Discovery of Viral Myosin Genes With Complex Evolutionary History Within Plankton

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, a...

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Main Authors: Soichiro Kijima, Tom O. Delmont, Urara Miyazaki, Morgan Gaia, Hisashi Endo, Hiroyuki Ogata
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-06-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.683294/full
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author Soichiro Kijima
Tom O. Delmont
Urara Miyazaki
Urara Miyazaki
Morgan Gaia
Hisashi Endo
Hiroyuki Ogata
author_facet Soichiro Kijima
Tom O. Delmont
Urara Miyazaki
Urara Miyazaki
Morgan Gaia
Hisashi Endo
Hiroyuki Ogata
author_sort Soichiro Kijima
collection DOAJ
description 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.
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spelling doaj.art-660e0ce86e92481eb60b3093c5c73df12022-12-21T18:58:59ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-06-011210.3389/fmicb.2021.683294683294Discovery of Viral Myosin Genes With Complex Evolutionary History Within PlanktonSoichiro Kijima0Tom O. Delmont1Urara Miyazaki2Urara Miyazaki3Morgan Gaia4Hisashi Endo5Hiroyuki Ogata6Chemical Life Science, Institute for Chemical Research, Kyoto University, Uji, JapanMetabolic Genomics, Genoscope, Institut de Biologie François Jacob, CEA, CNRS, Univ Evry, Université Paris Saclay, Évry-Courcouronnes, FranceChemical Life Science, Institute for Chemical Research, Kyoto University, Uji, JapanLaboratory of Marine Environmental Microbiology, Division of Applied Biosciences, Graduate School of Agriculture, Kyoto University, Kyoto, JapanMetabolic Genomics, Genoscope, Institut de Biologie François Jacob, CEA, CNRS, Univ Evry, Université Paris Saclay, Évry-Courcouronnes, FranceChemical Life Science, Institute for Chemical Research, Kyoto University, Uji, JapanChemical Life Science, Institute for Chemical Research, Kyoto University, Uji, JapanNucleocytoplasmic 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.https://www.frontiersin.org/articles/10.3389/fmicb.2021.683294/fullNCLDVgiant virusesmyosinphylogenyviral diversityNucleocytoviricota
spellingShingle Soichiro Kijima
Tom O. Delmont
Urara Miyazaki
Urara Miyazaki
Morgan Gaia
Hisashi Endo
Hiroyuki Ogata
Discovery of Viral Myosin Genes With Complex Evolutionary History Within Plankton
Frontiers in Microbiology
NCLDV
giant viruses
myosin
phylogeny
viral diversity
Nucleocytoviricota
title Discovery of Viral Myosin Genes With Complex Evolutionary History Within Plankton
title_full Discovery of Viral Myosin Genes With Complex Evolutionary History Within Plankton
title_fullStr Discovery of Viral Myosin Genes With Complex Evolutionary History Within Plankton
title_full_unstemmed Discovery of Viral Myosin Genes With Complex Evolutionary History Within Plankton
title_short Discovery of Viral Myosin Genes With Complex Evolutionary History Within Plankton
title_sort discovery of viral myosin genes with complex evolutionary history within plankton
topic NCLDV
giant viruses
myosin
phylogeny
viral diversity
Nucleocytoviricota
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.683294/full
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