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The Widespread Occurrence and Potential Biological Roles of Endogenous Viral Elements in Insect Genomes

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The Widespread Occurrence and Potential Biological Roles of Endogenous Viral Elements in Insect Genomes The Widespread Occurrence and Potential Biological Roles of Endogenous Viral Elements in Insect Genomes Carol D. Blair1, Ken E. Olson1 and Mariangela Bonizzoni2* 1Arthropod-borne and Infectious Diseases Laboratory, Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, CO, USA. 2Department of Biology and Biotechnology, University of Pavia, Pavia, Italy. *Correspondence: [email protected] htps://doi.org/10.21775/cimb.034.013 Abstract insect biology, particularly antiviral immunity, and Modern genomic sequencing and bioinformatics suggest directions for future research. approaches have detected numerous examples of DNA sequences derived from DNA and RNA virus genomes integrated into both vertebrate and insect Introduction: defnition of genomes. Retroviruses encode RNA-dependent endogenous viral elements DNA polymerases (reverse transcriptases) and and the surprising discovery of integrases that convert their RNA viral genomes those from non-retroviral RNA into DNA proviruses and facilitate proviral DNA viruses integration into the host genome. Surprisingly, Interactions between viruses and their hosts occur DNA sequences derived from RNA viruses that at many levels. Viruses evolve rapidly through do not encode these enzymes also occur in host genetic drif and/or natural selection and can genomes. Non-retroviral integrated RNA virus infuence the genetic structures of host popula- sequences (NIRVS) occur at relatively high fre- tions, especially if viral infection results in disease quency in the genomes of the arboviral vectors and mortality. A classic example of virus and host Aedes aegypti and Aedes albopictus, are not distrib- co-evolution is the natural experiment initiated uted randomly and possibly contribute to mosquito by the release of highly pathogenic myxoma virus antiviral immunity, suggesting these mosquitoes into the naive Australian wild rabbit population could serve as a model system for unravelling the in 1950, followed by rapid development of resist- function of NIRVS. Here we address the follow- ance in rabbits coincident with natural atenuation ing questions: What drives DNA synthesis from of the virus (Best and Kerr, 2000; Kerr, 2012). the genomes of non-retroviral RNA viruses? How Another mechanism through which viruses afect does integration of virus cDNA into host DNA the genetics of the host is viral genome integra- occur, and what is its biological function (if any)? tion. Integrations of viral nucleic acid sequences We review current knowledge of viral integrations can occur in both somatic and germline cells. in insect genomes, hypothesize mechanisms of Somatic integrations are frequently associated with NIRVS formation and their potential impact on host genome instability (e.g. Chen et al., 2014). Curr. Issues Mol. Biol. (2020) Vol. 34 caister.com/cimb 14 | Blair et al. Additionally, complete viral sequence integration 2013; Ballinger et al., 2014; Olson and Bonizzoni, into host genomes can favour the persistence of the 2017; Palatini et al., 2017). infection (Cohn et al., 2015). If integrations occur Here we describe current knowledge on the in germline cells, they can be inherited by the next origin, widespread occurrence and genomic context generation. Te persistence and outcome of these of EVEs in insect genomes. Additionally, we report integrations in host populations depend on their examples of the infuence of EVEs on both verte- efects on host ftness. If deleterious, integrations brate and insect host physiology and immunity. are likely lost. Alternatively, viral sequences can be functionally adopted by the host and exert benefcial functions (Frank and Feschote, 2017). Integration of genomes from For instance, the product of the murine retrovirus DNA viruses restriction gene, Fv1, protects mice against infec- Polydnaviruses (PDV) provide a well-known exam- tion with murine leukaemia virus (MLV). Fv1 ple of DNA virus integration into insect genomes genes in Mus musculus and other Mus spp. were (Table 2.1A; for a complete, authoritative review derived from the gag genes of ancient endogenous of polydnaviruses and their interactions with their retroviruses, some of which are distantly related insect hosts, see Chapter 8). PDV are recognized to MLV, and protect against other retroviruses, by the International Commitee on Taxonomy of including lentiviruses and spumaviruses (Yap et al., Viruses (ICTV; htps://talk.ictvonline.org/ictv- 2014). A third outcome is found when integrations reports/ictv_9th_report/dsdna-viruses-2011/w/ are in chromosomal locations that are not tran- dsdna_viruses/127/polydnaviridae) as the family scribed or