Unraveling the genetic diversity and phylogeny of Leishmania RNA virus 1 strains of infected Leishmania isolates circulating in French Guiana
Leishmania RNA virus type 1 (LRV1) is an endosymbiont of some Leishmania (Vianna) species in South America. Presence of LRV1 in parasites exacerbates disease severity in animal models and humans, related to a disproportioned innate immune response, and is correlated with drug treatment failures in h...
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| Veröffentlicht in: | PLoS neglected tropical diseases 2017-07, Vol.11 (7), p.e0005764-e0005764 |
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| creator | Tirera, Sourakhata Ginouves, Marine Donato, Damien Caballero, Ignacio S Bouchier, Christiane Lavergne, Anne Bourreau, Eliane Mosnier, Emilie Vantilcke, Vincent Couppié, Pierre Prevot, Ghislaine Lacoste, Vincent |
| description | Leishmania RNA virus type 1 (LRV1) is an endosymbiont of some Leishmania (Vianna) species in South America. Presence of LRV1 in parasites exacerbates disease severity in animal models and humans, related to a disproportioned innate immune response, and is correlated with drug treatment failures in humans. Although the virus was identified decades ago, its genomic diversity has been overlooked until now.
We subjected LRV1 strains from 19 L. (V.) guyanensis and one L. (V.) braziliensis isolates obtained from cutaneous leishmaniasis samples identified throughout French Guiana with next-generation sequencing and de novo sequence assembly. We generated and analyzed 24 unique LRV1 sequences over their full-length coding regions. Multiple alignment of these new sequences revealed variability (0.5%-23.5%) across the entire sequence except for highly conserved motifs within the 5' untranslated region. Phylogenetic analyses showed that viral genomes of L. (V.) guyanensis grouped into five distinct clusters. They further showed a species-dependent clustering between viral genomes of L. (V.) guyanensis and L. (V.) braziliensis, confirming a long-term co-evolutionary history. Noteworthy, we identified cases of multiple LRV1 infections in three of the 20 Leishmania isolates.
Here, we present the first-ever estimate of LRV1 genomic diversity that exists in Leishmania (V.) guyanensis parasites. Genetic characterization and phylogenetic analyses of these viruses has shed light on their evolutionary relationships. To our knowledge, this study is also the first to report cases of multiple LRV1 infections in some parasites. Finally, this work has made it possible to develop molecular tools for adequate identification and genotyping of LRV1 strains for diagnostic purposes. Given the suspected worsening role of LRV1 infection in the pathogenesis of human leishmaniasis, these data have a major impact from a clinical viewpoint and for the management of Leishmania-infected patients. |
| doi_str_mv | 10.1371/journal.pntd.0005764 |
| format | Article |
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We subjected LRV1 strains from 19 L. (V.) guyanensis and one L. (V.) braziliensis isolates obtained from cutaneous leishmaniasis samples identified throughout French Guiana with next-generation sequencing and de novo sequence assembly. We generated and analyzed 24 unique LRV1 sequences over their full-length coding regions. Multiple alignment of these new sequences revealed variability (0.5%-23.5%) across the entire sequence except for highly conserved motifs within the 5' untranslated region. Phylogenetic analyses showed that viral genomes of L. (V.) guyanensis grouped into five distinct clusters. They further showed a species-dependent clustering between viral genomes of L. (V.) guyanensis and L. (V.) braziliensis, confirming a long-term co-evolutionary history. Noteworthy, we identified cases of multiple LRV1 infections in three of the 20 Leishmania isolates.
