LINE-1 retrotransposons facilitate horizontal gene transfer into poxviruses

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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

(2020) Cascade evolution in poxviruses: retrotransposon-mediated host gene capture, complementation and recombination
E-MTAB-9682.

https://www.ebi.ac.uk/arrayexpress/experiments/E-MTAB-9682

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Author details

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.
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.
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.
Jie Li

Genome Center, University of California, Davis, Davis, United States

Competing interests
The authors declare that no competing interests exist.
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.

"This ORCID iD identifies the author of this article:" 0000-0002-4339-9045
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.

"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.

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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.