Poxviruses capture host genes by LINE-1 retrotransposition
- University of Utah, United States
- University of California, Davis, United States
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.
Article and author information
Author details
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
- Karla Kirkegaard, Stanford University School of Medicine, United States
Publication history
- Received: September 22, 2020
- Preprint posted: October 27, 2020 (view preprint)
- Accepted: September 6, 2022
- Accepted Manuscript published: September 7, 2022 (version 1)
- 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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Poxviruses capture host genes by LINE-1 retrotransposition
eLife 11:e63332.
https://doi.org/10.7554/eLife.63332
Further reading
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- Evolutionary Biology
- Microbiology and Infectious Disease
As long suspected, poxviruses capture host genes through a reverse-transcription process now shown to be mediated by retrotransposons.
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- Evolutionary Biology
The globally invasive mosquito subspecies Aedes aegypti aegypti is an effective vector of human arboviruses, in part because it specializes in biting humans and breeding in human habitats. Recent work suggests that specialization first arose as an adaptation to long, hot dry seasons in the West African Sahel, where Ae. aegypti relies on human-stored water for breeding. Here, we use whole-genome cross-coalescent analysis to date the emergence of human-specialist populationsand thus further probe the climate hypothesis. Importantly, we take advantage of the known migration of specialists out of Africa during the Atlantic Slave Trade to calibrate the coalescent clock and thus obtain a more precise estimate of the older evolutionary event than would otherwise be possible. We find that human-specialist mosquitoes diverged rapidly from ecological generalists approximately 5000 years ago, at the end of the African Humid Period—a time when the Sahara dried and water stored by humans became a uniquely stable, aquatic niche in the Sahel. We also use population genomic analyses to date a previously observed influx of human-specialist alleles into major West African cities. The characteristic length of tracts of human-specialist ancestry present on a generalist genetic background in Kumasi and Ouagadougou suggests the change in behavior occurred during rapid urbanization over the last 20–40 years. Taken together, we show that the timing and ecological context of two previously observed shifts towards human biting in Ae. aegypti differ; climate was likely the original driver, but urbanization has become increasingly important in recent decades.
