Diversification of giant and large eukaryotic dsDNA viruses predated the origin of modern eukaryotes

Giant and large eukaryotic double-stranded DNA viruses from the Nucleo-Cytoplasmic Large DNA Virus (NCLDV) assemblage represent a remarkably diverse and potentially ancient component of the eukaryotic virome. However, their origin(s), evolution, and potential roles in the emergence of modern eukaryo...

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Vydáno v:Proceedings of the National Academy of Sciences - PNAS Ročník 116; číslo 39; s. 19585
Hlavní autoři: Guglielmini, Julien, Woo, Anthony C, Krupovic, Mart, Forterre, Patrick, Gaia, Morgan
Médium: Journal Article
Jazyk:angličtina
Vydáno: United States 24.09.2019
Témata:
Biological Evolution
Cell Nucleus - genetics
Cytoplasm - virology
DNA Viruses - genetics
DNA-Directed RNA Polymerases - genetics
DNA-Directed RNA Polymerases - metabolism
Eukaryota - genetics
Eukaryotic Cells - metabolism
Evolution, Molecular
Giant Viruses - genetics
Giant Viruses - metabolism
Phylogeny
NCLDV
RNA polymerase
evolution
giant viruses
proto-eukaryotes
ISSN:1091-6490, 1091-6490
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Abstract Giant and large eukaryotic double-stranded DNA viruses from the Nucleo-Cytoplasmic Large DNA Virus (NCLDV) assemblage represent a remarkably diverse and potentially ancient component of the eukaryotic virome. However, their origin(s), evolution, and potential roles in the emergence of modern eukaryotes remain subjects of intense debate. Here we present robust phylogenetic trees of NCLDVs, based on the 8 most conserved proteins responsible for virion morphogenesis and informational processes. Our results uncover the evolutionary relationships between different NCLDV families and support the existence of 2 superclades of NCLDVs, each encompassing several families. We present evidence strongly suggesting that the NCLDV core genes, which are involved in both informational processes and virion formation, were acquired vertically from a common ancestor. Among them, the largest subunits of the DNA-dependent RNA polymerase were transferred between 2 clades of NCLDVs and proto-eukaryotes, giving rise to 2 of the 3 eukaryotic DNA-dependent RNA polymerases. Our results strongly suggest that these transfers and the diversification of NCLDVs predated the emergence of modern eukaryotes, emphasizing the major role of viruses in the evolution of cellular domains.
AbstractList Giant and large eukaryotic double-stranded DNA viruses from the Nucleo-Cytoplasmic Large DNA Virus (NCLDV) assemblage represent a remarkably diverse and potentially ancient component of the eukaryotic virome. However, their origin(s), evolution, and potential roles in the emergence of modern eukaryotes remain subjects of intense debate. Here we present robust phylogenetic trees of NCLDVs, based on the 8 most conserved proteins responsible for virion morphogenesis and informational processes. Our results uncover the evolutionary relationships between different NCLDV families and support the existence of 2 superclades of NCLDVs, each encompassing several families. We present evidence strongly suggesting that the NCLDV core genes, which are involved in both informational processes and virion formation, were acquired vertically from a common ancestor. Among them, the largest subunits of the DNA-dependent RNA polymerase were transferred between 2 clades of NCLDVs and proto-eukaryotes, giving rise to 2 of the 3 eukaryotic DNA-dependent RNA polymerases. Our results strongly suggest that these transfers and the diversification of NCLDVs predated the emergence of modern eukaryotes, emphasizing the major role of viruses in the evolution of cellular domains.Giant and large eukaryotic double-stranded DNA viruses from the Nucleo-Cytoplasmic Large DNA Virus (NCLDV) assemblage represent a remarkably diverse and potentially ancient component of the eukaryotic virome. However, their origin(s), evolution, and potential roles in the emergence of modern eukaryotes remain subjects of intense debate. Here we present robust phylogenetic trees of NCLDVs, based on the 8 most conserved proteins responsible for virion morphogenesis and informational processes. Our results uncover the evolutionary relationships between different NCLDV families and support the existence of 2 superclades of NCLDVs, each encompassing several families. We present evidence strongly suggesting that the NCLDV core genes, which are involved in both informational processes and virion formation, were acquired vertically from a common ancestor. Among them, the largest subunits of the DNA-dependent RNA polymerase were transferred between 2 clades of NCLDVs and proto-eukaryotes, giving rise to 2 of the 3 eukaryotic DNA-dependent RNA polymerases. Our results strongly suggest that these transfers and the diversification of NCLDVs predated the emergence of modern eukaryotes, emphasizing the major role of viruses in the evolution of cellular domains.
