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Endogenous Viruses: Insights Into Viral Evolution and Impact on Host Biology C Endogenous viruses: insights into viral evolution and impact on host biology C. Feschotte, C. Gilbert To cite this version: C. Feschotte, C. Gilbert. Endogenous viruses: insights into viral evolution and impact on host biology. Nature Reviews Genetics, Nature Publishing Group, 2012, 13 (4), pp.283-296. 10.1038/nrg3199. hal-00679842 HAL Id: hal-00679842 https://hal.archives-ouvertes.fr/hal-00679842 Submitted on 16 Mar 2012 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. REVIEWS Endogenous viruses: insights into viral evolution and impact on host biology Cédric Feschotte1 and Clément Gilbert2 Abstract | Recent studies have uncovered myriad viral sequences that are integrated or ‘endogenized’ in the genomes of various eukaryotes. Surprisingly, it appears that not just retroviruses but almost all types of viruses can become endogenous. We review how these genomic ‘fossils’ offer fresh insights into the origin, evolutionary dynamics and structural evolution of viruses, which are giving rise to the burgeoning field of palaeovirology. We also examine the multitude of ways through which endogenous viruses have influenced, for better or worse, the biology of their hosts. We argue that the conflict between hosts and viruses has led to the invention and diversification of molecular arsenals, which, in turn, promote the cellular co-option of endogenous viruses. Horizontally Viruses are the most numerous and diverse genetic expression and domestication into new protein-coding In the context of genetic entities on earth. They are environmentally ubiquitous genes with cellular functions. Although other types of information, horizontal and are capable of infecting organisms from all three invasive, parasitic genetic elements, such as transposable transmission is the transfer domains of life, as well as other viruses1. Through vari- elements, have a similarly broad impact on their host6, of genetic material by means other than sex. ous interactions, viruses have profoundly influenced EVE sequences may have a greater propensity to be co- the evolution of cellular life ever since its origin2,3. In opted for certain regulatory and physiological functions. Vertical transmission addition to the infectious properties of viruses, which Most transposable elements are engaged in a long-term Sexual transmission of enable them to spread horizontally between individuals co-evolutionary relationship with their hosts, pressing genetic material from and across species, many viruses can also become part them to evolve strategies to minimize their deleteri- parent to offspring. of the genetic material of their host species, a process ous impact, which, in some cases, may reach a form of 6,7 Fixation that is called endogenization. Such endogenous viral commensalism or symbiosis . By contrast, most viruses A mutation reaches fixation elements (EVEs)4 result from the chromosomal inte- assume a more destructive parasitic lifestyle, often lead- when it is present in all gration of viral DNA (or DNA copies of viral RNA) in ing to the death of infected cells, which sets them in individuals of a given species. the host germ cells, which allows for vertical transmission an intense and perpetual conflict with their host. This Transposable elements and potential fixation in the host population. Although arms race continuously selects for the emergence of Pieces of DNA (typically endogenization was for a long time thought to be lim- genomic adaptations in viruses to manipulate the host genomic elements) that are ited to retroviruses, recent studies have shown that all cell machinery and to counteract antiviral defences. able to move from one locus major types of eukaryotic viruses can give rise to EVEs. Ironically, as we will see, such viral weaponry often to another, often duplicating themselves in the process. The recent availability of large numbers of eukary- forms the foundation for the subsequent recruitment otic genome sequences, combined with an enhanced of EVEs to cellular functions. bioinformatics ability to detect and date ancient EVEs, has laid the foundation for the emerging field of palaeo- Discoveries of endogenous viruses 1Department of Biology, virology5. After describing the discovery of EVEs, we Retroviruses are the only known eukaryotic viruses University of Texas, Arlington, discuss how this burgeoning area has already generated that require chromosomal integration for successful Texas 76016, USA. 2Université de Poitiers, an important shift in our perception