Department of Ecology, University of Innsbruck, Technikerstrasse 25, A-6020, Innsbruck, Austria.
Microbiome. 2021 Jan 12;9(1):13. doi: 10.1186/s40168-020-00956-0.
Polintons are large mobile genetic elements found in the genomes of eukaryotic organisms that are considered the ancient ancestors of most eukaryotic dsDNA viruses. Originally considered as transposons, they have been found to encode virus capsid genes, suggesting they may actually be integrated viruses; however, an extracellular form has yet to be detected. Recently, circa 25 Polinton-like viruses have been discovered in environmental metagenomes and algal genomes, which shared distantly related genes to both Polintons and virophages (Lavidaviridae). These entities could be the first members of a major class of ancient eukaryotic viruses; however, owing to the lack of available genomes for analysis, information on their global diversity, evolutionary relationships, eukaryotic hosts, and status as free virus particles is limited.
Here, we analysed the metaviromes of an alpine lake to show that Polinton-like virus genome sequences are abundant in the water column. We identify major capsid protein genes belonging to 82 new Polinton-like viruses and use these to interrogate publicly available metagenomic datasets, identifying 543 genomes and a further 16 integrated into eukaryotic genomes. Using an analysis of shared gene content and major capsid protein phylogeny, we define large groups of Polinton-like viruses and link them to diverse eukaryotic hosts, including a new group of viruses, which possess all the core genes of virophages and infect oomycetes and Chrysophyceae.
Our study increased the number of known Polinton-like viruses by 25-fold, identifying five major new groups of eukaryotic viruses, which until now have been hidden in metagenomic datasets. The large enrichment (> 100-fold) of Polinton-like virus sequences in the virus-sized fraction of this alpine lake and the fact that their viral major capsid proteins are found in eukaryotic host transcriptomes support the hypothesis that Polintons in unicellular eukaryotes are viruses. In summary, our data reveals a diverse assemblage of globally distributed viruses, associated with a wide range of unicellular eukaryotic hosts. We anticipate that the methods we have developed for Polinton-like virus detection and the database of over 20,000 genes we present will allow for continued discovery and analysis of these new viral groups. Video abstract.
多聚核苷酸是真核生物基因组中发现的大型移动遗传元件，被认为是大多数真核双链 DNA 病毒的古老祖先。最初被认为是转座子，现已发现它们可编码病毒衣壳基因，这表明它们实际上可能是整合病毒；然而，尚未检测到细胞外形式。最近，在环境宏基因组和藻类基因组中发现了大约 25 种多聚核苷酸样病毒，它们与多聚核苷酸和噬病毒（Lavidaviridae）都有远缘相关的基因。这些实体可能是一类主要的古老真核病毒的第一批成员；然而，由于缺乏可供分析的基因组，关于它们的全球多样性、进化关系、真核宿主以及作为游离病毒颗粒的状态的信息有限。
在这里，我们分析了高山湖泊的宏病毒组，以显示多聚核苷酸样病毒基因组序列在水柱中丰富。我们鉴定了属于 82 种新多聚核苷酸样病毒的主要衣壳蛋白基因，并使用这些基因来查询公开的宏基因组数据集，鉴定了 543 个基因组和另外 16 个整合到真核基因组中。通过共享基因内容和主要衣壳蛋白系统发育的分析，我们定义了多聚核苷酸样病毒的大群组，并将它们与包括新病毒组在内的各种真核宿主联系起来，该病毒组具有噬病毒的所有核心基因，并感染卵菌纲和金藻门。
我们的研究将已知的多聚核苷酸样病毒数量增加了 25 倍，鉴定了 5 个主要的新真核病毒群，这些病毒群直到现在一直隐藏在宏基因组数据集中。在高山湖泊的病毒大小部分中，多聚核苷酸样病毒序列的大量富集（>100 倍）以及它们的病毒主要衣壳蛋白存在于真核宿主转录组中，支持了这样的假设，即单细胞真核生物中的多聚核苷酸是病毒。总之，我们的数据揭示了一组多样化的全球分布的病毒，与广泛的单细胞真核宿主相关。我们预计，我们开发的多聚核苷酸样病毒检测方法和我们提供的超过 20,000 个基因的数据库将允许对这些新病毒群进行持续的发现和分析。视频摘要。
