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A critical analysis of the current state of virus taxonomy

Taxonomical classification has preceded evolutionary understanding. For that reason, taxonomy has become a battleground fueled by knowledge gaps, technical limitations, and a priorism. Here we assess the current state of the challenging field, focusing on fallacies that are common in viral classific...

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Autores principales: Caetano-Anollés, Gustavo, Claverie, Jean-Michel, Nasir, Arshan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10435761/
https://www.ncbi.nlm.nih.gov/pubmed/37601376
http://dx.doi.org/10.3389/fmicb.2023.1240993
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author Caetano-Anollés, Gustavo
Claverie, Jean-Michel
Nasir, Arshan
author_facet Caetano-Anollés, Gustavo
Claverie, Jean-Michel
Nasir, Arshan
author_sort Caetano-Anollés, Gustavo
collection PubMed
description Taxonomical classification has preceded evolutionary understanding. For that reason, taxonomy has become a battleground fueled by knowledge gaps, technical limitations, and a priorism. Here we assess the current state of the challenging field, focusing on fallacies that are common in viral classification. We emphasize that viruses are crucial contributors to the genomic and functional makeup of holobionts, organismal communities that behave as units of biological organization. Consequently, viruses cannot be considered taxonomic units because they challenge crucial concepts of organismality and individuality. Instead, they should be considered processes that integrate virions and their hosts into life cycles. Viruses harbor phylogenetic signatures of genetic transfer that compromise monophyly and the validity of deep taxonomic ranks. A focus on building phylogenetic networks using alignment-free methodologies and molecular structure can help mitigate the impasse, at least in part. Finally, structural phylogenomic analysis challenges the polyphyletic scenario of multiple viral origins adopted by virus taxonomy, defeating a polyphyletic origin and supporting instead an ancient cellular origin of viruses. We therefore, prompt abandoning deep ranks and urgently reevaluating the validity of taxonomic units and principles of virus classification.
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spelling pubmed-104357612023-08-19 A critical analysis of the current state of virus taxonomy Caetano-Anollés, Gustavo Claverie, Jean-Michel Nasir, Arshan Front Microbiol Microbiology Taxonomical classification has preceded evolutionary understanding. For that reason, taxonomy has become a battleground fueled by knowledge gaps, technical limitations, and a priorism. Here we assess the current state of the challenging field, focusing on fallacies that are common in viral classification. We emphasize that viruses are crucial contributors to the genomic and functional makeup of holobionts, organismal communities that behave as units of biological organization. Consequently, viruses cannot be considered taxonomic units because they challenge crucial concepts of organismality and individuality. Instead, they should be considered processes that integrate virions and their hosts into life cycles. Viruses harbor phylogenetic signatures of genetic transfer that compromise monophyly and the validity of deep taxonomic ranks. A focus on building phylogenetic networks using alignment-free methodologies and molecular structure can help mitigate the impasse, at least in part. Finally, structural phylogenomic analysis challenges the polyphyletic scenario of multiple viral origins adopted by virus taxonomy, defeating a polyphyletic origin and supporting instead an ancient cellular origin of viruses. We therefore, prompt abandoning deep ranks and urgently reevaluating the validity of taxonomic units and principles of virus classification. Frontiers Media S.A. 2023-08-03 /pmc/articles/PMC10435761/ /pubmed/37601376 http://dx.doi.org/10.3389/fmicb.2023.1240993 Text en Copyright © 2023 Caetano-Anollés, Claverie and Nasir. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Caetano-Anollés, Gustavo
Claverie, Jean-Michel
Nasir, Arshan
A critical analysis of the current state of virus taxonomy
title A critical analysis of the current state of virus taxonomy
title_full A critical analysis of the current state of virus taxonomy
title_fullStr A critical analysis of the current state of virus taxonomy
title_full_unstemmed A critical analysis of the current state of virus taxonomy
title_short A critical analysis of the current state of virus taxonomy
title_sort critical analysis of the current state of virus taxonomy
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10435761/
https://www.ncbi.nlm.nih.gov/pubmed/37601376
http://dx.doi.org/10.3389/fmicb.2023.1240993
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