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A billion years arms-race between viruses, virophages, and eukaryotes

Bamfordviruses are arguably the most diverse group of viruses infecting eukaryotes. They include the Nucleocytoplasmic Large DNA viruses (NCLDVs), virophages, adenoviruses, Mavericks and Polinton-like viruses. Two main hypotheses for their origins have been proposed: the ‘nuclear-escape’ and ‘viroph...

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Autores principales: Barreat, Jose Gabriel Nino, Katzourakis, Aris
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10328495/
https://www.ncbi.nlm.nih.gov/pubmed/37358563
http://dx.doi.org/10.7554/eLife.86617
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author Barreat, Jose Gabriel Nino
Katzourakis, Aris
author_facet Barreat, Jose Gabriel Nino
Katzourakis, Aris
author_sort Barreat, Jose Gabriel Nino
collection PubMed
description Bamfordviruses are arguably the most diverse group of viruses infecting eukaryotes. They include the Nucleocytoplasmic Large DNA viruses (NCLDVs), virophages, adenoviruses, Mavericks and Polinton-like viruses. Two main hypotheses for their origins have been proposed: the ‘nuclear-escape’ and ‘virophage-first’ hypotheses. The nuclear-escape hypothesis proposes an endogenous, Maverick-like ancestor which escaped from the nucleus and gave rise to adenoviruses and NCLDVs. In contrast, the virophage-first hypothesis proposes that NCLDVs coevolved with protovirophages; Mavericks then evolved from virophages that became endogenous, with adenoviruses escaping from the nucleus at a later stage. Here, we test the predictions made by both models and consider alternative evolutionary scenarios. We use a data set of the four core virion proteins sampled across the diversity of the lineage, together with Bayesian and maximum-likelihood hypothesis-testing methods, and estimate rooted phylogenies. We find strong evidence that adenoviruses and NCLDVs are not sister groups, and that Mavericks and Mavirus acquired the rve-integrase independently. We also found strong support for a monophyletic group of virophages (family Lavidaviridae) and a most likely root placed between virophages and the other lineages. Our observations support alternatives to the nuclear-escape scenario and a billion years evolutionary arms-race between virophages and NCLDVs.
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spelling pubmed-103284952023-07-08 A billion years arms-race between viruses, virophages, and eukaryotes Barreat, Jose Gabriel Nino Katzourakis, Aris eLife Evolutionary Biology Bamfordviruses are arguably the most diverse group of viruses infecting eukaryotes. They include the Nucleocytoplasmic Large DNA viruses (NCLDVs), virophages, adenoviruses, Mavericks and Polinton-like viruses. Two main hypotheses for their origins have been proposed: the ‘nuclear-escape’ and ‘virophage-first’ hypotheses. The nuclear-escape hypothesis proposes an endogenous, Maverick-like ancestor which escaped from the nucleus and gave rise to adenoviruses and NCLDVs. In contrast, the virophage-first hypothesis proposes that NCLDVs coevolved with protovirophages; Mavericks then evolved from virophages that became endogenous, with adenoviruses escaping from the nucleus at a later stage. Here, we test the predictions made by both models and consider alternative evolutionary scenarios. We use a data set of the four core virion proteins sampled across the diversity of the lineage, together with Bayesian and maximum-likelihood hypothesis-testing methods, and estimate rooted phylogenies. We find strong evidence that adenoviruses and NCLDVs are not sister groups, and that Mavericks and Mavirus acquired the rve-integrase independently. We also found strong support for a monophyletic group of virophages (family Lavidaviridae) and a most likely root placed between virophages and the other lineages. Our observations support alternatives to the nuclear-escape scenario and a billion years evolutionary arms-race between virophages and NCLDVs. eLife Sciences Publications, Ltd 2023-06-26 /pmc/articles/PMC10328495/ /pubmed/37358563 http://dx.doi.org/10.7554/eLife.86617 Text en © 2023, Barreat and Katzourakis https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Evolutionary Biology
Barreat, Jose Gabriel Nino
Katzourakis, Aris
A billion years arms-race between viruses, virophages, and eukaryotes
title A billion years arms-race between viruses, virophages, and eukaryotes
title_full A billion years arms-race between viruses, virophages, and eukaryotes
title_fullStr A billion years arms-race between viruses, virophages, and eukaryotes
title_full_unstemmed A billion years arms-race between viruses, virophages, and eukaryotes
title_short A billion years arms-race between viruses, virophages, and eukaryotes
title_sort billion years arms-race between viruses, virophages, and eukaryotes
topic Evolutionary Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10328495/
https://www.ncbi.nlm.nih.gov/pubmed/37358563
http://dx.doi.org/10.7554/eLife.86617
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