Re-assessing the diversity of negative strand RNA viruses in insects
Re-assessing the diversity of negative strand RNA viruses in insects
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DOI：
10.1371/journal.ppat.1008224
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发表时间：
2019-12-01
期刊：
影响因子：
6.7
通讯作者：
Drosten, Christian
中科院分区：
文献类型：
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作者：
Kaefer, Simon;Paraskevopoulou, Sofia;Drosten, Christian
作者摘要昆虫病毒的多样性与医学、环境和食品科学相关。我们对昆虫病毒的了解存在很大偏差，因为医学研究主要集中在蚊子和其他一些吸血物种上。虽然昆虫是地球上最多样化的动物群，但大多数昆虫物种仍然完全没有经过病毒检查。在这里，我们基于全转录组搜索了最全面、组成最均匀的昆虫集合中的负链 RNA 病毒。在所有目 1243 种昆虫中，我们发现了 488 个独立的病毒序列，编码 RNA 指导的 RNA 聚合酶，这是 RNA 病毒的特征基因。这些数据大大增加了我们对病毒多样性的了解，并揭示了病毒与昆虫宿主共同进化。然而，我们的结果也提醒人们在宏基因组学时代与病毒发现和分类学分类相关的陷阱。昆虫病毒谱对于公共卫生、兽医、食品生产和生物多样性保护等多种学科都很重要。对人类和牲畜媒介传播疾病的传统兴趣引起了对食血昆虫物种的病毒研究的关注。然而，这些只代表了六足动物（最特殊的动物群）广泛多样性的一小部分。在这里，我们系统地探讨了最大且最具代表性的昆虫转录组样本中负链 RNA 病毒的多样性，这些样本代表了所有 34 个现存六足目和 3 个内颌类以及外类群，总共代表了 1243 个物种。基于隐马尔可夫模型，我们检测到了 488 个与负链 RNA 病毒相似的病毒 RNA 定向 RNA 聚合酶 (RdRp) 序列。这些是在 324 种节肢动物物种的成员中发现的。根据长度、质量和独特性进行选择，留下 234 个序列用于分析，显示与布尼亚病毒目 (n = 86)、节肢病毒目 (n = 54) 和单病毒目 (n = 94) 内的几个目病毒的基因组相似。 61 个病例获得了编码完整的基因组或接近完整的亚基因组组装。根据系统发育拓扑和编码完整基因组的可用性，我们估计需要定义七个科中至少 20 个新病毒属，其中只有两个是单特异性的。当将本研究的序列添加到以前的单特异性谱系时，会出现七个额外的病毒进化枝，可能需要多达七个额外的属。一个长序列可能表明一个新奇的家庭。对于分段病毒，基因组片段之间的共系统发育通常通过纳入本研究中的病毒而得到改善，这表明分段基因组的计算机错误组装很少或不存在。与之前的评估相反，基于假设检验框架中两种不同的共分化分析方法，在主要系统发育谱系中发现了显着的病毒-宿主共分化。尽管已知昆虫病毒谱中增加了这些内容，但我们警告说，由于技术上的不确定性，例如无法证明分段病毒的完整基因组组装的完整性，仅根据基因组信息做出分类决策具有挑战性。
Author summary The diversity of insect viruses is relevant to medical, environmental, and food sciences. Our knowledge of insect viruses is highly biased because medical research has focused on mosquitoes and a few other blood-feeding species. While insects are the most diversified group of animals on the planet, the great majority of all insect species remain completely unexamined for viruses. Here we searched the most comprehensive and most evenly composed collection of insects for negative strand RNA viruses based on full transcriptomes. In 1243 insect species of all orders, we found 488 independent viral sequences encoding an RNA-directed RNA polymerase, a signature gene for RNA viruses. These data add considerably to our knowledge on viral diversity, and reveal that viruses have coevolved with insect hosts. However, our results also provide a reminder of the pitfalls associated with virus discovery and taxonomic classification in the age of metagenomics.The spectrum of viruses in insects is important for subjects as diverse as public health, veterinary medicine, food production, and biodiversity conservation. The traditional interest in vector-borne diseases of humans and livestock has drawn the attention of virus studies to hematophagous insect species. However, these represent only a tiny fraction of the broad diversity of Hexapoda, the most speciose group of animals. Here, we systematically probed the diversity of negative strand RNA viruses in the largest and most representative collection of insect transcriptomes from samples representing all 34 extant orders of Hexapoda and 3 orders of Entognatha, as well as outgroups, altogether representing 1243 species. Based on profile hidden Markov models we detected 488 viral RNA-directed RNA polymerase (RdRp) sequences with similarity to negative strand RNA viruses. These were identified in members of 324 arthropod species. Selection for length, quality, and uniqueness left 234 sequences for analyses, showing similarity to genomes of viruses classified in Bunyavirales (n = 86), Articulavirales (n = 54), and several orders within Haploviricotina (n = 94). Coding-complete genomes or nearly-complete subgenomic assemblies were obtained in 61 cases. Based on phylogenetic topology and the availability of coding-complete genomes we estimate that at least 20 novel viral genera in seven families need to be defined, only two of them monospecific. Seven additional viral clades emerge when adding sequences from the present study to formerly monospecific lineages, potentially requiring up to seven additional genera. One long sequence may indicate a novel family. For segmented viruses, cophylogenies between genome segments were generally improved by the inclusion of viruses from the present study, suggesting that in silico misassembly of segmented genomes is rare or absent. Contrary to previous assessments, significant virus-host codivergence was identified in major phylogenetic lineages based on two different approaches of codivergence analysis in a hypotheses testing framework. In spite of these additions to the known spectrum of viruses in insects, we caution that basing taxonomic decisions on genome information alone is challenging due to technical uncertainties, such as the inability to prove integrity of complete genome assemblies of segmented viruses.