Aix-Marseille University, Centre National de la Recherche Scientifique, Information Génomique & Structurale (IGS), Unité Mixte de Recherche 7256 (Institut de Microbiologie de la Méditerranée, FR3479), IM2B, IOM, Marseille, Cedex 9, France.
Univ. Grenoble Alpes, INSERM, CEA, UA13 BGE, CNRS, CEA, FR2048, Grenoble, France.
Nat Commun. 2024 Oct 9;15(1):8608. doi: 10.1038/s41467-024-52906-1.
Hyperparasitism is a common pattern in nature that is not limited to cellular organisms. Giant viruses infecting protists can be hyperparasitized by smaller ones named virophages. In addition, both may carry episomal DNA molecules known as transpovirons in their particles. They all share transcriptional regulatory elements that dictate the expression of their genes within viral factories built by giant viruses in the host cytoplasm. This suggests the existence of interactions between their respective transcriptional networks. Here we investigated Acanthamoeba castellanii cells infected by a giant virus (megavirus chilensis), and coinfected with a virophage (zamilon vitis) and/or a transpoviron (megavirus vitis transpoviron). Infectious cycles were monitored through time-course RNA sequencing to decipher the transcriptional program of each partner and its impact on the gene expression of the others. We found highly diverse transcriptional responses. While the giant virus drastically reshaped the host cell transcriptome, the transpoviron had no effect on the gene expression of any of the players. In contrast, the virophage strongly modified the giant virus gene expression, albeit transiently, without altering the protein composition of mature viral particles. The virophage also induced the overexpression of transpoviron genes, likely through the indirect upregulation of giant virus-encoded transcription factors. Together, these analyses document the intricated transcriptionally regulated networks taking place in the infected cell.
重寄生在自然界中很常见，并不局限于细胞生物。感染原生生物的巨型病毒可被称为噬病毒体的更小病毒重寄生。此外，两者的颗粒中都可能携带称为转座病毒的附加 DNA 分子。它们都具有转录调控元件，这些元件决定了它们在宿主细胞质中由巨型病毒构建的病毒工厂内基因的表达。这表明它们各自的转录网络之间存在相互作用。在这里，我们研究了感染巨型病毒（奇塔姆病毒）的嗜热四膜虫细胞，并同时感染了噬病毒体（齐米隆病毒）和/或转座病毒（奇塔姆病毒转座病毒）。通过时间过程 RNA 测序监测感染周期，以破译每个伙伴的转录程序及其对其他伙伴基因表达的影响。我们发现了高度多样化的转录反应。虽然巨型病毒极大地重塑了宿主细胞的转录组，但转座病毒对任何参与者的基因表达都没有影响。相比之下，噬病毒体强烈地改变了巨型病毒的基因表达，尽管是短暂的，但不改变成熟病毒颗粒的蛋白质组成。噬病毒体还诱导了转座病毒基因的过表达，可能是通过间接上调巨型病毒编码的转录因子。总之，这些分析记录了感染细胞中发生的错综复杂的转录调控网络。
