Insights into the Host Range, Genetic Diversity, and Geographical Distribution of Jingmenviruses

ABSTRACT Jingmenvirus is a recently identified group of segmented RNA viruses phylogenetically linked with unsegmented Flaviviridae viruses. Primarily identified in various tick genera originating in China, Jingmenvirus geographical distribution has rapidly expanded to cover Africa, South America, C...

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Autores principales: Sarah Temmam, Thomas Bigot, Delphine Chrétien, Mathilde Gondard, Philippe Pérot, Virginie Pommelet, Evelyne Dufour, Stéphane Petres, Elodie Devillers, Thavry Hoem, Valérie Pinarello, Vibol Hul, Khamsing Vongphayloth, Jeffrey C. Hertz, Irène Loiseau, Marine Dumarest, Veasna Duong, Muriel Vayssier-Taussat, Marc Grandadam, Emmanuel Albina, Philippe Dussart, Sara Moutailler, Julien Cappelle, Paul T. Brey, Marc Eloit
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Publicado: American Society for Microbiology 2019
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spelling oai:doaj.org-article:b8cd568f403f4fa0add30b68ad69818e2021-11-15T15:22:24ZInsights into the Host Range, Genetic Diversity, and Geographical Distribution of Jingmenviruses10.1128/mSphere.00645-192379-5042https://doaj.org/article/b8cd568f403f4fa0add30b68ad69818e2019-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00645-19https://doaj.org/toc/2379-5042ABSTRACT Jingmenvirus is a recently identified group of segmented RNA viruses phylogenetically linked with unsegmented Flaviviridae viruses. Primarily identified in various tick genera originating in China, Jingmenvirus geographical distribution has rapidly expanded to cover Africa, South America, Caribbean, and Europe. The identification of Jingmen-related viruses in various mammals, including febrile humans, opens the possibility that Jingmenviruses may be novel tick-borne arboviruses. In this study, we aimed at increasing knowledge of the host range, genetic diversity, and geographical distribution of Jingmenviruses by reporting for the first time the identification of Jingmenviruses associated with Rhipicephalus microplus ticks originating in the French Antilles (Guadeloupe and Martinique islands), with Amblyomma testudinarium ticks in Lao PDR, and with Ixodes ricinus ticks in metropolitan France, and from urine of Pteropus lylei bats in Cambodia. Analyses of the relationships between the different Jingmenvirus genomes resulted in the identification of three main phylogenic subclades, each of them containing both tick-borne and mammal-borne strains, reinforcing the idea that Jingmenviruses may be considered as tick-borne arboviruses. Finally, we estimated the prevalence of Jingmenvirus-like infection using luciferase immunoprecipitation assay screening (LIPS) of asymptomatic humans and cattle highly exposed to tick bites. Among 70 French human, 153 Laotian human, and 200 Caribbean cattle sera tested, only one French human serum was found (slightly) positive, suggesting that the prevalence of Jingmenvirus human and cattle infections in these areas is probably low. IMPORTANCE Several arboviruses emerging as new pathogens for humans and domestic animals have recently raised public health concern and increased interest in the study of their host range and in detection of spillover events. Recently, a new group of segmented Flaviviridae-related viruses, the Jingmenviruses, has been identified worldwide in many invertebrate and vertebrate hosts, pointing out the issue of whether they belong to the arbovirus group. The study presented here combined whole-genome sequencing of three tick-borne Jingmenviruses and one bat-borne Jingmenvirus with comprehensive phylogenetic analyses and high-throughput serological screening of human and cattle populations exposed to these viruses to contribute to the knowledge of Jingmenvirus host range, geographical distribution, and mammalian exposure.Sarah TemmamThomas BigotDelphine ChrétienMathilde GondardPhilippe PérotVirginie PommeletEvelyne DufourStéphane PetresElodie DevillersThavry HoemValérie PinarelloVibol HulKhamsing VongphaylothJeffrey C. HertzIrène LoiseauMarine DumarestVeasna DuongMuriel Vayssier-TaussatMarc GrandadamEmmanuel AlbinaPhilippe DussartSara MoutaillerJulien CappellePaul T. BreyMarc EloitAmerican Society for MicrobiologyarticleJingmenvirusLIPSemergenceevolutionMicrobiologyQR1-502ENmSphere, Vol 4, Iss 6 (2019)
institution DOAJ
collection DOAJ
language EN
topic Jingmenvirus
LIPS
emergence
evolution
Microbiology
QR1-502
spellingShingle Jingmenvirus
LIPS
emergence
evolution
Microbiology
QR1-502
Sarah Temmam
Thomas Bigot
Delphine Chrétien
