Viruses as vectors of horizontal transfer of genetic material in eukaryotes
Introduction
A large number of viral genome fragments have been uncovered in eukaryote genomes during the last ten years. The study of these viral fossils, called ‘endogenous viral elements’ (EVE), yielded important insights into the evolution of extant viral families as well as on the biology of their eukaryotic hosts [1, 2]. The discovery of numerous and diverse EVE also reinforces the idea that viruses may serve as vectors of horizontal transfer (HT) of genetic material in eukaryotes. Horizontal transfer can be defined as the passage of DNA from one organism to another through a mechanism other than reproduction. Eukaryotes repeatedly acquired bacterial genes via HT and such transfers have been instrumental in the adaptation of the receiving taxa to new ecological niches [3, 4]. Few studies have so far searched for genes horizontally transferred between eukaryotes, that is, resulting from eukaryote-to-eukaryote HT [5]. In fact, the majority of eukaryote-to-eukaryote HT characterized so far are transfers of transposable elements (TE), pieces of DNA that are able to move from one locus to another in the genome of their host. Nearly 3000 cases of HT of TE (HTT) have been reported in plants, animals and fungi [6, 7•]. Although a precise measure of the frequency of HTT is still lacking, several studies suggest that such transfers are pervasive and strongly contributed to the evolution of genome architecture of some eukaryote lineages [7•, 8•, 9•, 10].
One of the key questions regarding HT between eukaryotes is that of the mechanisms underlying these transfers. Unlike prokaryotic cells, eukaryotic cells do not possess any molecular apparatus specifically dedicated to HT. Instead, HT in eukaryotes is thought to be accidental and may be mediated by vectors. Viruses have been proposed as prime candidate vectors because they are infectious and they can be transmitted both horizontally and vertically [10, 11, 12]. A virus-mediated HT can be viewed as the result of two successive steps: (i) acquisition of a host genome fragment by a virus, and (ii) integration of this virus-borne fragment into the genome of another host (Figure 1). Here we highlight recent studies in viral population genomics and paleovirology showing that these two steps can be common, thus giving strong credit to the role of viruses as vectors of HT within eukaryotes.
Section snippets
Can viruses receive and carry a foreign genetic load?
That a host gene can be integrated in a viral genome and persist over many viral replication cycles has been known since the discovery of the src oncogene in the Rous sarcoma virus in the 1970s [13]. Since then, several other viral oncogenes and many other eukaryote genes have been characterized in multiple viruses. For example, a substantial fraction of the genes encoded by large dsDNA viruses (up to 30% in some herpesviruses) have been captured from eukaryotes [14, 15, 16, 17, 18, 19]. Today
Polymorphic host sequence insertions in viral genome populations
To be transferred from one host to another via a virus, a gene or TE does not necessarily need to be fixed or present in high frequency in a viral species. It is thus important to realize that the presence of cellular genes or TE fixed in viral species implies that many host sequences may be regularly introduced in viral genomes with varying consequences on viral fitness. Given the high gene density of viral genomes, many of these insertions are expected to be deleterious and to persist at very
Viral endogenization is rampant
For a virus-mediated HT to be complete, a viral-borne host gene or TE must be transferred from the virus to another host. Such virus-to-host transfer may take place through viral endogenization, whereby any host sequence contained in a viral genome can be co-integrated into the genome of another host (Figure 1). It has long been known that endogenization of retroviruses and pararetroviruses has been rampant and is still ongoing in vertebrates and plants, respectively [34, 35]. More recently, a
Virus-mediated horizontal transfer without endogenization
Endogenization may not be the only way through which viral-borne host sequences can be integrated back into a host genome. Experimental evidence suggests that when the viral-borne sequence is sufficiently similar to a sequence present in the receiving host, gene exchange between the virus and the host can occur via homologous recombination at a measurable frequency [49]. In principle, direct transposition of TE from virus to host is also possible in the absence of endogenization (Figure 1).
Conclusion
A strong body of evidence accumulates showing that the flux of genetic material from host to virus and from virus to host is rampant in at least some host–virus systems. Although these observations support the role of viruses as vectors of HT between eukaryotes, direct proofs of such virus-mediated transfers are still scarce. Perhaps the closest evidence to such a direct proof is the discovery of hymenopteran genes transferred into the genome of lepidopterans via bracoviruses [56••]. In this
Conflict of interest
We wish to confirm that there are no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome.
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgment
This work was supported by a grant from Agence Nationale de la Recherche to CG (ANR-15-CE32-0011-01 TransVir).