Here, we present the first-ever estimate of LRV1 genomic diversity that exists in Leishmania (V.) guyanensis parasites. Genetic characterization and phylogenetic analyses of these viruses has shed light on their evolutionary relationships. To our knowledge, this study is also the first to report cases of multiple LRV1 infections in some parasites. Finally, this work has made it possible to develop molecular tools for adequate identification and genotyping of LRV1 strains for diagnostic purposes. Given the suspected worsening role of LRV1 infection in the pathogenesis of human leishmaniasis, these data have a major impact from a clinical viewpoint and for the management of Leishmania-infected patients.</description><identifier>ISSN: 1935-2735</identifier><identifier>ISSN: 1935-2727</identifier><identifier>EISSN: 1935-2735</identifier><identifier>DOI: 10.1371/journal.pntd.0005764</identifier><identifier>PMID: 28715422</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adult ; Aged ; Analysis ; Animal diseases ; Animal models ; Biodiversity ; Bioinformatics ; Biology and Life Sciences ; Cluster Analysis ; Clustering ; Clusters ; Computer and Information Sciences ; Conserved sequence ; Cutaneous leishmaniasis ; Defence mechanisms ; Diagnostic systems ; Drugs ; Evolution ; Evolutionary genetics ; Failures ; Female ; French Guiana ; Funding ; Genetic diversity ; Genetic Variation ; Genetics ; Genome, Viral ; Genomes ; Genotyping ; Health aspects ; History ; Human genetics ; Humans ; Identification ; Immune response ; Immune system ; Immunity ; Infections ; Innate immunity ; Laboratories ; Leishmania ; Leishmania - isolation & purification ; Leishmania - virology ; Leishmaniasis ; Leishmaniasis - parasitology ; Leishmaniavirus ; Leishmaniavirus - classification ; Leishmaniavirus - genetics ; Leishmaniavirus - isolation & purification ; Life Sciences ; Male ; Management ; Medicine ; Medicine and Health Sciences ; Microbiological strains ; Microbiology and Parasitology ; Middle Aged ; Molecular biology ; Multinational space ventures ; Nucleic acids ; Nucleotide sequence ; Parasites ; Parasitic diseases ; Parasitology ; Pathogenesis ; Phylogenetics ; Phylogeny ; Research and analysis methods ; Ribonucleic acid ; RNA ; RNA viruses ; RNA, Viral ; RNA, Viral - genetics ; Sequence Alignment ; Sequence Analysis, DNA ; Sequencing ; Strains ; Strains (organisms) ; Taxonomy ; Tropical diseases ; Variability ; Vector-borne diseases ; Virology ; Viruses ; Young Adult</subject><ispartof>PLoS neglected tropical diseases, 2017-07, Vol.11 (7), p.e0005764-e0005764</ispartof><rights>COPYRIGHT 2017 Public Library of Science</rights><rights>2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: isolates circulating in French Guiana. PLoS Negl Trop Dis 11(7): e0005764. https://doi.org/10.1371/journal.pntd.0005764</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>2017 Tirera et al 2017 Tirera et al</rights><rights>2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: isolates circulating in French Guiana. PLoS Negl Trop Dis 11(7): e0005764. https://doi.org/10.1371/journal.pntd.0005764</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c662t-396d1dabbc5d471cc1c7538809b01f8928699db02b807e6159dda96b98d4eb73</citedby><cites>FETCH-LOGICAL-c662t-396d1dabbc5d471cc1c7538809b01f8928699db02b807e6159dda96b98d4eb73</cites><orcidid>0000-0002-3173-4053 ; 0000-0002-7268-4953 ; 0000-0003-3549-1543 ; 0000-0002-5304-5574 ; 0000-0002-6004-3323</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5531682/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5531682/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,729,782,786,866,887,2106,2932,23875,27933,27934,53800,53802</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28715422$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://riip.hal.science/pasteur-01583523$$DView record in HAL$$Hfree_for_read</backlink></links><search><contributor>Tibayrenc, Michel</contributor><creatorcontrib>Tirera, Sourakhata</creatorcontrib><creatorcontrib>Ginouves, Marine</creatorcontrib><creatorcontrib>Donato, Damien</creatorcontrib><creatorcontrib>Caballero, Ignacio