Mathilde Gondard
Philippe Pérot
Virginie Pommelet
Evelyne Dufour
Stéphane Petres
Elodie Devillers
Thavry Hoem
Valérie Pinarello
Vibol Hul
Khamsing Vongphayloth
Jeffrey C. Hertz
Irène Loiseau
Marine Dumarest
Veasna Duong
Muriel Vayssier-Taussat
Marc Grandadam
Emmanuel Albina
Philippe Dussart
Sara Moutailler
Julien Cappelle
Paul T. Brey
Marc Eloit
Insights into the Host Range, Genetic Diversity, and Geographical Distribution of Jingmenviruses
description ABSTRACT Jingmenvirus is a recently identified group of segmented RNA viruses phylogenetically linked with unsegmented Flaviviridae viruses. Primarily identified in various tick genera originating in China, Jingmenvirus geographical distribution has rapidly expanded to cover Africa, South America, Caribbean, and Europe. The identification of Jingmen-related viruses in various mammals, including febrile humans, opens the possibility that Jingmenviruses may be novel tick-borne arboviruses. In this study, we aimed at increasing knowledge of the host range, genetic diversity, and geographical distribution of Jingmenviruses by reporting for the first time the identification of Jingmenviruses associated with Rhipicephalus microplus ticks originating in the French Antilles (Guadeloupe and Martinique islands), with Amblyomma testudinarium ticks in Lao PDR, and with Ixodes ricinus ticks in metropolitan France, and from urine of Pteropus lylei bats in Cambodia. Analyses of the relationships between the different Jingmenvirus genomes resulted in the identification of three main phylogenic subclades, each of them containing both tick-borne and mammal-borne strains, reinforcing the idea that Jingmenviruses may be considered as tick-borne arboviruses. Finally, we estimated the prevalence of Jingmenvirus-like infection using luciferase immunoprecipitation assay screening (LIPS) of asymptomatic humans and cattle highly exposed to tick bites. Among 70 French human, 153 Laotian human, and 200 Caribbean cattle sera tested, only one French human serum was found (slightly) positive, suggesting that the prevalence of Jingmenvirus human and cattle infections in these areas is probably low. IMPORTANCE Several arboviruses emerging as new pathogens for humans and domestic animals have recently raised public health concern and increased interest in the study of their host range and in detection of spillover events. Recently, a new group of segmented Flaviviridae-related viruses, the Jingmenviruses, has been identified worldwide in many invertebrate and vertebrate hosts, pointing out the issue of whether they belong to the arbovirus group. The study presented here combined whole-genome sequencing of three tick-borne Jingmenviruses and one bat-borne Jingmenvirus with comprehensive phylogenetic analyses and high-throughput serological screening of human and cattle populations exposed to these viruses to contribute to the knowledge of Jingmenvirus host range, geographical distribution, and mammalian exposure.
format article
author Sarah Temmam
Thomas Bigot
Delphine Chrétien
Mathilde Gondard
Philippe Pérot
Virginie Pommelet
Evelyne Dufour
Stéphane Petres
Elodie Devillers
Thavry Hoem
Valérie Pinarello
Vibol Hul
Khamsing Vongphayloth
Jeffrey C. Hertz
Irène Loiseau
Marine Dumarest
Veasna Duong
Muriel Vayssier-Taussat
Marc Grandadam
Emmanuel Albina
Philippe Dussart
Sara Moutailler
Julien Cappelle
Paul T. Brey
Marc Eloit
author_facet Sarah Temmam
Thomas Bigot
Delphine Chrétien
Mathilde Gondard
Philippe Pérot
Virginie Pommelet
Evelyne Dufour
Stéphane Petres
Elodie Devillers
Thavry Hoem
Valérie Pinarello
Vibol Hul
Khamsing Vongphayloth
Jeffrey C. Hertz
Irène Loiseau
Marine Dumarest
Veasna Duong
Muriel Vayssier-Taussat
Marc Grandadam
Emmanuel Albina
Philippe Dussart
Sara Moutailler
Julien Cappelle
Paul T. Brey
Marc Eloit
author_sort Sarah Temmam
title Insights into the Host Range, Genetic Diversity, and Geographical Distribution of Jingmenviruses
title_short Insights into the Host Range, Genetic Diversity, and Geographical Distribution of Jingmenviruses
title_full Insights into the Host Range, Genetic Diversity, and Geographical Distribution of Jingmenviruses
title_fullStr Insights into the Host Range, Genetic Diversity, and Geographical Distribution of Jingmenviruses
title_full_unstemmed Insights into the Host Range, Genetic Diversity, and Geographical Distribution of Jingmenviruses
title_sort insights into the host range, genetic diversity, and geographical distribution of jingmenviruses
publisher American Society for Microbiology
publishDate 2019
url https://doaj.org/article/b8cd568f403f4fa0add30b68ad69818e
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