Culicoides-Borne Viruses 2023

A special issue of Viruses (ISSN 1999-4915). This special issue belongs to the section "Insect Viruses".

Deadline for manuscript submissions: closed (20 March 2024) | Viewed by 9053

Special Issue Editors


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Guest Editor
National Research Institute for Agriculture, Food and the Environment, Department of Animal Health, UMR1161 Virologie, INRAE-Anses-ENVA, 94700 Maisons-Alort, France
Interests: arboviruses; arthropod vectors; mammalian hosts; innate immunity; orbiviruses; vaccines; virus genetics and reverse genetic; structural biology; genomics; bluetongue virus; virus taxonomy
Special Issues, Collections and Topics in MDPI journals

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Guest Editor
Inrae Anses Maisons Alfort, Maisons-Alfort, France
Interests: mammalian arboviruses; arthropod vectors; innate immunity; orbiviruses; virus genetics and reverse genetic; genomics; plant arboviruses; bioinformatics; population genetics; multiomics

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Guest Editor
ANSES Maisons-Alfort Laboratory for Animal Health., Maisons-Alfort, France
Interests: arboviruses; arthropod vectors; innate immunity; orbiviruses; vaccines; virus genetics and reverse genetic; structural biology; genomics; proteomics, dsRNA viruses; virus taxonomy

Special Issue Information

Dear Colleagues,

Culicoides-borne viruses are RNA arboviruses which belong to diverse orders including Reovirales (Orbivirus), Bunyavirales (Orthobunyavirus, Nairovirus), and Mononegavirales (Ephemerovirus and Vesiculovirus). Many of these viruses are responsible for severe disease in animals and important economic losses in affected areas.

The spread and introduction of many of these viruses into novel geographical regions has enabled research opportunities to assess their evolutionary history, disease phenotypes, immune responses, diagnostics, cell biology, structural biology, interaction with both hosts and vectors, and the development of novel vaccine and antiviral strategies. Of particular interest, the discovery of novel orbiviruses which fail to replicate in Culicoides vectors and which are efficiently transmitted by direct contact from infected to non-infected contact animals has provided the opportunity to study virus genes/proteins that influence vector infection. The ‘frozen evolution’ of the re-emerged bluetongue virus type 8 in France appears to have been caused by an accidental re-introduction, which raises questions about the safety testing of specific frozen stored biological samples.

This Special Issue on Culicoides-borne viruses is open to original research and/or reviews which focus on various aspects of virus–host–vector interactions, genomics, proteomics, phylogenetic analyses/evolutionary history, vaccinology/immune responses, diagnostics, cell biology, and translational science.

Dr. Houssam Attoui
Dr. Baptiste Monsion
Dr. Fauziah Mohd Jaafar
Guest Editors

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Keywords

  • culicoides-borne viruses
  • orbivirus
  • nairovirus
  • ephemerovirus
  • vesiculovirus
  • orthobunyavirus

Published Papers (8 papers)

