The majority of viruses infecting hyperthermophilic archaea display unique virion architectures and are evolutionarily unrelated to viruses of bacteria and eukaryotes. The lack of relationships to other known viruses suggests that the mechanisms of virus–host interaction in Archaea are also likely to be distinct. To gain insights into archaeal virus–host interactions, we studied the life cycle of the enveloped, ∼2-μm-long Sulfolobus islandicus filamentous virus (SIFV), a member of the family Lipothrixviridae infecting a hyperthermophilic and acidophilic archaeon Saccharolobus islandicus LAL14/1. Using dual-axis electron tomography and convolutional neural network analysis, we characterize the life cycle of SIFV and show that the virions, which are nearly two times longer than the host cell diameter, are assembled in the cell cytoplasm, forming twisted virion bundles organized on a nonperfect hexagonal lattice. Remarkably, our results indicate that envelopment of the helical nucleocapsids takes place inside the cell rather than by budding as in the case of most other known enveloped viruses. The mature virions are released from the cell through large (up to 220 nm in diameter), six-sided pyramidal portals, which are built from multiple copies of a single 89-amino-acid-long viral protein gp43. The overexpression of this protein in Escherichia coli leads to pyramid formation in the bacterial membrane. Collectively, our results provide insights into the assembly and release of enveloped filamentous viruses and illuminate the evolution of virus–host interactions in Archaea.

大多数感染嗜热古生菌的病毒都表现出独特的病毒体结构，并且在进化上与细菌和真核生物的病毒无关。与其他已知病毒缺乏关系表明古细菌中病毒与宿主相互作用的机制也可能是不同的。为了深入了解古细菌病毒与宿主的相互作用，我们研究了有包膜的、长约 2 微米的硫叶菌丝状病毒 (SIFV) 的生命周期，它是脂丝病毒科的成员，感染了超嗜热和嗜酸的古生菌Saccharolobus islandicusLAL14/1。使用双轴电子断层扫描和卷积神经网络分析，我们描述了 SIFV 的生命周期，并表明比宿主细胞直径长近两倍的病毒粒子在细胞质中组装，形成扭曲的病毒粒子束，组织在一个不完美的六边形晶格。值得注意的是，我们的结果表明螺旋核衣壳的包膜发生在细胞内，而不是像大多数其他已知的包膜病毒那样通过出芽发生。成熟的病毒粒子通过大的（直径达 220 nm）六面锥体入口从细胞中释放出来，这些入口由单个 89 个氨基酸长的病毒蛋白 gp43 的多个拷贝构成。这种蛋白质在大肠杆菌中的过表达导致在细菌膜中形成金字塔。总的来说，我们的结果提供了对包膜丝状病毒的组装和释放的见解，并阐明了古生菌中病毒-宿主相互作用的进化。