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Slippery when wet: cross-species transmission of divergent coronaviruses in bony and jawless fish and the evolutionary history of the Coronaviridae

The Nidovirales comprise a genetically diverse group of positive-sense single-stranded RNA virus families that infect a range of invertebrate and vertebrate hosts. Recent metagenomic studies have identified nido-like virus sequences, particularly those related to the Coronaviridae, in a range of aqu...

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Autores principales: Miller, Allison K, Mifsud, Jonathon C O, Costa, Vincenzo A, Grimwood, Rebecca M, Kitson, Jane, Baker, Cindy, Brosnahan, Cara L, Pande, Anjali, Holmes, Edward C, Gemmell, Neil J, Geoghegan, Jemma L
Formato: Online Artículo Texto
Lenguaje:English
Publicado: OUP 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8244743/
https://www.ncbi.nlm.nih.gov/pubmed/34527280
http://dx.doi.org/10.1093/ve/veab050
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author Miller, Allison K
Mifsud, Jonathon C O
Costa, Vincenzo A
Grimwood, Rebecca M
Kitson, Jane
Baker, Cindy
Brosnahan, Cara L
Pande, Anjali
Holmes, Edward C
Gemmell, Neil J
Geoghegan, Jemma L
author_facet Miller, Allison K
Mifsud, Jonathon C O
Costa, Vincenzo A
Grimwood, Rebecca M
Kitson, Jane
Baker, Cindy
Brosnahan, Cara L
Pande, Anjali
Holmes, Edward C
Gemmell, Neil J
Geoghegan, Jemma L
author_sort Miller, Allison K
collection PubMed
description The Nidovirales comprise a genetically diverse group of positive-sense single-stranded RNA virus families that infect a range of invertebrate and vertebrate hosts. Recent metagenomic studies have identified nido-like virus sequences, particularly those related to the Coronaviridae, in a range of aquatic hosts including fish, amphibians, and reptiles. We sought to identify additional members of the Coronaviridae in both bony and jawless fish through a combination of total RNA sequencing (meta-transcriptomics) and data mining of published RNA sequencing data and from this reveal more of the long-term patterns and processes of coronavirus evolution. Accordingly, we identified a number of divergent viruses that fell within the Letovirinae subfamily of the Coronaviridae, including those in a jawless fish—the pouched lamprey. By mining fish transcriptome data, we identified additional virus transcripts matching these viruses in bony fish from both marine and freshwater environments. These new viruses retained sequence conservation in the RNA-dependant RNA polymerase across the Coronaviridae but formed a distinct and diverse phylogenetic group. Although there are broad-scale topological similarities between the phylogenies of the major groups of coronaviruses and their vertebrate hosts, the evolutionary relationship of viruses within the Letovirinae does not mirror that of their hosts. For example, the coronavirus found in the pouched lamprey fell within the phylogenetic diversity of bony fish letoviruses, indicative of past host switching events. Hence, despite possessing a phylogenetic history that likely spans the entire history of the vertebrates, coronavirus evolution has been characterised by relatively frequent cross-species transmission, particularly in hosts that reside in aquatic habitats.
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spelling pubmed-82447432021-07-01 Slippery when wet: cross-species transmission of divergent coronaviruses in bony and jawless fish and the evolutionary history of the Coronaviridae Miller, Allison K Mifsud, Jonathon C O Costa, Vincenzo A Grimwood, Rebecca M Kitson, Jane Baker, Cindy Brosnahan, Cara L Pande, Anjali Holmes, Edward C Gemmell, Neil J Geoghegan, Jemma L Virus Evol Research Article The Nidovirales comprise a genetically diverse group of positive-sense single-stranded RNA virus families that infect a range of invertebrate and vertebrate hosts. Recent metagenomic studies have identified nido-like virus sequences, particularly those related to the Coronaviridae, in a range of aquatic hosts including fish, amphibians, and reptiles. We sought to identify additional members of the Coronaviridae in both bony and jawless fish through a combination of total RNA sequencing (meta-transcriptomics) and data mining of published RNA sequencing data and from this reveal more of the long-term patterns and processes of coronavirus evolution. Accordingly, we identified a number of divergent viruses that fell within the Letovirinae subfamily of the Coronaviridae, including those in a jawless fish—the pouched lamprey. By mining fish transcriptome data, we identified additional virus transcripts matching these viruses in bony fish from both marine and freshwater environments. These new viruses retained sequence conservation in the RNA-dependant RNA polymerase across the Coronaviridae but formed a distinct and diverse phylogenetic group. Although there are broad-scale topological similarities between the phylogenies of the major groups of coronaviruses and their vertebrate hosts, the evolutionary relationship of viruses within the Letovirinae does not mirror that of their hosts. For example, the coronavirus found in the pouched lamprey fell within the phylogenetic diversity of bony fish letoviruses, indicative of past host switching events. Hence, despite possessing a phylogenetic history that likely spans the entire history of the vertebrates, coronavirus evolution has been characterised by relatively frequent cross-species transmission, particularly in hosts that reside in aquatic habitats. OUP 2021-05-31 /pmc/articles/PMC8244743/ /pubmed/34527280 http://dx.doi.org/10.1093/ve/veab050 Text en © The Author(s) 2021. Published by Oxford University Press. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) ), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Miller, Allison K
Mifsud, Jonathon C O
Costa, Vincenzo A
Grimwood, Rebecca M
Kitson, Jane
Baker, Cindy
Brosnahan, Cara L
Pande, Anjali
Holmes, Edward C
Gemmell, Neil J
Geoghegan, Jemma L
Slippery when wet: cross-species transmission of divergent coronaviruses in bony and jawless fish and the evolutionary history of the Coronaviridae
title Slippery when wet: cross-species transmission of divergent coronaviruses in bony and jawless fish and the evolutionary history of the Coronaviridae
title_full Slippery when wet: cross-species transmission of divergent coronaviruses in bony and jawless fish and the evolutionary history of the Coronaviridae
title_fullStr Slippery when wet: cross-species transmission of divergent coronaviruses in bony and jawless fish and the evolutionary history of the Coronaviridae
title_full_unstemmed Slippery when wet: cross-species transmission of divergent coronaviruses in bony and jawless fish and the evolutionary history of the Coronaviridae
title_short Slippery when wet: cross-species transmission of divergent coronaviruses in bony and jawless fish and the evolutionary history of the Coronaviridae
title_sort slippery when wet: cross-species transmission of divergent coronaviruses in bony and jawless fish and the evolutionary history of the coronaviridae
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8244743/
https://www.ncbi.nlm.nih.gov/pubmed/34527280
http://dx.doi.org/10.1093/ve/veab050
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