Blanc-Mathieu Romain, Dahle Håkon, Hofgaard Antje, Brandt David, Ban Hiroki, Kalinowski Jörn, Ogata Hiroyuki, Sandaa Ruth-Anne
Institute for Chemical Research, Kyoto University, Gokasho, Uji, 611-0011, Japan.
Laboratoire de Physiologie Cellulaire & Végétale, CEA, Univ. Grenoble Alpes, CNRS, INRA, IRIG, Grenoble, France.
J Virol. 2021 Mar 25;95(8). doi: 10.1128/JVI.02446-20. Epub 2021 Feb 3.
Viruses have long been viewed as entities possessing extremely limited metabolic capacities. Over the last decade, however, this view has been challenged, as metabolic genes have been identified in viruses possessing large genomes and virions-the synthesis of which is energetically demanding. Here, we unveil peculiar phenotypic and genomic features of virus RF01 (PkV RF01), a giant virus of the family. We found that this virus encodes an unprecedented number of proteins involved in energy metabolism, such as all four succinate dehydrogenase (SDH) subunits (A-D) as well as key enzymes in the -oxidation pathway. The gene was transcribed upon infection, indicating that the viral SDH is actively used by the virus- potentially to modulate its host's energy metabolism. We detected orthologous and genes in numerous genome fragments from uncultivated marine viruses, which suggests that the viral SDH is widespread in oceans. PkV RF01 was less virulent compared with other cultured prymnesioviruses, a phenomenon possibly linked to the metabolic capacity of this virus and suggestive of relatively long co-evolution with its hosts. It also has a unique morphology, compared to other characterized viruses in the family. Finally, we found that PkV RF01 is the only alga-infecting virus encoding two aminoacyl-tRNA synthetases and enzymes corresponding to an entire base-excision repair pathway, as seen in heterotroph-infecting These encoded-enzymes were found to be monophyletic and branching at the root of the eukaryotic tree of life. This placement suggests that the last common ancestor of was endowed with a large, complex genome prior to the divergence of known extant eukaryotes. Viruses on Earth are tremendously diverse in terms of morphology, functionality, and genomic composition. Over the last decade, the conceptual gap separating viruses and cellular life has tightened because of the detection of metabolic genes in viral genomes that express complex virus phenotypes upon infection. Here, we describe virus RF01, a large alga-infecting virus with a unique morphology, an atypical infection profile, and an unprecedented number of genes involved in energy metabolism (such as the tricarboxylic (TCA) cycle and the -oxidation pathway). Moreover, we show that the gene corresponding to one of these enzymes (the succinate dehydrogenase subunit A) is transcribed during infection and is widespread among marine viruses. This discovery provides evidence that a virus has the potential to actively regulate energy metabolism with its own gene.
长期以来，病毒一直被视为代谢能力极其有限的实体。然而，在过去十年中，这种观点受到了挑战，因为在拥有大基因组和病毒粒子的病毒中发现了代谢基因，而病毒粒子的合成在能量方面要求很高。在这里，我们揭示了病毒RF01（PkV RF01）的独特表型和基因组特征，它是该家族的一种巨型病毒。我们发现这种病毒编码了数量空前的参与能量代谢的蛋白质，比如所有四个琥珀酸脱氢酶（SDH）亚基（A - D）以及β - 氧化途径中的关键酶。该基因在感染时被转录，这表明病毒的SDH被病毒积极利用，可能是为了调节其宿主的能量代谢。我们在来自未培养的海洋病毒的众多基因组片段中检测到了直系同源的SDH和相关基因，这表明病毒SDH在海洋中广泛存在。与其他培养的定鞭藻病毒相比，PkV RF01的毒性较小，这种现象可能与该病毒的代谢能力有关，并暗示其与宿主有相对较长的共同进化历史。与该家族中其他已鉴定的病毒相比，它还具有独特的形态。最后，我们发现PkV RF01是唯一一种感染藻类的病毒，它编码两种氨酰 - tRNA合成酶以及对应于整个碱基切除修复途径的酶，就像感染异养生物的病毒那样。这些编码的酶被发现是单系的，并且在真核生物生命树的根部分支。这种位置表明，在已知现存真核生物分化之前，该病毒的最后一个共同祖先就拥有一个庞大、复杂的基因组。地球上的病毒在形态、功能和基因组组成方面极其多样。在过去十年中，由于在病毒基因组中检测到代谢基因，这些基因在感染时会表达出复杂的病毒表型，病毒与细胞生命之间的概念差距已经缩小。在这里，我们描述了病毒RF01，一种感染大型藻类的病毒，它具有独特的形态、非典型的感染特征以及数量空前的参与能量代谢的基因（如三羧酸（TCA）循环和β - 氧化途径）。此外，我们表明与这些酶之一（琥珀酸脱氢酶亚基A）对应的基因在感染期间被转录，并且在海洋病毒中广泛存在。这一发现提供了证据，证明一种病毒有可能利用自身基因积极调节能量代谢。
