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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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2019-12-01
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| Series: | mSphere |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mSphere.00645-19 |
| _version_ | 1818398486567059456 |
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| 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 |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-14T07:05:33Z |
| format | Article |
| id | doaj.art-b8cd568f403f4fa0add30b68ad69818e |
| institution | Directory Open Access Journal |
| issn | 2379-5042 |
| language | English |
| last_indexed | 2024-12-14T07:05:33Z |
| publishDate | 2019-12-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSphere |
| spelling | doaj.art-b8cd568f403f4fa0add30b68ad69818e2022-12-21T23:12:13ZengAmerican Society for MicrobiologymSphere2379-50422019-12-014610.1128/mSphere.00645-19Insights into the Host Range, Genetic Diversity, and Geographical Distribution of JingmenvirusesSarah Temmam0Thomas Bigot1Delphine Chrétien2Mathilde Gondard3Philippe Pérot4Virginie Pommelet5Evelyne Dufour6Stéphane Petres7Elodie Devillers8Thavry Hoem9Valérie Pinarello10Vibol Hul11Khamsing Vongphayloth12Jeffrey C. Hertz13Irène Loiseau14Marine Dumarest15Veasna Duong16Muriel Vayssier-Taussat17Marc Grandadam18Emmanuel Albina19Philippe Dussart20Sara Moutailler21Julien Cappelle22Paul T. Brey23Marc Eloit24Institut Pasteur, Biology of Infection Unit, Inserm U1117, Pathogen Discovery Laboratory, Institut Pasteur, Paris, FranceInstitut Pasteur, Biology of Infection Unit, Inserm U1117, Pathogen Discovery Laboratory, Institut Pasteur, Paris, FranceInstitut Pasteur, Biology of Infection Unit, Inserm U1117, Pathogen Discovery Laboratory, Institut Pasteur, Paris, FranceUMR ASTRE, CIRAD, INRA, Université de Montpellier, Montpellier, FranceInstitut Pasteur, Biology of Infection Unit, Inserm U1117, Pathogen Discovery Laboratory, Institut Pasteur, Paris, FranceInstitut Pasteur du Laos, Vientiane, Lao People's Democratic RepublicInstitut Pasteur, Production and Purification of Recombinant Proteins Technological Platform—C2RT, Institut Pasteur, Paris, FranceInstitut Pasteur, Production and Purification of Recombinant Proteins Technological Platform—C2RT, Institut Pasteur, Paris, FranceUMR BIPAR, Animal Health Laboratory, ANSES, INRA, Ecole Nationale Vétérinaire d’Alfort, Université Paris-Est, Maisons-Alfort, FranceVirology Unit, Institut Pasteur du Cambodge, Institut Pasteur International Network, Phnom Penh, CambodiaUMR ASTRE, CIRAD, INRA, Université de Montpellier, Montpellier, FranceVirology Unit, Institut Pasteur du Cambodge, Institut Pasteur International Network, Phnom Penh, CambodiaInstitut Pasteur du Laos, Vientiane, Lao People's Democratic RepublicU.S. NAMRU 2, NMRCA, SingaporeInstitut Pasteur, Biology of Infection Unit, Inserm U1117, Pathogen Discovery Laboratory, Institut Pasteur, Paris, FranceInstitut Pasteur, Biology of Infection Unit, Inserm U1117, Pathogen Discovery Laboratory, Institut Pasteur, Paris, FranceVirology Unit, Institut Pasteur du Cambodge, Institut Pasteur International Network, Phnom Penh, CambodiaUMR BIPAR, Animal Health Laboratory, ANSES, INRA, Ecole Nationale Vétérinaire d’Alfort, Université Paris-Est, Maisons-Alfort, FranceInstitut Pasteur du Laos, Vientiane, Lao People's Democratic RepublicUMR ASTRE, CIRAD, INRA, Université de Montpellier, Montpellier, FranceVirology Unit, Institut Pasteur du Cambodge, Institut Pasteur International Network, Phnom Penh, CambodiaUMR BIPAR, Animal Health Laboratory, ANSES, INRA, Ecole Nationale Vétérinaire d’Alfort, Université Paris-Est, Maisons-Alfort, FranceUMR ASTRE, CIRAD, INRA, Université de Montpellier, Montpellier, FranceInstitut Pasteur du Laos, Vientiane, Lao People's Democratic RepublicInstitut Pasteur, Biology of Infection Unit, Inserm U1117, Pathogen Discovery Laboratory, Institut Pasteur, Paris, FranceABSTRACT 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.https://journals.asm.org/doi/10.1128/mSphere.00645-19JingmenvirusLIPSemergenceevolution |
| spellingShingle | 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 mSphere Jingmenvirus LIPS emergence evolution |
| title | 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_short | 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 |
| topic | Jingmenvirus LIPS emergence evolution |
| url | https://journals.asm.org/doi/10.1128/mSphere.00645-19 |
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