References (78)
Functional and ecological impacts of horizontal gene transfer in eukaryotes
Curr Opin Genet Dev
(2009)Retroviral oncogenes: a historical primer
Nat Rev Cancer
(2012)- et al.
Gene acquisition convergence between entomopoxviruses and baculoviruses
Viruses
(2015) - et al.
DNA transposons have colonized the genome of the giant virus Pandoravirus salinus
BMC Biol
(2015) - et al.
RNAs from two independently isolated defective interfering particles of Sindbis virus contain a cellular tRNA sequence at their 5′ ends
Proc Natl Acad Sci U S A
(1983) - et al.
Increased viral pathogenicity after insertion of a 28S ribosomal RNA sequence into the haemagglutinin gene of an influenza virus
Nature
(1989) - et al.
Analysis of the human immunodeficiency virus-1 RNA packageome
RNA
(2016) - et al.
Host RNAs, including transposons, are encapsidated by a eukaryotic single-stranded RNA virus
Proc Natl Acad Sci U S A
(2012) - et al.
Insertion of cellular NEDD8 coding sequences in a pestivirus
Virology
(2000) - et al.
Insertion of a bovine SMT3B gene in NS4B and duplication of NS3 in a bovine viral diarrhea virus genome correlate with the cytopathogenicity of the virus
Virus Res
(1998)
Cellular sequences in pestivirus genomes encoding gamma-aminobutyric acid (A) receptor-associated protein and Golgi-associated ATPase enhancer of 16 kilodaltons
J Virol
Horizontal gene transfer from human host to HIV-1 reverse transcriptase confers drug resistance and partly compensates for replication deficits
Virology
Augmentation of human immunodeficiency virus type 1 subtype E (CRF01_AE) multiple-drug resistance by insertion of a foreign 11-amino-acid fragment into the reverse transcriptase
J Virol
Endogenous viruses: insights into viral evolution and impact on host biology
Nat Rev Genet
Endogenous viral elements in animal genomes
PLOS Genet
Horizontal gene transfer in the acquisition of novel traits by metazoans
Proc Biol Sci
Horizontal gene transfer: building the web of life
Nat Rev Genet
HTT-DB: horizontally transferred transposable elements database
Bioinformatics
Massive horizontal transfer of transposable elements in insects
Proc Natl Acad Sci
Widespread and frequent horizontal transfers of transposable elements in plants
Genome Res
VHICA, a new method to discriminate between vertical and horizontal transposon transfer: application to the mariner family within Drosophila
Mol Biol Evol
Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution
Trends Ecol Evol
Revisiting horizontal transfer of transposable elements in Drosophila
Hered Edinb
Comparative analysis estimates the relative frequencies of co-divergence and cross-species transmission within viral families
PLOS Pathog
Identification of new herpesvirus gene homologs in the human genome
Genome Res
The evolutionary biology of poxviruses
Infect Genet Evol
In-depth study of Mollivirus sibericum, a new 30,000-y-old giant virus infecting Acanthamoeba
Proc Natl Acad Sci U S A
Giant viruses, giant chimeras: the multiple evolutionary histories of Mimivirus genes
BMC Evol Biol
Giant viruses with an expanded complement of translation system components
Science
Host-related immunomodulators encoded by poxviruses and herpesviruses
Curr Opin Microbiol
Poxviruses as possible vectors for horizontal transfer of retroposons from reptiles to mammals
Proc Natl Acad Sci U S A
Complete genome sequence of invertebrate iridescent virus 22 isolated from a blackfly larva
J Gen Virol
Arboviral bottlenecks and challenges to maintaining diversity and fitness during mosquito transmission
Viruses
A virus mutant with an insertion of a copia-like transposable element
Nature
Acquisition of host cell DNA sequences by baculoviruses: relationship between host DNA insertions and FP mutants of Autographa californica and Galleria mellonella nuclear polyhedrosis viruses
J Virol
TCl4.7: a novel lepidopteran transposon found in Cydia pomonella granulosis virus
Virology
Identification and nucleotide sequence of the regions of Autographa californica nuclear polyhedrosis virus genome carrying insertion elements derived from Spodoptera frugiperda
Virology
Poliovirus genome RNA hybridizes specifically to higher eukaryotic rRNAs
Nucleic Acids Res
Continuous influx of genetic material from host to virus populations
PLoS Genet
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Current address: Laboratoire Evolution, Génomes, Comportement, Écologie, UMR 9191 CNRS, UMR 247 IRD, Université Paris-Sud, 91198 Gif-sur-Yvette, France.