Gilbert Clément, Peccoud Jean, Chateigner Aurélien, Moumen Bouziane, Cordaux Richard, Herniou Elisabeth A
UMR CNRS 7267 Ecologie et Biologie des Interactions, Equipe Ecologie Evolution Symbiose, Université de Poitiers, Poitiers, France.
Institut de Recherche sur la Biologie de l'Insecte, UMR CNRS 7261, UFR des Sciences et Techniques, Université François-Rabelais, Tours, France.
PLoS Genet. 2016 Feb 1;12(2):e1005838. doi: 10.1371/journal.pgen.1005838. eCollection 2016 Feb.
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.
许多大型双链DNA病毒的基因都有细胞起源，这表明DNA从宿主到病毒的水平转移（HT）是反复发生的。然而，这些转移的频率从未在病毒群体中得到评估。在这里，我们对从两种蛾类物种中提取的21个杆状病毒群体进行了超深度DNA测序，结果表明，在病毒感染过程中，种类繁多的蛾类DNA序列（n = 86）能够整合到病毒基因组中。这86种不同的蛾类DNA序列中，大多数是转座元件（TEs，n = 69），属于10个DNA转座子超家族和3个逆转座子超家族。其余17个序列是性质未知的蛾类序列。除了真正的DNA转座外，我们还发现微同源性介导的重组是一种解释蛾类序列整合到病毒基因组中的机制。许多序列在病毒基因组的多个位置多次整合。我们在21个病毒群体中总共检测到27504次蛾类序列插入，并且计算得出，在这些群体中，平均有4.8%的病毒至少含有一个蛾类序列。尽管这一比例相当可观，但在连续10个感染周期后，没有任何一个病毒群体中保留有蛾类DNA的插入。因此，每次病毒感染蛾类时，插入病毒基因组的宿主DNA都会不断更新。最后，我们发现至少有21个整合到病毒基因组中的蛾类TEs在包括一些对杆状病毒敏感的鳞翅目昆虫在内的各种昆虫物种之间经历了反复的水平转移。我们的结果确定宿主DNA流入是病毒群体中遗传多样性的一个重要来源。它们还支持杆状病毒作为昆虫之间DNA HT载体的作用，并呼吁在将病毒用作生物杀虫剂或基因传递载体时评估可能的基因或TE传播情况。
