Novel viruses of the family Partitiviridae discovered in Saccharomyces cerevisiae

It has been 49 years since the last discovery of a new virus family in the model yeast Saccharomyces cerevisiae. A large-scale screen to determine the diversity of double-stranded RNA (dsRNA) viruses in S. cerevisiae has identified multiple novel viruses from the family Partitiviridae that have been...

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Veröffentlicht in:PLoS pathogens 2023-06, Vol.19 (6), p.e1011418-e1011418
Hauptverfasser: Taggart, Nathan T, Crabtree, Angela M, Creagh, Jack W, Bizarria, Jr, Rodolfo, Li, Shunji, de la Higuera, Ignacio, Barnes, Jonathan E, Shipley, Mason A, Boyer, Josephine M, Stedman, Kenneth M, Ytreberg, F Marty, Rowley, Paul A
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container_issue 6
container_start_page e1011418
container_title PLoS pathogens
container_volume 19
creator Taggart, Nathan T
Crabtree, Angela M
Creagh, Jack W
Bizarria, Jr, Rodolfo
Li, Shunji
de la Higuera, Ignacio
Barnes, Jonathan E
Shipley, Mason A
Boyer, Josephine M
Stedman, Kenneth M
Ytreberg, F Marty
Rowley, Paul A
description It has been 49 years since the last discovery of a new virus family in the model yeast Saccharomyces cerevisiae. A large-scale screen to determine the diversity of double-stranded RNA (dsRNA) viruses in S. cerevisiae has identified multiple novel viruses from the family Partitiviridae that have been previously shown to infect plants, fungi, protozoans, and insects. Most S. cerevisiae partitiviruses (ScPVs) are associated with strains of yeasts isolated from coffee and cacao beans. The presence of partitiviruses was confirmed by sequencing the viral dsRNAs and purifying and visualizing isometric, non-enveloped viral particles. ScPVs have a typical bipartite genome encoding an RNA-dependent RNA polymerase (RdRP) and a coat protein (CP). Phylogenetic analysis of ScPVs identified three species of ScPV, which are most closely related to viruses of the genus Cryspovirus from the mammalian pathogenic protozoan Cryptosporidium parvum. Molecular modeling of the ScPV RdRP revealed a conserved tertiary structure and catalytic site organization when compared to the RdRPs of the Picornaviridae. The ScPV CP is the smallest so far identified in the Partitiviridae and has structural homology with the CP of other partitiviruses but likely lacks a protrusion domain that is a conspicuous feature of other partitivirus particles. ScPVs were stably maintained during laboratory growth and were successfully transferred to haploid progeny after sporulation, which provides future opportunities to study partitivirus-host interactions using the powerful genetic tools available for the model organism S. cerevisiae.
doi_str_mv 10.1371/journal.ppat.1011418
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A large-scale screen to determine the diversity of double-stranded RNA (dsRNA) viruses in S. cerevisiae has identified multiple novel viruses from the family Partitiviridae that have been previously shown to infect plants, fungi, protozoans, and insects. Most S. cerevisiae partitiviruses (ScPVs) are associated with strains of yeasts isolated from coffee and cacao beans. The presence of partitiviruses was confirmed by sequencing the viral dsRNAs and purifying and visualizing isometric, non-enveloped viral particles. ScPVs have a typical bipartite genome encoding an RNA-dependent RNA polymerase (RdRP) and a coat protein (CP). Phylogenetic analysis of ScPVs identified three species of ScPV, which are most closely related to viruses of the genus Cryspovirus from the mammalian pathogenic protozoan Cryptosporidium parvum. Molecular modeling of the ScPV RdRP revealed a conserved tertiary structure and catalytic site organization when compared to the RdRPs of the Picornaviridae. The ScPV CP is the smallest so far identified in the Partitiviridae and has structural homology with the CP of other partitiviruses but likely lacks a protrusion domain that is a conspicuous feature of other partitivirus particles. ScPVs were stably maintained during laboratory growth and were successfully transferred to haploid progeny after sporulation, which provides future opportunities to study partitivirus-host interactions using the powerful genetic tools available for the model organism S. cerevisiae.