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Research

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11 pages, 308 KiB  
Article
The Study of Bluetongue Virus (BTV) and Epizootic Hemorrhagic Disease Virus (EHDV) Circulation and Vectors at the Municipal Parks and Zoobotanical Foundation of Belo Horizonte, Minas Gerais, Brazil (FPMZB-BH)
by Eduardo Alves Caixeta, Mariana Andrioli Pinheiro, Victoria Souza Lucchesi, Anna Gabriella Guimarães Oliveira, Grazielle Cossenzo Florentino Galinari, Herlandes Penha Tinoco, Carlyle Mendes Coelho and Zélia Inês Portela Lobato
Viruses 2024, 16(2), 293; https://0-doi-org.brum.beds.ac.uk/10.3390/v16020293 - 15 Feb 2024
Viewed by 728
Abstract
Bluetongue Virus (BTV) and Epizootic Hemorrhagic Disease Virus (EHDV) are Orbiviruses primarily transmitted by their biological vector, Culicoides spp. Latreille, 1809 (Diptera: Ceratopogonidae). These viruses can infect a diverse range of vertebrate hosts, leading to disease outbreaks in domestic and wild ruminants worldwide. [...] Read more.
Bluetongue Virus (BTV) and Epizootic Hemorrhagic Disease Virus (EHDV) are Orbiviruses primarily transmitted by their biological vector, Culicoides spp. Latreille, 1809 (Diptera: Ceratopogonidae). These viruses can infect a diverse range of vertebrate hosts, leading to disease outbreaks in domestic and wild ruminants worldwide. This study, conducted at the Belo Horizonte Municipal Parks and Zoobotany Foundation (FPMZB-BH), Minas Gerais, Brazil, focused on Orbivirus and its vectors. Collections of Culicoides spp. were carried out at the FPMZB-BH from 9 December 2021 to 18 November 2022. A higher prevalence of these insects was observed during the summer months, especially in February. Factors such as elevated temperatures, high humidity, fecal accumulation, and proximity to large animals, like camels and elephants, were associated with increased Culicoides capture. Among the identified Culicoides spp. species, Culicoides insignis Lutz, 1913, constituted 75%, and Culicoides pusillus Lutz, 1913, 6% of the collected midges, both described as competent vectors for Orbivirus transmission. Additionally, a previously unreported species in Minas Gerais, Culicoides debilipalpis Lutz, 1913, was identified, also suspected of being a transmitter of these Orbiviruses. The feeding preferences of some Culicoides species were analyzed, revealing that C. insignis feeds on deer, Red deer (Cervus elaphus) and European fallow deer (Dama dama). Different Culicoides spp. were also identified feeding on humans, raising concerns about the potential transmission of arboviruses at the site. In parallel, 72 serum samples from 14 susceptible species, including various Cervids, collected between 2012 and 2022 from the FPMZB-BH serum bank, underwent Agar Gel Immunodiffusion (AGID) testing for BTV and EHDV. The results showed 75% seropositivity for BTV and 19% for EHDV. Post-testing analysis revealed variations in antibody presence against BTV in a tapir and a fallow deer and against EHDV in a gemsbok across different years. These studies confirm the presence of BTV and EHDV vectors, along with potential virus circulation in the zoo. Consequently, implementing control measures is essential to prevent susceptible species from becoming infected and developing clinical diseases. Full article
(This article belongs to the Special Issue Culicoides-Borne Viruses 2023)
18 pages, 2924 KiB  
Article
Assessing Reassortment between Bluetongue Virus Serotypes 10 and 17 at Different Coinfection Ratios in Culicoides sonorenesis
by Molly Carpenter, Jennifer Kopanke, Justin Lee, Case Rodgers, Kirsten Reed, Tyler J. Sherman, Barbara Graham, Mark Stenglein and Christie Mayo
Viruses 2024, 16(2), 240; https://0-doi-org.brum.beds.ac.uk/10.3390/v16020240 - 02 Feb 2024
Viewed by 690
Abstract
Bluetongue virus (BTV) is a segmented, double-stranded RNA orbivirus listed by the World Organization for Animal Health and transmitted by Culicoides biting midges. Segmented viruses can reassort, which facilitates rapid and important genotypic changes. Our study evaluated reassortment in Culicoides sonorensis midges coinfected [...] Read more.
Bluetongue virus (BTV) is a segmented, double-stranded RNA orbivirus listed by the World Organization for Animal Health and transmitted by Culicoides biting midges. Segmented viruses can reassort, which facilitates rapid and important genotypic changes. Our study evaluated reassortment in Culicoides sonorensis midges coinfected with different ratios of BTV-10 and BTV-17. Midges were fed blood containing BTV-10, BTV-17, or a combination of both serotypes at 90:10, 75:25, 50:50, 25:75, or 10:90 ratios. Midges were collected every other day and tested for infection using pan BTV and cox1 (housekeeping gene) qRT-PCR. A curve was fit to the ∆Ct values (pan BTV Ct—cox1 Ct) for each experimental group. On day 10, the midges were processed for BTV plaque isolation. Genotypes of the plaques were determined by next-generation sequencing. Pairwise comparison of ∆Ct curves demonstrated no differences in viral RNA levels between coinfected treatment groups. Plaque genotyping indicated that most plaques fully aligned with one of the parental strains; however, reassortants were detected, and in the 75:25 pool, most plaques were reassortant. Reassortant prevalence may be maximized upon the occurrence of reassortant genotypes that can outcompete the parental genotypes. BTV reassortment and resulting biological consequences are important elements to understanding orbivirus emergence and evolution. Full article
(This article belongs to the Special Issue Culicoides-Borne Viruses 2023)
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14 pages, 1821 KiB  
Article
Detection, Characterization and Sequencing of BTV Serotypes Circulating in Cuba in 2022
