Abstract
Our knowledge of the diversity and frequency of genomic structural variation segregating in populations of large double-stranded (ds) DNA viruses is limited. Here, we sequenced the genome of a baculovirus (Autographa californica multiple nucleopolyhedrovirus [AcMNPV]) purified from beet armyworm (Spodoptera exigua) larvae at depths >195,000× using both short- (Illumina) and long-read (PacBio) technologies. Using a pipeline relying on hierarchical clustering of structural variants (SVs) detected in individual short- and long-reads by six variant callers, we identified a total of 1,141 SVs in AcMNPV, including 464 deletions, 443 inversions, 160 duplications, and 74 insertions. These variants are considered robust and unlikely to result from technical artifacts because they were independently detected in at least three long reads as well as at least three short reads. SVs are distributed along the entire AcMNPV genome and may involve large genomic regions (30,496 bp on average). We show that no less than 39.9 per cent of genomes carry at least one SV in AcMNPV populations, that the vast majority of SVs (75%) segregate at very low frequency (<0.01%) and that very few SVs persist after ten replication cycles, consistent with a negative impact of most SVs on AcMNPV fitness. Using short-read sequencing datasets, we then show that populations of two iridoviruses and one herpesvirus are also full of SVs, as they contain between 426 and 1,102 SVs carried by 52.4–80.1 per cent of genomes. Finally, AcMNPV long reads allowed us to identify 1,757 transposable elements (TEs) insertions, 895 of which are truncated and occur at one extremity of the reads. This further supports the role of baculoviruses as possible vectors of horizontal transfer of TEs. Altogether, we found that SVs, which evolve mostly under rapid dynamics of gain and loss in viral populations, represent an important feature in the biology of large dsDNA viruses.
Highlights
Estimating the evolutionary potential of viral populations is key to our understanding of how and how fast viruses may evolve in response to new environmental constraints
structural variants (SVs) have been implicated as an important source of viral evolution in several large double-stranded DNA (dsDNA) viruses (Lopez-Ferber et al 2003; Elde et al 2012; Mahiet et al 2012; Chateigner et al 2015; Filee, 2015; Karamitros et al 2018; Sasani et al 2018), the full spectrum and overall frequency of SVs carried by populations of these viruses has never been probed using high-throughput sequencing
We begin tackling this issue by focusing on three invertebrate viruses for which obtaining large quantities of DNA from in vivo infections was possible (AcMNPV, IIV6, and iridescent virus 31 (IIV31)) as well as on one human virus replicated in cell lines (HCMV)
Summary
Estimating the evolutionary potential of viral populations is key to our understanding of how and how fast viruses may evolve in response to new environmental constraints. RNA viruses display high mutation rates, large population sizes, and fast replication dynamics, which all together generate clouds of genetically linked single nucleotide variants that functionally cooperate and collectively contribute to the fitness of the viral population (Lauring and Andino 2010; Acevedo, Brodsky, and Andino 2014). Such extremely high levels of polymorphism allow RNA viruses to rapidly adapt to the various host and cellular environments they may be exposed to (Lauring, Frydman, and Andino 2013; Sanjuan and Domingo-Calap 2016). The majority of these SNPs are at low frequency and likely neutral, a fraction was shown to be under positive selection and involved in rapid adaptation during intra-host evolution (Renzette et al 2013)
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