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1011418</identifier><identifier>PMID: 37285383</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Amino acids ; Analysis ; Animals ; Biology and Life Sciences ; Brewer's yeast ; Cell division ; Coat protein ; Cocoa beans ; Coffee ; Control ; Cryptosporidiosis - genetics ; Cryptosporidium ; DNA-directed RNA polymerase ; Double Stranded RNA Viruses ; Double-stranded RNA ; Fermentation ; Fungal Viruses ; Fungi ; Genes ; Genome, Viral ; Genomes ; Genomics ; Homology ; Host-virus relationships ; Identification and classification ; Infections ; Insects ; Isometric ; Mammals ; Medicine and Health Sciences ; Methods ; Molecular modelling ; Molecular weight ; Partitiviridae ; Phylogeny ; Physiology ; Protein structure ; Research and Analysis Methods ; Ribonucleic acid ; RNA ; RNA polymerase ; RNA Viruses ; RNA, Double-Stranded ; RNA, Viral - genetics ; RNA-Dependent RNA Polymerase - genetics ; RNA-directed RNA polymerase ; Saccharomyces cerevisiae ; Saccharomyces cerevisiae - genetics ; Satellites ; Sporulation ; Taxonomy ; Tertiary structure ; Toxins ; Viruses ; Yeast ; Yeasts</subject><ispartof>PLoS pathogens, 2023-06, Vol.19 (6), p.e1011418-e1011418</ispartof><rights>Copyright: © 2023 Taggart et al. 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A large-scale screen to determine the diversity of double-stranded RNA (dsRNA) viruses in S. cerevisiae has identified multiple novel viruses from the family Partitiviridae that have been previously shown to infect plants, fungi, protozoans, and insects. Most S. cerevisiae partitiviruses (ScPVs) are associated with strains of yeasts isolated from coffee and cacao beans. The presence of partitiviruses was confirmed by sequencing the viral dsRNAs and purifying and visualizing isometric, non-enveloped viral particles. ScPVs have a typical bipartite genome encoding an RNA-dependent RNA polymerase (RdRP) and a coat protein (CP). Phylogenetic analysis of ScPVs identified three species of ScPV, which are most closely related to viruses of the genus Cryspovirus from the mammalian pathogenic protozoan Cryptosporidium parvum. Molecular modeling of the ScPV RdRP revealed a conserved tertiary structure and catalytic site organization when compared to the RdRPs of the Picornaviridae. 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genetics</subject><subject>RNA-Dependent RNA Polymerase - genetics</subject><subject>RNA-directed RNA polymerase</subject><subject>Saccharomyces cerevisiae</subject><subject>Saccharomyces cerevisiae - genetics</subject><subject>Satellites</subject><subject>Sporulation</subject><subject>Taxonomy</subject><subject>Tertiary structure</subject><subject>Toxins</subject><subject>Viruses</subject><subject>Yeast</subject><subject>Yeasts</subject><issn>1553-7374</issn><issn>1553-7366</issn><issn>1553-7374</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqVkk1v1DAQhiMEoqXwDxBEcIHDLnYcx84JVRUfK1Xlo3C2JhN716tsvNjOiv33OGxadVEvKAdH42femXc8Wfackjllgr5bu8H30M23W4hzSigtqXyQnVLO2UwwUT6883-SPQlhTUhJGa0eZydMFJIzyU6zb1dup7t8Z_0QdMidyeNK5wY2ttvnX8FHG226tC3ovLUBE-11m9s-vwbEFXi32WNKxBTe2WBBP80eGeiCfjadZ9nPjx9-XHyeXX75tLg4v5xhJes4A2wM50hR8LbRHBspmhK4hlIbKQpTItQNoqGsqolhjMuWyUpKg23Z8GTsLHt50N12LqhpGkEVMvliPE0jEYsD0TpYq623G_B75cCqvwHnl2o0iJ1WBSl5LQQ1tYASWpZKM90AmAqxFASS1vup2tBsdIu6jx66I9Hjm96u1NLtFCWFpFyO_b46KLgQrQpoo8YVur7XGBWtZUmJTNCbqYx3vwYdotqkoeuug167YXRXsFrWNRvdvf4HvX8GE7WEZNP2xqXucBRV54JXjFBSs0TN76HS1-qNTT1qY1P8KOHtUUJiov4dlzCEoBbX3_-DvTpmywOL3oXgtbmdMCVqXPsbk2pcezWtfUp7cfd1bpNu9pz9AaOf_nc</recordid><startdate>20230607</startdate><enddate>20230607</enddate><creator>Taggart, Nathan