Colson Philippe, Levasseur Anthony, La Scola Bernard, Sharma Vikas, Nasir Arshan, Pontarotti Pierre, Caetano-Anollés Gustavo, Raoult Didier
Aix-Marseille Université, Institut de Recherche pour le Développement (IRD), Assistance Publique - Hôpitaux de Marseille (AP-HM); Microbes, Evolution, Phylogeny and Infection (MEΦI); Institut Hospitalo-Universitaire (IHU) - Méditerranée Infection, Marseille, France.
Centre National de la Recherche Scientifique, Marseille, France.
Front Microbiol. 2018 Nov 27;9:2668. doi: 10.3389/fmicb.2018.02668. eCollection 2018.
Giant viruses of amoebae were discovered in 2003. Since then, their diversity has greatly expanded. They were suggested to form a fourth branch of life, collectively named 'TRUC' (for "Things Resisting Uncompleted Classifications") alongside , , and . Their origin and ancestrality remain controversial. Here, we specify the evolution and definition of giant viruses. Phylogenetic and phenetic analyses of informational gene repertoires of giant viruses and selected bacteria, archaea and eukaryota were performed, including structural phylogenomics based on protein structural domains grouped into 289 universal fold superfamilies (FSFs). Hierarchical clustering analysis was performed based on a binary presence/absence matrix constructed using 727 informational COGs from cellular organisms. The presence/absence of 'universal' FSF domains was used to generate an unrooted maximum parsimony phylogenomic tree. Comparison of the gene content of a giant virus with those of a bacterium, an archaeon, and a eukaryote with small genomes was also performed. Overall, both cladistic analyses based on gene sequences of very central and ancient proteins and on highly conserved protein fold structures as well as phenetic analyses were congruent regarding the delineation of a fourth branch of microbes comprised by giant viruses. Giant viruses appeared as a basal group in the tree of all proteomes. A pangenome and core genome determined for (bacteria), (archaeon), (eukaryote), and Tupanvirus (giant virus) showed a substantial proportion of Tupanvirus genes that overlap with those of the cellular microbes. In addition, a substantial genome mosaicism was observed, with 51, 11, 8, and 0.2% of Tupanvirus genes best matching with viruses, eukaryota, bacteria, and archaea, respectively. Finally, we found that genes themselves may be subject to lateral sequence transfers. In summary, our data highlight the quantum leap between classical and giant viruses. Phylogenetic and phyletic analyses and the study of protein fold superfamilies confirm previous evidence of the existence of a fourth TRUC of life that includes giant viruses, and highlight its ancestrality and mosaicism. They also point out that best evolutionary representations for giant viruses and cellular microorganisms are rhizomes, and that sequence transfers rather than gene transfers have to be considered.
变形虫的巨型病毒于2003年被发现。从那时起，它们的多样性大幅扩展。有人提出它们构成生命的第四个分支，与细菌、古菌和真核生物一起被统称为“TRUC”（“抗拒未完成分类的事物”）。它们的起源和祖先关系仍存在争议。在此，我们明确了巨型病毒的进化和定义。对巨型病毒以及选定的细菌、古菌和真核生物的信息基因库进行了系统发育和表型分析，包括基于蛋白质结构域的结构系统基因组学分析，这些蛋白质结构域被归为289个通用折叠超家族（FSF）。基于使用来自细胞生物的727个信息性直系同源基因簇（COG）构建的二元存在/缺失矩阵进行了层次聚类分析。“通用”FSF结构域的存在/缺失被用于生成一棵无根的最大简约系统基因组树。还对一种巨型病毒与一种细菌、一种古菌以及一种基因组较小的真核生物的基因内容进行了比较。总体而言，基于非常核心和古老蛋白质的基因序列以及高度保守的蛋白质折叠结构的分支分析以及表型分析，在由巨型病毒构成的微生物第四个分支的划分方面是一致的。巨型病毒在所有蛋白质组的树状图中表现为一个基部类群。对大肠杆菌（细菌）、嗜热栖热菌（古菌）、酿酒酵母（真核生物）和图潘病毒（巨型病毒）确定的泛基因组和核心基因组显示，图潘病毒有相当比例的基因与细胞微生物的基因重叠。此外，观察到大量的基因组镶嵌现象，图潘病毒分别有51%、11%、8%和0.2%的基因与病毒、真核生物、细菌和古菌的基因最匹配。最后，我们发现基因本身可能会发生侧向序列转移。总之，我们的数据突出了经典病毒和巨型病毒之间的巨大飞跃。系统发育和谱系分析以及对蛋白质折叠超家族的研究证实了先前关于存在包括巨型病毒在内的生命的第四个TRUC的证据，并突出了其祖先关系和镶嵌性。它们还指出，巨型病毒和细胞微生物的最佳进化表示是根茎，并且必须考虑序列转移而非基因转移。