S</creatorcontrib><creatorcontrib>Bouchier, Christiane</creatorcontrib><creatorcontrib>Lavergne, Anne</creatorcontrib><creatorcontrib>Bourreau, Eliane</creatorcontrib><creatorcontrib>Mosnier, Emilie</creatorcontrib><creatorcontrib>Vantilcke, Vincent</creatorcontrib><creatorcontrib>Couppié, Pierre</creatorcontrib><creatorcontrib>Prevot, Ghislaine</creatorcontrib><creatorcontrib>Lacoste, Vincent</creatorcontrib><title>Unraveling the genetic diversity and phylogeny of Leishmania RNA virus 1 strains of infected Leishmania isolates circulating in French Guiana</title><title>PLoS neglected tropical diseases</title><addtitle>PLoS Negl Trop Dis</addtitle><description>Leishmania RNA virus type 1 (LRV1) is an endosymbiont of some Leishmania (Vianna) species in South America. Presence of LRV1 in parasites exacerbates disease severity in animal models and humans, related to a disproportioned innate immune response, and is correlated with drug treatment failures in humans. Although the virus was identified decades ago, its genomic diversity has been overlooked until now.
We subjected LRV1 strains from 19 L. (V.) guyanensis and one L. (V.) braziliensis isolates obtained from cutaneous leishmaniasis samples identified throughout French Guiana with next-generation sequencing and de novo sequence assembly. We generated and analyzed 24 unique LRV1 sequences over their full-length coding regions. Multiple alignment of these new sequences revealed variability (0.5%-23.5%) across the entire sequence except for highly conserved motifs within the 5' untranslated region. Phylogenetic analyses showed that viral genomes of L. (V.) guyanensis grouped into five distinct clusters. They further showed a species-dependent clustering between viral genomes of L. (V.) guyanensis and L. (V.) braziliensis, confirming a long-term co-evolutionary history. Noteworthy, we identified cases of multiple LRV1 infections in three of the 20 Leishmania isolates.
Here, we present the first-ever estimate of LRV1 genomic diversity that exists in Leishmania (V.) guyanensis parasites. Genetic characterization and phylogenetic analyses of these viruses has shed light on their evolutionary relationships. To our knowledge, this study is also the first to report cases of multiple LRV1 infections in some parasites. Finally, this work has made it possible to develop molecular tools for adequate identification and genotyping of LRV1 strains for diagnostic purposes. Given the suspected worsening role of LRV1 infection in the pathogenesis of human leishmaniasis, these data have a major impact from a clinical viewpoint and for the management of Leishmania-infected patients.</description><subject>Adult</subject><subject>Aged</subject><subject>Analysis</subject><subject>Animal diseases</subject><subject>Animal models</subject><subject>Biodiversity</subject><subject>Bioinformatics</subject><subject>Biology and Life Sciences</subject><subject>Cluster Analysis</subject><subject>Clustering</subject><subject>Clusters</subject><subject>Computer and Information Sciences</subject><subject>Conserved sequence</subject><subject>Cutaneous leishmaniasis</subject><subject>Defence mechanisms</subject><subject>Diagnostic systems</subject><subject>Drugs</subject><subject>Evolution</subject><subject>Evolutionary genetics</subject><subject>Failures</subject><subject>Female</subject><subject>French Guiana</subject><subject>Funding</subject><subject>Genetic diversity</subject><subject>Genetic Variation</subject><subject>Genetics</subject><subject>Genome, Viral</subject><subject>Genomes</subject><subject>Genotyping</subject><subject>Health aspects</subject><subject>History</subject><subject>Human genetics</subject><subject>Humans</subject><subject>Identification</subject><subject>Immune response</subject><subject>Immune system</subject><subject>Immunity</subject><subject>Infections</subject><subject>Innate immunity</subject><subject>Laboratories</subject><subject>Leishmania</subject><subject>Leishmania - isolation & purification</subject><subject>Leishmania - virology</subject><subject>Leishmaniasis</subject><subject>Leishmaniasis - parasitology</subject><subject>Leishmaniavirus</subject><subject>Leishmaniavirus - classification</subject><subject>Leishmaniavirus - genetics</subject><subject>Leishmaniavirus - isolation & purification</subject><subject>Life Sciences</subject><subject>Male</subject><subject>Management</subject><subject>Medicine</subject><subject>Medicine and Health Sciences</subject><subject>Microbiological strains</subject><subject>Microbiology and Parasitology</subject><subject>Middle Aged</subject><subject>Molecular biology</subject><subject>Multinational space ventures</subject><subject>Nucleic acids</subject><subject>Nucleotide sequence</subject><subject>Parasites</subject><subject>Parasitic diseases</subject><subject>Parasitology</subject><subject>Pathogenesis</subject><subject>Phylogenetics</subject><subject>Phylogeny</subject><subject>Research and analysis methods</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA viruses</subject><subject>RNA, Viral</subject><subject>RNA, Viral - genetics</subject><subject>Sequence Alignment</subject><subject>Sequence Analysis, DNA</subject><subject>Sequencing</subject><subject>Strains</subject><subject>Strains (organisms)</subject><subject>Taxonomy</subject><subject>Tropical diseases</subject><subject>Variability</subject><subject>Vector-borne diseases</subject><subject>Virology</subject><subject>Viruses</subject><subject>Young 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Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>ProQuest Central</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 3: Aquatic Pollution & Environmental Quality</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Access via ProQuest (Open Access)</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS neglected tropical diseases</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Tirera, Sourakhata</au><au>Ginouves, Marine</au><au>Donato, Damien</au><au>Caballero, Ignacio S</au><au>Bouchier, Christiane</au><au>Lavergne, Anne</au><au>Bourreau, Eliane</au><au>Mosnier, Emilie</au><au>Vantilcke, Vincent</au><au>Couppié, Pierre</au><au>Prevot, Ghislaine</au><au>Lacoste, Vincent</au><au>Tibayrenc, Michel</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Unraveling the genetic diversity and phylogeny of Leishmania RNA virus 1 strains of infected Leishmania isolates circulating in French Guiana</atitle><jtitle>PLoS neglected tropical diseases</jtitle><addtitle>PLoS Negl Trop Dis</addtitle><date>2017-07-17</date><risdate>2017</risdate><volume>11</volume><issue>7</issue><spage>e0005764</spage><epage>e0005764</epage><pages>e0005764-e0005764</pages><issn>1935-2735</issn><issn>1935-2727</issn><eissn>1935-2735</eissn><abstract>Leishmania RNA virus type 1 (LRV1) is an endosymbiont of some Leishmania (Vianna) species in South America. Presence of LRV1 in parasites exacerbates disease severity in animal models and humans, related to a disproportioned innate immune response, and is correlated with drug treatment failures in humans. Although the virus was identified decades ago, its genomic diversity has been overlooked until now.
We subjected LRV1 strains from 19 L. (V.) guyanensis and one L. (V.) braziliensis isolates obtained from cutaneous leishmaniasis samples identified throughout French Guiana with next-generation sequencing and de novo sequence assembly. We generated and analyzed 24 unique LRV1 sequences over their full-length coding regions. Multiple alignment of these new sequences revealed variability (0.5%-23.5%) across the entire sequence except for highly conserved motifs within the 5' untranslated region. Phylogenetic analyses showed that viral genomes of L. (V.) guyanensis grouped into five distinct clusters. They further showed a species-dependent clustering between viral genomes of L. (V.) guyanensis and L. (V.) braziliensis, confirming a long-term co-evolutionary history. Noteworthy, we identified cases of multiple LRV1 infections in three of the 20 Leishmania isolates.
