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. Interestingly, these genes were often accompanied by kinesin genes in the environmental genomes, suggesting a role of these viral proteins in the intracellular viral particle transport. 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.

Diversity and genomics of giant viruses in the North Pacific Subtropical Gyre

“…Viral rhodopsins may permit viruses to modify host phototaxis during infection, which may promote their proliferation (Gallot-Lavallée and Archibald, 2020). Proteins involved in cytoskeletal dynamics have also been found to be quite common in a variety of marine giant viruses; viral homologs to actin, myosin, and kinesin genes could potentially benefit viruses by manipulating the host's cytoskeleton by using host motor proteins to traffic virions or maintain the localization of viral machinery during infection (Ha et al, 2021;Kijima et al, 2021;Da Cunha et al, 2022). These recent findings collectively suggest that giant viruses use a broad assortment of functional genes to manipulate host physiology and alter the intracellular environment to promote virion propagation.…”

High Transcriptional Activity and Diverse Functional Repertoires of Hundreds of Giant Viruses in a Coastal Marine System

“…Surprisingly, we also found several transcripts matching to predicted cytoskeletal proteins, including actin, myosin, and kinesin. Recent studies have identified divergent actin, myosin, and kinesin homologs in Nucleocytoviricota and, in some cases, it has been suggested they may have played a role in the emergence of this protein in extant eukaryotic lineages ( 65 – 67 ). We found three expressed viral genes with predicted myosin motor domains and one with kinesin domains, and subsequent analysis of all Nucleocytoviricota genomes in our reference database recovered an additional 109 myosin and 200 kinesin homologs.…”

The Secret Life of Giant Viruses in the California Current

“…In addition, the authors present data confirming the expression of several transcripts related to cytoskeletal proteins, including actin, myosin, and kinesin. Remarkably, previous studies have identified cytoskeletal-related homologs in Nucleocytoviricota genomes ( 18 – 20 ). Ha and colleagues contributed to this knowledge by presenting 109 myosin and 200 kinesin homologs.…”