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LINE-1 retrotransposons facilitate horizontal gene transfer into poxviruses

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 develop...

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Autores principales: Rahman, M Julhasur, Haller, Sherry L, Stoian, Ana MM, Li, Jie, Brennan, Greg, Rothenburg, Stefan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9578709/
https://www.ncbi.nlm.nih.gov/pubmed/36069678
http://dx.doi.org/10.7554/eLife.63327
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author Rahman, M Julhasur
Haller, Sherry L
Stoian, Ana MM
Li, Jie
Brennan, Greg
Rothenburg, Stefan
author_facet Rahman, M Julhasur
Haller, Sherry L
Stoian, Ana MM
Li, Jie
Brennan, Greg
Rothenburg, Stefan
author_sort Rahman, M Julhasur
collection PubMed
description 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.
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spelling pubmed-95787092022-10-19 LINE-1 retrotransposons facilitate horizontal gene transfer into poxviruses Rahman, M Julhasur Haller, Sherry L Stoian, Ana MM Li, Jie Brennan, Greg Rothenburg, Stefan eLife Microbiology and Infectious Disease 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. eLife Sciences Publications, Ltd 2022-09-07 /pmc/articles/PMC9578709/ /pubmed/36069678 http://dx.doi.org/10.7554/eLife.63327 Text en © 2022, Rahman et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Microbiology and Infectious Disease
Rahman, M Julhasur
Haller, Sherry L
Stoian, Ana MM
Li, Jie
Brennan, Greg
Rothenburg, Stefan
LINE-1 retrotransposons facilitate horizontal gene transfer into poxviruses
title LINE-1 retrotransposons facilitate horizontal gene transfer into poxviruses
title_full LINE-1 retrotransposons facilitate horizontal gene transfer into poxviruses
title_fullStr LINE-1 retrotransposons facilitate horizontal gene transfer into poxviruses
title_full_unstemmed LINE-1 retrotransposons facilitate horizontal gene transfer into poxviruses
title_short LINE-1 retrotransposons facilitate horizontal gene transfer into poxviruses
title_sort line-1 retrotransposons facilitate horizontal gene transfer into poxviruses
topic Microbiology and Infectious Disease
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9578709/
https://www.ncbi.nlm.nih.gov/pubmed/36069678
http://dx.doi.org/10.7554/eLife.63327
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