Archaeal Virology Unit, Department of Microbiology, Institut Pasteur, 75015, Paris, France.
Sorbonne Université, Collège Doctoral, 7 Quai Saint-Bernard, 75005, Paris, France.
ISME J. 2020 Jul;14(7):1821-1833. doi: 10.1038/s41396-020-0653-z. Epub 2020 Apr 22.
Viruses of hyperthermophilic archaea represent one of the least understood parts of the virosphere, showing little genomic and morphological similarity to viruses of bacteria or eukaryotes. Here, we investigated virus diversity in the active sulfurous fields of the Campi Flegrei volcano in Pozzuoli, Italy. Virus-like particles displaying eight different morphotypes, including lemon-shaped, droplet-shaped and bottle-shaped virions, were observed and five new archaeal viruses proposed to belong to families Rudiviridae, Globuloviridae and Tristromaviridae were isolated and characterized. Two of these viruses infect neutrophilic hyperthermophiles of the genus Pyrobaculum, whereas the remaining three have rod-shaped virions typical of the family Rudiviridae and infect acidophilic hyperthermophiles belonging to three different genera of the order Sulfolobales, namely, Saccharolobus, Acidianus, and Metallosphaera. Notably, Metallosphaera rod-shaped virus 1 is the first rudivirus isolated on Metallosphaera species. Phylogenomic analysis of the newly isolated and previously sequenced rudiviruses revealed a clear biogeographic pattern, with all Italian rudiviruses forming a monophyletic clade, suggesting geographical structuring of virus communities in extreme geothermal environments. Analysis of the CRISPR spacers suggests that isolated rudiviruses have experienced recent host switching across the genus boundary, potentially to escape the targeting by CRISPR-Cas immunity systems. Finally, we propose a revised classification of the Rudiviridae family, with the establishment of six new genera. Collectively, our results further show that high-temperature continental hydrothermal systems harbor a highly diverse virome and shed light on the evolution of archaeal viruses.
超嗜热古菌病毒是病毒圈中了解最少的部分之一，它们与细菌或真核生物的病毒在基因组和形态上几乎没有相似之处。在这里，我们研究了意大利波佐利坎帕菲莱雷火山活跃硫磺区的病毒多样性。观察到了显示出八种不同形态的病毒样颗粒，包括柠檬形、液滴形和瓶形病毒粒子，并分离和鉴定了 5 种新的古菌病毒，它们属于 Rudiviridae、Globuloviridae 和 Tristromaviridae 科。其中两种病毒感染嗜中性的 Pyrobaculum 嗜热菌，而其余三种病毒的杆状病毒粒子具有典型的 Rudiviridae 科特征，感染属于 Sulfolobales 目三个不同属的嗜酸嗜热菌，即 Saccharolobus、Acidianus 和 Metallosphaera。值得注意的是，Metallosphaera 杆状病毒 1 是第一个在 Metallosphaera 属中分离出来的 rudivirus。对新分离和以前测序的 rudiviruses 进行的系统基因组分析显示出明显的生物地理模式，所有意大利 rudiviruses 形成一个单系群，表明极端地热环境中的病毒群落存在地理结构。对 CRISPR 间隔区的分析表明，分离出的 rudiviruses 经历了最近的跨越属界的宿主转换，可能是为了逃避 CRISPR-Cas 免疫系统的靶向。最后，我们提出了 Rudiviridae 科的修订分类，建立了 6 个新属。总的来说，我们的研究结果进一步表明，高温大陆热液系统蕴藏着高度多样化的病毒组，并揭示了古菌病毒的进化。
