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...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2022-09-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/63327 |
| _version_ | 1811181881927925760 |
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| author | M Julhasur Rahman Sherry L Haller Ana MM Stoian Jie Li Greg Brennan Stefan Rothenburg |
| author_facet | M Julhasur Rahman Sherry L Haller Ana MM Stoian Jie Li Greg Brennan Stefan Rothenburg |
| author_sort | M Julhasur Rahman |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-04-11T09:23:17Z |
| format | Article |
| id | doaj.art-15294a9833ac415b978d011df0890a85 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T09:23:17Z |
| publishDate | 2022-09-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-15294a9833ac415b978d011df0890a852022-12-22T04:32:05ZengeLife Sciences Publications LtdeLife2050-084X2022-09-011110.7554/eLife.63327LINE-1 retrotransposons facilitate horizontal gene transfer into poxvirusesM Julhasur Rahman0Sherry L Haller1Ana MM Stoian2Jie Li3Greg Brennan4https://orcid.org/0000-0002-4339-9045Stefan Rothenburg5https://orcid.org/0000-0002-2525-8230Department of Medial Microbiology and Immunology, School of Medicine, University of California, Davis, Davis, United StatesCenter for Biodefense and Emerging Infectious Diseases, University of Texas Medical Branch, Galveston, United StatesDepartment of Medial Microbiology and Immunology, School of Medicine, University of California, Davis, Davis, United StatesGenome Center, University of California, Davis, Davis, United StatesDepartment of Medial Microbiology and Immunology, School of Medicine, University of California, Davis, Davis, United StatesDepartment of Medial Microbiology and Immunology, School of Medicine, University of California, Davis, Davis, United StatesThere 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.https://elifesciences.org/articles/63327horizontal gene transferLINE-1retrotransposonspoxvirusevolutionPKR |
| spellingShingle | M Julhasur Rahman Sherry L Haller Ana MM Stoian Jie Li Greg Brennan Stefan Rothenburg LINE-1 retrotransposons facilitate horizontal gene transfer into poxviruses eLife horizontal gene transfer LINE-1 retrotransposons poxvirus evolution PKR |
| 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 | horizontal gene transfer LINE-1 retrotransposons poxvirus evolution PKR |
| url | https://elifesciences.org/articles/63327 |
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