Continuous Influx of Genetic Material from Host to Virus Populations

Abstract

Many genes of large double-stranded DNA viruses have a cellular origin, suggesting that host-to-virus horizontal transfer (HT) of DNA is recurrent. Yet, the frequency of these transfers has never been assessed in viral populations. Here we used ultra-deep DNA sequencing of 21 baculovirus populations extracted from two moth species to show that a large diversity of moth DNA sequences (n = 86) can integrate into viral genomes during the course of a viral infection. The majority of the 86 different moth DNA sequences are transposable elements (TEs, n = 69) belonging to 10 superfamilies of DNA transposons and three superfamilies of retrotransposons. The remaining 17 sequences are moth sequences of unknown nature. In addition to bona fide DNA transposition, we uncover microhomology-mediated recombination as a mechanism explaining integration of moth sequences into viral genomes. Many sequences integrated multiple times at multiple positions along the viral genome. We detected a total of 27,504 insertions of moth sequences in the 21 viral populations and we calculate that on average, 4.8% of viruses harbor at least one moth sequence in these populations. Despite this substantial proportion, no insertion of moth DNA was maintained in any viral population after 10 successive infection cycles. Hence, there is a constant turnover of host DNA inserted into viral genomes each time the virus infects a moth. Finally, we found that at least 21 of the moth TEs integrated into viral genomes underwent repeated horizontal transfers between various insect species, including some lepidopterans susceptible to baculoviruses. Our results identify host DNA influx as a potent source of genetic diversity in viral populations. They also support a role for baculoviruses as vectors of DNA HT between insects, and call for an evaluation of possible gene or TE spread when using viruses as biopesticides or gene delivery vectors.

Expansion of the Metazoan Virosphere: Progress, Pitfalls, and Prospects

“…If expressed and/or 'domesticated' by the recipient genome, these may be represented at high levels and retain open reading frames (Katzourakis and Gifford 2010;Palatini et al 2017). Conversely, host sequences-especially transposable elements (TEs)-are often incorporated into large DNA viruses and can move freely between hosts and viruses (Gilbert et al 2016). Second, the host can be misassigned if samples contain multiple hosts, either naturally or through contamination.…”

Viral insulin-like peptides activate human insulin and IGF-1 receptor signaling: A paradigm shift for host–microbe interactions

“…While most interactions are nonconsequential, in some cases viruses penetrate host defense barriers, and this may lead to disease through direct tissue damage or as a result of inflammatory or secondary immunological responses (2). Viruses may also manipulate their hosts by expressing host-like proteins (3)(4)(5). These can have immunomodulatory actions (6) or serve as transforming growth factors, as in the case of Simian sarcoma virus-derived platelet-derived growth factor (PDGF, v-sis) (7) and the epidermal and transforming growth factor-like molecules of vaccinia virus (8,9).…”

Evaluating the Probability of CRISPR-based Gene Drive Contaminating Another Species

“…Compared to other DNA sequences, TEs have particular characteristics that allow them to integrate into DNA more frequently, and they can also self-replicate in the new host after HT, so that they are more likely to be noticed.Whether the higher rate observed for HTT than for HGT is only due to the integration and replicative properties of TE is unknown. If viruses are important vectors for HT, the propensity of TE to jump from eukaryote genomes to viruses, and reversely, more frequently than random pieces of DNA (Gilbert et al 2016) may also explain their higher rate of HT. Compared to TE, a gene drive cassette can also insert itself into a host genome, but its integration into DNA may be less likely and its number of copies in a genome should be lower, so that gene drives may transfer horizontally between genomes less frequently than TEs.…”