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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Published in:Proceedings of the National Academy of Sciences - PNAS Vol. 116; no. 39; p. 19585
Main Authors: Guglielmini, Julien, Woo, Anthony C, Krupovic, Mart, Forterre, Patrick, Gaia, Morgan
Format: Journal Article
Language:English
Published: United States 24.09.2019
Subjects:
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
Online Access:Get more information
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Summary: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.
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ISSN:1091-6490
1091-6490
DOI:10.1073/pnas.1912006116