Here, we present the first-ever estimate of LRV1 genomic diversity that exists in Leishmania (V.) guyanensis parasites. Genetic characterization and phylogenetic analyses of these viruses has shed light on their evolutionary relationships. To our knowledge, this study is also the first to report cases of multiple LRV1 infections in some parasites. Finally, this work has made it possible to develop molecular tools for adequate identification and genotyping of LRV1 strains for diagnostic purposes. Given the suspected worsening role of LRV1 infection in the pathogenesis of human leishmaniasis, these data have a major impact from a clinical viewpoint and for the management of Leishmania-infected patients.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>28715422</pmid><doi>10.1371/journal.pntd.0005764</doi><orcidid>https://orcid.org/0000-0002-3173-4053</orcidid><orcidid>https://orcid.org/0000-0002-7268-4953</orcidid><orcidid>https://orcid.org/0000-0003-3549-1543</orcidid><orcidid>https://orcid.org/0000-0002-5304-5574</orcidid><orcidid>https://orcid.org/0000-0002-6004-3323</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1935-2735 |
| ispartof | PLoS neglected tropical diseases, 2017-07, Vol.11 (7), p.e0005764-e0005764 |
| issn | 1935-2735 1935-2727 1935-2735 |
| language | eng |
| recordid | cdi_plos_journals_1929416104 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central Open Access; Public Library of Science (PLoS) Journals Open Access; PubMed Central |
| subjects | Adult Aged Analysis Animal diseases Animal models Biodiversity Bioinformatics Biology and Life Sciences Cluster Analysis Clustering Clusters Computer and Information Sciences Conserved sequence Cutaneous leishmaniasis Defence mechanisms Diagnostic systems Drugs Evolution Evolutionary genetics Failures Female French Guiana Funding Genetic diversity Genetic Variation Genetics Genome, Viral Genomes Genotyping Health aspects History Human genetics Humans Identification Immune response Immune system Immunity Infections Innate immunity Laboratories Leishmania Leishmania - isolation & purification Leishmania - virology Leishmaniasis Leishmaniasis - parasitology Leishmaniavirus Leishmaniavirus - classification Leishmaniavirus - genetics Leishmaniavirus - isolation & purification Life Sciences Male Management Medicine Medicine and Health Sciences Microbiological strains Microbiology and Parasitology Middle Aged Molecular biology Multinational space ventures Nucleic acids Nucleotide sequence Parasites Parasitic diseases Parasitology Pathogenesis Phylogenetics Phylogeny Research and analysis methods Ribonucleic acid RNA RNA viruses RNA, Viral RNA, Viral - genetics Sequence Alignment Sequence Analysis, DNA Sequencing Strains Strains (organisms) Taxonomy Tropical diseases Variability Vector-borne diseases Virology Viruses Young Adult |
| title | Unraveling the genetic diversity and phylogeny of Leishmania RNA virus 1 strains of infected Leishmania isolates circulating in French Guiana |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-02T06%3A39%3A38IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Unraveling%20the%20genetic%20diversity%20and%20phylogeny%20of%20Leishmania%20RNA%20virus%201%20strains%20of%20infected%20Leishmania%20isolates%20circulating%20in%20French%20Guiana&rft.jtitle=PLoS%20neglected%20tropical%20diseases&rft.au=Tirera,%20Sourakhata&rft.date=2017-07-17&rft.volume=11&rft.issue=7&rft.spage=e0005764&rft.epage=e0005764&rft.pages=e0005764-e0005764&rft.issn=1935-2735&rft.eissn=1935-2735&rft_id=info:doi/10.1371/journal.pntd.0005764&rft_dat=%3Cgale_plos_%3EA499694258%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1929416104&rft_id=info:pmid/28715422&rft_galeid=A499694258&rft_doaj_id=oai_doaj_org_article_2a107f869ff34bc590e71c76b93bb1e1&rfr_iscdi=true |