Discovery of Viral Myosin Genes With Complex Evolutionary History Within Plankton

Abstract

Nucleocytoplasmic large DNA viruses (NCLDVs) infect diverse eukaryotes and form a group of viruses with capsids encapsulating large genomes. Recent studies are increasingly revealing a spectacular array of functions encoded in their genomes, including genes for energy metabolisms, nutrient uptake, as well as cytoskeleton. Here, we report the discovery of genes homologous to myosins, the major eukaryotic motor proteins previously unrecognized in the virosphere, in environmental genomes of NCLDVs from the surface of the oceans. Phylogenetic analyses indicate that most viral myosins (named “virmyosins”) belong to the Imitervirales order, except for one belonging to the Phycodnaviridae family. On the one hand, the phylogenetic positions of virmyosin-encoding Imitervirales are scattered within the Imitervirales. On the other hand, Imitervirales virmyosin genes form a monophyletic group in the phylogeny of diverse myosin sequences. Furthermore, phylogenetic trends for the virmyosin genes and viruses containing them were incongruent. Based on these results, we argue that multiple transfers of myosin homologs have occurred not only from eukaryotes to viruses but also between viruses, supposedly during co-infections of the same host. Like other viruses that use host motor proteins for their intracellular transport or motility, these viruses may use the virally encoded myosins for the intracellular trafficking of giant viral particles.

A phylogenomic framework for charting the diversity and evolution of giant viruses

“…Genes involved in translation, including tRNA synthetases and translation initiation factors, were consistently highly represented in the Imitervirales, showing that the rich complement of these genes that has been described for the Mimiviridae is broadly characteristic of other families in this order (Fig 4B) [40,42]. Throughout the Imitervirales genes involved in glycolysis and the TCA cycle, cytoskeleton components such as viral-encoded actin, myosin, and kinesin proteins, and nutrient transporters including those that target ammonia and phosphate were also common (Fig 4B) [10,[44][45][46], underscoring the complex functional repertoires of this virus order.…”

Giant Viruses Encode Actin-Related Proteins

“…The discovery of viractins closely related to the eukaryotic actin echoes the close association between Imitervirales and several eukaryotic signature features (DNA-dependent RNA polymerase II [ Guglielmini et al 2019 ], histones [ Boyer et al 2009 ; Yoshikawa et al 2019 ], DNA polymerase [ Takemura et al 2015 ], kinesin [ Subramaniam et al 2020 ], myosin [ Ha et al 2021 ; Kijima et al 2021 ]), supporting the hypothesis of a coevolution between Nucleocytoviricota and protoeukaryotes that could have contributed in shaping the molecular components and functions of the modern eukaryotic cell.…”

“…The identification of viral actin-like genes sharing a common ancestry with eukaryotic conventional actins now brings a new piece to the puzzle. A few studies have previously emphasized a possible evolutionary relationship between the eukaryotic nucleus and Nucleocytoviricota ’ viral factories ( Forterre and Gaïa 2016 and herein; Bell 2020 ), but no connection had been made between these viruses and the eukaryotic cytoskeleton until very recently ( Kijima et al 2021 ). In this context, it is interesting to note that actin is present in both the cytoplasm and the nucleus of eukaryotic cells and with nuclear ARPs seems to be involved in several nuclear-related processes ( Bajusz et al 2018 ).…”

Evolving Perspective on the Origin and Diversification of Cellular Life and the Virosphere

“…Particularly the discovery of eukaryotic NucleoCytoplasmic Large DNA viruses (NCLDVs), also referred to as giant viruses ( Raoult et al 2004 ), has sparked debates on the boundaries between viruses and cellular organisms as well as raised questions regarding their origins, relationship to cellular life and role in the origin of the eukaryotic cell. NCLDVs comprise members with unique features among viruses including genome sizes that resemble those of some free-living microorganisms, the presence of genes for DNA maintenance including repair, replication, transcription, and translation, complex metabolic capabilities, cytoskeleton components, as well as other signature proteins of complex eukaryotic cells, all of which were originally thought to be confined to cellular life ( Schulz et al 2017 ; Abrahao et al 2018 ; Schvarcz and Steward 2018 ; Koonin and Yutin 2019 ; Yoshikawa et al 2019 ; Da Cunha et al 202 2; Moniruzzaman, Martinez-Gutierrez et al 2020 ; Kijima et al 2021 ). Some representatives replicate within viral factories, that is, intracellular compartments in which viral components are localized and that may be enclosed by membranes ( Novoa et al 2005 ; Suzan-Monti et al 2007 ), and can be parasitized by their own virophages ( Krupovic et al 2016 ).…”