Giant and large eukaryotic double-stranded DNA viruses from the Nucleo-Cytoplasmic Large DNA Virus (NCLDV) assemblage represent a remarkably diverse and potentially ancient component of the eukaryotic virome. However, their origin(s), evolution, and potential roles in the emergence of modern eukaryotes remain subjects of intense debate. Here we present robust phylogenetic trees of NCLDVs, based on the 8 most conserved proteins responsible for virion morphogenesis and informational processes. Our results uncover the evolutionary relationships between different NCLDV families and support the existence of 2 superclades of NCLDVs, each encompassing several families. We present evidence strongly suggesting that the NCLDV core genes, which are involved in both informational processes and virion formation, were acquired vertically from a common ancestor. Among them, the largest subunits of the DNA-dependent RNA polymerase were transferred between 2 clades of NCLDVs and proto-eukaryotes, giving rise to 2 of the 3 eukaryotic DNA-dependent RNA polymerases. Our results strongly suggest that these transfers and the diversification of NCLDVs predated the emergence of modern eukaryotes, emphasizing the major role of viruses in the evolution of cellular domains.
Author Krupovic, Mart
Gaia, Morgan
Guglielmini, Julien
Forterre, Patrick
Woo, Anthony C
Author_xml – sequence: 1
  givenname: Julien
  surname: Guglielmini
  fullname: Guglielmini, Julien
  organization: HUB Bioinformatique et Biostatistique, C3BI, USR 3756 IP CNRS, Institut Pasteur, 75015 Paris, France
– sequence: 2
  givenname: Anthony C
  surname: Woo
  fullname: Woo, Anthony C
  organization: Unité de Biologie Moléculaire du Gène ches les Extrêmophiles, Département de Microbiologie, Institut Pasteur, 75015 Paris, France
– sequence: 3
  givenname: Mart
  surname: Krupovic
  fullname: Krupovic, Mart
  organization: Unité de Biologie Moléculaire du Gène ches les Extrêmophiles, Département de Microbiologie, Institut Pasteur, 75015 Paris, France
– sequence: 4
  givenname: Patrick
  surname: Forterre
  fullname: Forterre, Patrick
  email: patrick.forterre@pasteur.fr, morgan.gaia@pasteur.fr
  organization: Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Université Paris-Sud, Université Paris-Saclay, 91198 Gif-sur-Yvette cedex, France
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  givenname: Morgan
  orcidid: 0000-0003-4936-4780
  surname: Gaia
  fullname: Gaia, Morgan
  email: patrick.forterre@pasteur.fr, morgan.gaia@pasteur.fr
  organization: Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Université Paris-Sud, Université Paris-Saclay, 91198 Gif-sur-Yvette cedex, France
BackLink https://www.ncbi.nlm.nih.gov/pubmed/31506349$$D View this record in MEDLINE/PubMed
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Keywords NCLDV
RNA polymerase
evolution
giant viruses
proto-eukaryotes
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References 31992646 - Proc Natl Acad Sci U S A. 2020 Feb 11;117(6):2747-2748. doi: 10.1073/pnas.1919860117.
31992645 - Proc Natl Acad Sci U S A. 2020 Feb 11;117(6):2749-2750. doi: 10.1073/pnas.1920855117.
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Snippet Giant and large eukaryotic double-stranded DNA viruses from the Nucleo-Cytoplasmic Large DNA Virus (NCLDV) assemblage represent a remarkably diverse and...
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SubjectTerms Biological Evolution
Cell Nucleus - genetics
Cytoplasm - virology
DNA Viruses - genetics
DNA-Directed RNA Polymerases - genetics
DNA-Directed RNA Polymerases - metabolism
Eukaryota - genetics
Eukaryotic Cells - metabolism
Evolution, Molecular
Giant Viruses - genetics
Giant Viruses - metabolism
Phylogeny
Title Diversification of giant and large eukaryotic dsDNA viruses predated the origin of modern eukaryotes
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