T</creator><creator>Crabtree, Angela M</creator><creator>Creagh, Jack W</creator><creator>Bizarria, Jr, Rodolfo</creator><creator>Li, Shunji</creator><creator>de la Higuera, Ignacio</creator><creator>Barnes, Jonathan E</creator><creator>Shipley, Mason A</creator><creator>Boyer, Josephine M</creator><creator>Stedman, Kenneth M</creator><creator>Ytreberg, F Marty</creator><creator>Rowley, Paul A</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>ISN</scope><scope>ISR</scope><scope>3V.</scope><scope>7QL</scope><scope>7U9</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><scope>OTOTI</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-3590-5139</orcidid><orcidid>https://orcid.org/0000000235905139</orcidid></search><sort><creationdate>20230607</creationdate><title>Novel viruses of the family Partitiviridae discovered in Saccharomyces cerevisiae</title><author>Taggart, Nathan T ; Crabtree, Angela M ; Creagh, Jack W ; Bizarria, Jr, Rodolfo ; Li, Shunji ; de la Higuera, Ignacio ; Barnes, Jonathan E ; Shipley, Mason A ; Boyer, Josephine M ; Stedman, Kenneth M ; Ytreberg, F Marty ; Rowley, Paul A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c689t-acbf55c1c75dbe5cb87b4a5ea4ef872f4ca9bccf13690f3358d38688fcd4b5553</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Amino acids</topic><topic>Analysis</topic><topic>Animals</topic><topic>Biology and Life Sciences</topic><topic>Brewer's yeast</topic><topic>Cell division</topic><topic>Coat protein</topic><topic>Cocoa beans</topic><topic>Coffee</topic><topic>Control</topic><topic>Cryptosporidiosis - 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The ScPV CP is the smallest so far identified in the Partitiviridae and has structural homology with the CP of other partitiviruses but likely lacks a protrusion domain that is a conspicuous feature of other partitivirus particles. ScPVs were stably maintained during laboratory growth and were successfully transferred to haploid progeny after sporulation, which provides future opportunities to study partitivirus-host interactions using the powerful genetic tools available for the model organism S. cerevisiae.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>37285383</pmid><doi>10.1371/journal.ppat.1011418</doi><tpages>e1011418</tpages><orcidid>https://orcid.org/0000-0002-3590-5139</orcidid><orcidid>https://orcid.org/0000000235905139</orcidid><oa>free_for_read</oa></addata></record>
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subjects Amino acids
Analysis
Animals
Biology and Life Sciences
Brewer's yeast
Cell division
Coat protein
Cocoa beans
Coffee
Control
Cryptosporidiosis - genetics
Cryptosporidium
DNA-directed RNA polymerase
Double Stranded RNA Viruses
Double-stranded RNA
Fermentation
Fungal Viruses
Fungi
Genes
Genome, Viral
Genomes
Genomics
Homology
Host-virus relationships
Identification and classification
Infections
Insects
Isometric
Mammals
Medicine and Health Sciences
Methods
Molecular modelling
Molecular weight
Partitiviridae
Phylogeny
Physiology
Protein structure
Research and Analysis Methods
Ribonucleic acid
RNA
RNA polymerase
RNA Viruses
RNA, Double-Stranded
RNA, Viral - genetics
RNA-Dependent RNA Polymerase - genetics
RNA-directed RNA polymerase
Saccharomyces cerevisiae
Saccharomyces cerevisiae - genetics
Satellites
Sporulation
Taxonomy
Tertiary structure
Toxins
Viruses
Yeast
Yeasts
title Novel viruses of the family Partitiviridae discovered in Saccharomyces cerevisiae
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