Evidence for an ancient aquatic origin of the RNA viral order Articulavirales

The emergence of previously unknown disease-causing viruses in mammals is in part the result of a long-term evolutionary process. Reconstructing the deep phylogenetic histories of viruses helps identify major evolutionary transitions and contextualizes the emergence of viruses in new hosts. We used...

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Main Authors: Petrone, M.E., Parry, R., Mifsud, J.C.O., Van Brussel, K., Vorhees, I., Richards, Zoe, Holmes, E.C.
Format: Journal Article
Language:English
Published: 2023
Subjects:
Online Access:http://purl.org/au-research/grants/arc/LP160101508
http://hdl.handle.net/20.500.11937/96165
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author Petrone, M.E.
Parry, R.
Mifsud, J.C.O.
Van Brussel, K.
Vorhees, I.
Richards, Zoe
Holmes, E.C.
author_facet Petrone, M.E.
Parry, R.
Mifsud, J.C.O.
Van Brussel, K.
Vorhees, I.
Richards, Zoe
Holmes, E.C.
author_sort Petrone, M.E.
building Curtin Institutional Repository
collection Online Access
description The emergence of previously unknown disease-causing viruses in mammals is in part the result of a long-term evolutionary process. Reconstructing the deep phylogenetic histories of viruses helps identify major evolutionary transitions and contextualizes the emergence of viruses in new hosts. We used a combination of total RNA sequencing and transcriptome data mining to extend the diversity and evolutionary history of the RNA virus order Articulavirales, which includes the influenza viruses. We identified instances of Articulavirales in the invertebrate phylum Cnidaria (including corals), constituting a novel and divergent family that we provisionally named the “Cnidenomoviridae.” We further extended the evolutionary history of the influenza virus lineage by identifying four divergent, fish-associated influenza-like viruses, thereby supporting the hypothesis that fish were among the first hosts of influenza viruses. In addition, we substantially expanded the phylogenetic diversity of quaranjaviruses and proposed that this genus be reclassified as a family—the “Quaranjaviridae.” Within this putative family, we identified a novel arachnid-infecting genus, provisionally named “Cheliceravirus.” Notably, we observed a close phylogenetic relationship between the Crustacea- and Chelicerata-infecting “Quaranjaviridae” that is inconsistent with virus–host codivergence. Together, these data suggest that the Articulavirales has evolved over at least 600 million years, first emerging in aquatic animals. Importantly, the evolution of the Articulavirales was likely shaped by multiple aquatic–terrestrial transitions and substantial host jumps, some of which are still observable today.
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spelling curtin-20.500.11937-961652024-11-07T23:35:03Z Evidence for an ancient aquatic origin of the RNA viral order Articulavirales Petrone, M.E. Parry, R. Mifsud, J.C.O. Van Brussel, K. Vorhees, I. Richards, Zoe Holmes, E.C. Articulavirales Cnidaria evolution influenza virosphere Animals Humans Phylogeny RNA Viruses Influenza, Human Invertebrates Orthomyxoviridae RNA Evolution, Molecular RNA, Viral Mammals Animals Mammals Humans Invertebrates RNA Viruses Orthomyxoviridae RNA RNA, Viral Evolution, Molecular Phylogeny Influenza, Human The emergence of previously unknown disease-causing viruses in mammals is in part the result of a long-term evolutionary process. Reconstructing the deep phylogenetic histories of viruses helps identify major evolutionary transitions and contextualizes the emergence of viruses in new hosts. We used a combination of total RNA sequencing and transcriptome data mining to extend the diversity and evolutionary history of the RNA virus order Articulavirales, which includes the influenza viruses. We identified instances of Articulavirales in the invertebrate phylum Cnidaria (including corals), constituting a novel and divergent family that we provisionally named the “Cnidenomoviridae.” We further extended the evolutionary history of the influenza virus lineage by identifying four divergent, fish-associated influenza-like viruses, thereby supporting the hypothesis that fish were among the first hosts of influenza viruses. In addition, we substantially expanded the phylogenetic diversity of quaranjaviruses and proposed that this genus be reclassified as a family—the “Quaranjaviridae.” Within this putative family, we identified a novel arachnid-infecting genus, provisionally named “Cheliceravirus.” Notably, we observed a close phylogenetic relationship between the Crustacea- and Chelicerata-infecting “Quaranjaviridae” that is inconsistent with virus–host codivergence. Together, these data suggest that the Articulavirales has evolved over at least 600 million years, first emerging in aquatic animals. Importantly, the evolution of the Articulavirales was likely shaped by multiple aquatic–terrestrial transitions and substantial host jumps, some of which are still observable today. 2023 Journal Article http://hdl.handle.net/20.500.11937/96165 10.1073/pnas.2310529120 eng http://purl.org/au-research/grants/arc/LP160101508 https://creativecommons.org/licenses/by/4.0/ fulltext
spellingShingle Articulavirales
Cnidaria
evolution
influenza
virosphere
Animals
Humans
Phylogeny
RNA Viruses
Influenza, Human
Invertebrates
Orthomyxoviridae
RNA
Evolution, Molecular
RNA, Viral
Mammals
Animals
Mammals
Humans
Invertebrates
RNA Viruses
Orthomyxoviridae
RNA
RNA, Viral
Evolution, Molecular
Phylogeny
Influenza, Human
Petrone, M.E.
Parry, R.
Mifsud, J.C.O.
Van Brussel, K.
Vorhees, I.
Richards, Zoe
Holmes, E.C.
Evidence for an ancient aquatic origin of the RNA viral order Articulavirales
title Evidence for an ancient aquatic origin of the RNA viral order Articulavirales
title_full Evidence for an ancient aquatic origin of the RNA viral order Articulavirales
title_fullStr Evidence for an ancient aquatic origin of the RNA viral order Articulavirales
title_full_unstemmed Evidence for an ancient aquatic origin of the RNA viral order Articulavirales
title_short Evidence for an ancient aquatic origin of the RNA viral order Articulavirales
title_sort evidence for an ancient aquatic origin of the rna viral order articulavirales
topic Articulavirales
Cnidaria
evolution
influenza
virosphere
Animals
Humans
Phylogeny
RNA Viruses
Influenza, Human
Invertebrates
Orthomyxoviridae
RNA
Evolution, Molecular
RNA, Viral
Mammals
Animals
Mammals
Humans
Invertebrates
RNA Viruses
Orthomyxoviridae
RNA
RNA, Viral
Evolution, Molecular
Phylogeny
Influenza, Human
url http://purl.org/au-research/grants/arc/LP160101508
http://hdl.handle.net/20.500.11937/96165