The Double-Stranded DNA Virosphere as a Modular Hierarchical Network of Gene Sharing.

The Double-Stranded DNA Virosphere as a Modular Hierarchical Network of Gene Sharing.
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DOI:
10.1128/mbio.00978-16
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发表时间:
2016-08-02
期刊:
影响因子:
6.4
通讯作者:
Koonin EV
Koonin EV
中科院分区:
生物学1区
文献类型:
--
作者:
Iranzo J;Krupovic M;Koonin EV

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病毒基因组容易发生广泛的基因丢失、获得和交换,并且不共享通用基因。因此,在病毒进化的大范围研究中,基因和基因组网络分析可以补充传统的系统发育学。我们使用二部网络方法对双链DNA(DsDNA)病毒的基因组进行了详尽的比较分析,发现dsDNA病毒圈中存在一个健壮的层次模块化。二部网络由两类节点组成,其中一类节点,在这种情况下是基因组,通过第二类节点,在这种情况下是基因。这样的网络可以被划分为组合来自两个类的节点的模块。DsDNA病毒的两部分网络包括19个模块,形成5个主要和3个次要的超级模块。在这些模块中,有11个包括尾部噬菌体,反映了这一最大病毒组的多样性。该模块分析定量地验证和提炼了先前提出的非平凡进化关系。一个扩展的超级模块将假定的“超级病毒目”的大型和巨型病毒与各种中等大小的病毒和相关的移动元素结合起来。这个超级模块中的所有病毒都共享一个独特的形态发生工具包,带有一个双糖冻卷主要衣壳蛋白。疱疹病毒和尾随噬菌体组成另一个超级模块,由一组不同的以HK97类主要衣壳蛋白为中心的形态发生蛋白结合在一起。这两个超级模块一起覆盖了目前已知的绝大多数dsDNA病毒。我们正式确定了一组14个病毒标志基因,这些基因组成了网络的枢纽,并解释了大部分模块间的连接。病毒和相关的可移动遗传元件是地球上的主要生物实体,但对它们的进化和分类还没有充分了解。关键原因是病毒进化速度高,不仅涉及序列变化,还涉及广泛的基因丢失、获得和交换。因此,在大规模的病毒进化研究中,传统的系统发育方法适用性有限,必须辅之以基因和基因组网络分析。我们应用了这种分析的最先进的方法来揭示双链DNA病毒基因组中强大的层次模块化。一些已识别的模块结合了感染细菌、古菌和真核生物的高度多样化的病毒,以支持先前关于细胞生命三个领域的病毒之间直接进化关系的假设。我们正式确定了一组14个病毒标志基因,这些基因将基因组网络连接在一起。
Virus genomes are prone to extensive gene loss, gain, and exchange and share no universal genes. Therefore, in a broad-scale study of virus evolution, gene and genome network analyses can complement traditional phylogenetics. We performed an exhaustive comparative analysis of the genomes of double-stranded DNA (dsDNA) viruses by using the bipartite network approach and found a robust hierarchical modularity in the dsDNA virosphere. Bipartite networks consist of two classes of nodes, with nodes in one class, in this case genomes, being connected via nodes of the second class, in this case genes. Such a network can be partitioned into modules that combine nodes from both classes. The bipartite network of dsDNA viruses includes 19 modules that form 5 major and 3 minor supermodules. Of these modules, 11 include tailed bacteriophages, reflecting the diversity of this largest group of viruses. The module analysis quantitatively validates and refines previously proposed nontrivial evolutionary relationships. An expansive supermodule combines the large and giant viruses of the putative order “Megavirales” with diverse moderate-sized viruses and related mobile elements. All viruses in this supermodule share a distinct morphogenetic tool kit with a double jelly roll major capsid protein. Herpesviruses and tailed bacteriophages comprise another supermodule, held together by a distinct set of morphogenetic proteins centered on the HK97-like major capsid protein. Together, these two supermodules cover the great majority of currently known dsDNA viruses. We formally identify a set of 14 viral hallmark genes that comprise the hubs of the network and account for most of the intermodule connections. Viruses and related mobile genetic elements are the dominant biological entities on earth, but their evolution is not sufficiently understood and their classification is not adequately developed. The key reason is the characteristic high rate of virus evolution that involves not only sequence change but also extensive gene loss, gain, and exchange. Therefore, in the study of virus evolution on a large scale, traditional phylogenetic approaches have limited applicability and have to be complemented by gene and genome network analyses. We applied state-of-the art methods of such analysis to reveal robust hierarchical modularity in the genomes of double-stranded DNA viruses. Some of the identified modules combine highly diverse viruses infecting bacteria, archaea, and eukaryotes, in support of previous hypotheses on direct evolutionary relationships between viruses from the three domains of cellular life. We formally identify a set of 14 viral hallmark genes that hold together the genomic network.