lack regulatory regions. In this case, viral Polydnaviridae, divided into the genera Bracovirus integrations may persist but accumulate mutations (BV) and Ichnovirus (IV), which are associated at the host rate, which is typically much slower with braconid and ichneumonid parasitoid wasps, than that of exogenous viruses. Tese endogenous respectively (Strand and Burke, 2015; Gauthier et viral elements (EVEs) thus represent a magnifying al., 2018). Bracoviruses have been domesticated by lens into the past, allowing researchers to more wasps, and their genomes are integrated as proviral closely examine the evolutionary history of viruses segments dispersed throughout the genome in and virus–host co-evolution (Aiewsakun and Kat- every cell of both female and male wasps (Desjar- sourakis, 2015; Katzourakis, 2017). dins et al., 2008). Tey replicate by producing Integration of genome sequences from DNA defective virus-like particles (VLPs) in the calyx of viruses and retroviruses is a relatively common the wasp ovary. Bracovirus genomes in VLPs con- phenomenon, as evidenced by the abundance sist of multiple, diverse, circular dsDNAs depleted of virus-derived sequences in the genomes of of replication genes, with one DNA molecule per various organisms. For instance, genetic code from VLP. Parasitoid wasps reproduce by depositing their retroviruses constitutes about 8% of the human eggs in or on other insects, which are consumed by genome (Grifths et al., 2001). Genome integra- juvenile stages of the wasp as they develop (Burke tions are essential events in the retrovirus life cycle. et al., 2014). Te defective VLPs are deposited into Because non-retroviral RNA viruses lack coding the wasp’s hemipteran or dipteran host along with for reverse transcriptase, the machinery needed its eggs, their defective genomes migrate to the host for successful conversion to DNA and integration cell nucleus, where they subsequently express viru- into host genomes, their potential to endogenize lence factors that alter host physiology and allow has been considered minimal. However, an increas- the development of wasp progeny (Strand and ing number of studies show genome integrations Burke, 2015; Gauthier et al., 2018). PDVs cannot into both somatic and germline host cells from be transmited horizontally; rather, the integrated non-retroviral RNA viruses, including both proviruses are transmited vertically in wasps. Tran- single-stranded (positive and negative) and double- script studies suggest that BVs evolved from a single stranded RNA viruses. Te acronym non-retroviral whole genome integration of an ancient ancestor integrated RNA virus sequences (NIRVS) has been of the insect virus family Nudiviridae (Bezier et al., proposed to emphasize the unusual viral origin of 2009; Burke and Strand, 2012). Lineages of ichneu- these EVEs (Ballinger et al., 2012; Kondo et al., monid wasps with integrated IVs are polyphyletic Curr. Issues Mol. Biol. (2020) Vol. 34 caister.com/cimb Endogenous Viral Elements in Insect Genomes | 15 and integrated IVs are diverse, suggesting multiple additional unexpected integrations from ISVs were evolutionary integration events (Gauthier et al., detected in wild-caught Aedes and Ochlerotatus 2018). genomes by PCR using favivirus-specifc primers Analyses of a recently discovered endogeniza- (Roiz et al., 2009; Rizzo et al., 2009; Sanchez-Seco tion involving an alphanudivirus and the braconid et al., 2010). wasp Fopius arisanus are shedding light on the Descriptions of RNA virus genome sequence mechanisms of integration. Alphanudiviruses are integrations into insect genomes increased with members of the family Nudiviridae with a single the advent of next-generation sequencing tech- circular dsDNA genome that usually cause virulent nologies and metagenomic analyses in the early infections in insects. Fopius arisanus belongs to the 2000s. Bioinformatics-based identifcation of viral Opiinae subfamily of Braconidae. Wasp species integrations uses BLAST+ in the form of BLASTx in this subfamily usually lack integrations from or tBLASTn (Altschul et al., 1990). Researchers bracoviruses (Burke et al., 2018). Consequently, parse positive BLAST hits using cut-of values of the identifcation of integrated alphanudivirus between 10–3 and 10–6 (Kondo et al., 2019; Whit- sequences in the genome of F. arisanus suggests that feld et al., 2017; ter Horst et al., 2018). Additional this integration is a recent event. Tis event shows criteria (i.e. presence of viral open reading frames that endogenization is accompanied with gene-loss or minimum size restrictions) are applied to further in the viral genome, and that changes in its archi- reduce false positive results that occur primarily tecture occur before expression of the endogenized due to low-complexity reads with short tandem virus genes falls under the control of the wasp repeats or
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