of the evolution- completion of their lifecycle. As such, they encode all UMR CNRS 7267, Ecologie ary origins and dynamics of several notorious groups of of the enzymatic machinery that is necessary to per- et Biologie des Interactions, eukaryotic viruses. form this step autonomously. These properties probably Equipe Ecologie Evolution Another exciting facet of palaeovirology is that it explain why endogenous retroviruses (ERVs) were the Symbiose, France. uncovers how EVEs have contributed to the evolu- first EVEs to be characterized and why they still make e-mails: [email protected]; clement.gilbert@univ- tion of the host genome by introducing genetic vari- up the vast majority of EVEs that are recognized today. poitiers.fr ation and innovation, which we discuss in sections on However, it has been known for some time that other doi:10.1038/nrg3199 mutation of the host genome, influences on host gene viruses can be endogenized. For example, endogenous NATURE REVIEWS | GENETICS VOLUME 13 | APRIL 2012 | 283 © 2012 Macmillan Publishers Limited. All rights reserved REVIEWS Table 1 | EVEs identified in eukaryotic genomes Group/type Family or genus Taxa Number per Refs haploid genome Group I/dsDNA Baculovirus Insects Unknown (hybridization 124 data, no sequencing) Group I/dsDNA Herpesviridae Humans 1 125,126 Group I/dsDNA Nudivirus Parasitic wasps Several 127 Group I/dsDNA Phycodnaviridae Brown algae 1 128,129 Group II/ssDNA Circoviridae Mammals 1 to 2 4,20,130 Group II/ssDNA Geminiviridae Tomentosae (tobacco and 5 to 120 130–132 three other species) Group II/ssDNA Parvoviridae Mammals; shrimp 1 to 3 4,20,89, 133,134 Group III/dsRNA Partitiviridae Plants; arthropods; Protozoa 1 to 4 135 Group III/dsRNA Reovirus Aedes spp. mosquitoes 1 4 Group III/dsRNA Totiviridae Fungi; plants; ticks 1 to 6 16,135,136 Group IV/+ssRNA Dicistroviridae Honeybees 1 137 Group IV/+ssRNA Flaviviridae Medaka fish; mosquitoes 1 to 4 4,21,138, 139 Group IV/+ssRNA Potyviridae Grapes Several 140 Group V/–ssRNA Bornaviridae Vertebrates 1 to 17 4,21,17 Group V/–ssRNA Bunyaviridae Ticks 14 4 Group V/–ssRNA Filoviridae Mammals 1 to 13 4,21,141 Group V/–ssRNA Nyavirus Zebrafish 6 21 Group V/–ssRNA Orthomyxoviridae Ticks 1 4 Group V/–ssRNA Rhabdoviridae Insects (ticks and mosquitoes) 1 to 28 4 Group VI/ssRNA-RT Retroviridae Vertebrates Several hundreds to several 36 hundreds of thousands Group VII/dsDNA-RT Hepadnavirus Passerine birds 15 4,19 Group VII/dsDNA-RT Pararetrovirus Plants A dozen to a thousand 8,11 +, positive sense; –, negative sense; RT, reverse transcriptase. caulimoviruses (also called pararetroviruses) have endogenization has been appreciated. This progress was been identified in plant genomes since the late 1990s8. largely fuelled by the advent of whole-genome sequenc- Like retroviruses, caulimoviruses replicate via reverse ing and bioinformatics, which led to the identification Reverse transcription transcription, and they may have originated from the of dozens of non-retroviral EVEs in various eukary- Synthesis of DNA from fusion of a retrotransposon with an envelope (env)-like otes (TABLE 1). As for caulimoviruses, endogenization an RNA template. gene derived from a distinct virus9,10. Unlike retro­ of these non-retroviral EVEs is thought to result from 14 Retrotransposon viruses, however, plant caulimoviruses possess a double- accidental chromosomal integration events . Little is Mobile intracellular genetic stranded DNA genome, and they do not normally known about the underlying molecular mechanisms, elements that replicate via integrate into the host chromosome11. Accordingly, but several studies have identified sequence signatures reverse transcription of endogenous caulimoviruses are thought to result from at the EVE–host genome junction that point to retropo- an RNA intermediate. fortuitous integration into the genome of germ cells (or sition events, suggesting involvement of the enzymatic Envelope meristematic cell progenitors of germ cells), and they machinery encoded by retrotransposons residing in the 15–17 (Env). A glycoprotein encoded generally correspond to partial viral genomes that are host genome . In addition, it has been shown that by many viruses that binds incapable of further replication11. In rare cases, some of viral DNA can be used to patch double-strand breaks to host receptors located on the integrated caulimoviruses appear to have retained the in the host chromosome by non-homologous end joining18, the cell surface in order to promote viral entry. capacity to produce infectious particles but, intriguingly,
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