of traditionally cultivated maize and its wild relative teosinte (Zea mays subsp. parviglumis). We found that signatures of local adaptation based on the inference of adaptive fixations and selective sweeps are frequently exclusive to individual populations, more so in teosinte compared to maize. However, for both maize and teosinte, selective sweeps are also frequently shared by several populations, and often between subspecies. We were further able to infer that selective sweeps were shared among populations most often via migration, though sharing via standing variation was also common. Our analyses suggest that teosinte has been a continued source of beneficial alleles for maize, even after domestication, and that maize populations have facilitated adaptation in teosinte by moving beneficial alleles across the landscape. Taken together, our results suggest local adaptation in maize and teosinte has an intermediate geographic scale, one that is larger than individual populations but smaller than the species range.