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.

中文翻译：

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大型双链 DNA 病毒中的广谱和高频基因组结构变异，包括转座因子

摘要 我们对在大型双链 (ds) DNA 病毒种群中分离的基因组结构变异的多样性和频率的了解是有限的。在这里，我们使用短读长（Illumina）和长读长（PacBio）技术对从甜菜夜蛾（甜菜夜蛾）幼虫中纯化的杆状病毒（Autographa californica 多核多角体病毒 [AcMNPV]）的基因组进行了测序，深度>195,000×。使用依赖于由六个变异调用者在单个短读和长读中检测到的结构变异 (SV) 分层聚类的管道，我们在 AcMNPV 中总共鉴定了 1,141 个 SV，包括 464 个缺失、443 个倒位、160 个重复和 74 个插入. 这些变体被认为是稳健的，不太可能由技术人为造成，因为它们是在至少三个长读取和至少三个短读取中独立检测到的。SV 分布在整个 AcMNPV 基因组中，可能涉及大的基因组区域（平均 30,496 bp）。我们表明，在 AcMNPV 种群中，不少于 39.9% 的基因组携带至少一个 SV，绝大多数 SV (75%) 以非常低的频率 (<0.01%) 分离，并且极少数 SV 在十个复制周期后仍然存在，与大多数 SV 对 AcMNPV 适应性的负面影响一致。使用短读长测序数据集，我们然后显示两种虹彩病毒和一种疱疹病毒的种群也充满了 SV，因为它们包含 426 到 1,102 个 SV，由 52.4-80.1% 的基因组携带。最后，AcMNPV 长读数使我们能够识别 1,757 个转座元件 (TE) 插入，其中 895 个被截断并发生在读数的一端。这进一步支持杆状病毒作为 TE 水平转移的可能载体的作用。总而言之，我们发现 SVs 主要在病毒种群的快速获得和损失动态下进化，代表了大型 dsDNA 病毒生物学中的一个重要特征。