by Ana María Acevedo, Lydie Postic, Maray Curiel, Mathilde Gondard, Emmanuel Bréard, Stéphan Zientara, Fabien Vorimore, Mai-Lan Tran, Mathilde Turpaud, Giovanni Savini, Alessio Lorusso, Maurilia Marcacci, Damien Vitour, Pascal Dujardin, Carmen Laura Perera, Cristian Díaz, Yalainne Obret and Corinne Sailleau
Viruses 2024, 16(1), 164; https://0-doi-org.brum.beds.ac.uk/10.3390/v16010164 - 22 Jan 2024
Viewed by 769
Abstract
In Cuba, despite a high sero-prevalence of bluetongue virus (BTV), circulating serotypes remain unknown. The aim of this study was to identify circulating BTV serotypes in farms throughout the western region of Cuba. Blood samples were collected from 200 young cattle and sheep [...] Read more.
In Cuba, despite a high sero-prevalence of bluetongue virus (BTV), circulating serotypes remain unknown. The aim of this study was to identify circulating BTV serotypes in farms throughout the western region of Cuba. Blood samples were collected from 200 young cattle and sheep between May and July 2022 for virological analyses (PCR, viral isolation and virus neutralization) and genome sequencing. The results confirmed viral circulation, with viro-prevalence of 25% for BTV. The virus was isolated from 18 blood samples and twelve BTV serotypes were identified by sequencing RT-PCR products targeting the segment 2 of the BTV genome (BTV-1, 2, 3, 6, 10, 12, 13, 17, 18, 19, 22 and 24). Finally, the full genome sequences of 17 Cuban BTV isolates were recovered using a Sequence Independent Single Primer Amplification (SISPA) approach combined to MinION Oxford Nanopore sequencing technology. All together, these results highlight the co-circulation of a wide diversity of BTV serotypes in a quite restricted area and emphasize the need for entomological and livestock surveillance, particularly in light of recent changes in the global distribution and nature of BTV infections. Full article
(This article belongs to the Special Issue Culicoides-Borne Viruses 2023)
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13 pages, 1940 KiB  
Article
Vesicular Stomatitis Virus Elicits Early Transcriptome Response in Culicoides sonorensis Cells
by Stacey L. P. Scroggs, Edward J. Bird, David C. Molik and Dana Nayduch
Viruses 2023, 15(10), 2108; https://0-doi-org.brum.beds.ac.uk/10.3390/v15102108 - 18 Oct 2023
Viewed by 927
Abstract
Viruses that are transmitted by arthropods, or arboviruses, have evolved to successfully navigate both the invertebrate and vertebrate hosts, including their immune systems. Biting midges transmit several arboviruses including vesicular stomatitis virus (VSV). To study the interaction between VSV and midges, we characterized [...] Read more.
Viruses that are transmitted by arthropods, or arboviruses, have evolved to successfully navigate both the invertebrate and vertebrate hosts, including their immune systems. Biting midges transmit several arboviruses including vesicular stomatitis virus (VSV). To study the interaction between VSV and midges, we characterized the transcriptomic responses of VSV-infected and mock-infected Culicoides sonorensis cells at 1, 8, 24, and 96 h post inoculation (HPI). The transcriptomic response of VSV-infected cells at 1 HPI was significant, but by 8 HPI there were no detectable differences between the transcriptome profiles of VSV-infected and mock-infected cells. Several genes involved in immunity were upregulated (ATG2B and TRAF4) or downregulated (SMAD6 and TOLL7) in VSV-treated cells at 1 HPI. These results indicate that VSV infection in midge cells produces an early immune response that quickly wanes, giving insight into in vivo C. sonorensis VSV tolerance that may underlie their permissiveness as vectors for this virus. Full article
(This article belongs to the Special Issue Culicoides-Borne Viruses 2023)
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27 pages, 7616 KiB  
Article
Orbivirus NS4 Proteins Play Multiple Roles to Dampen Cellular Responses
by Fauziah Mohd Jaafar, Mourad Belhouchet, Baptiste Monsion, Lesley Bell-Sakyi, Peter P. C. Mertens and Houssam Attoui
Viruses 2023, 15(9), 1908; https://0-doi-org.brum.beds.ac.uk/10.3390/v15091908 - 12 Sep 2023
Viewed by 1172
Abstract
Non-structural protein 4 (NS4) of insect-borne and tick-borne orbiviruses is encoded by genome segment 9, from a secondary open reading frame. Though a protein dispensable for bluetongue virus (BTV) replication, it has been shown to counter the interferon response in cells infected with [...] Read more.
Non-structural protein 4 (NS4) of insect-borne and tick-borne orbiviruses is encoded by genome segment 9, from a secondary open reading frame. Though a protein dispensable for bluetongue virus (BTV) replication, it has been shown to counter the interferon response in cells infected with BTV or African horse sickness virus. We further explored the functional role(s) of NS4 proteins of BTV and the tick-borne Great Island virus (GIV). We show that NS4 of BTV or GIV helps an E3L deletion mutant of vaccinia virus to replicate efficiently in interferon-treated cells, further confirming the role of NS4 as an interferon antagonist. Our results indicate that ectopically expressed NS4 of BTV localised with caspase 3 within the nucleus and was found in a protein complex with active caspase 3 in a pull-down assay. Previous studies have shown that pro-apoptotic caspases (including caspase 3) suppress type I interferon response by cleaving mediators involved in interferon signalling. Our data suggest that orbivirus NS4 plays a role in modulating the apoptotic process and/or regulating the interferon response in mammalian cells, thus acting as a virulence factor in pathogenesis. Full article
(This article belongs to the Special Issue Culicoides-Borne Viruses 2023)
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12 pages, 1976 KiB  
Article
Metavirome Analysis and Identification of Midge-Borne Viruses from Yunnan Province, China, in 2021
by Chenghui Li, Wei Wang, Xuancheng Zhang, Pengpeng Xiao, Zhuoxin Li, Peng Wang, Ning Shi, Hongning Zhou, Huijun Lu, Xu Gao, He Zhang and Ningyi Jin
Viruses 2023, 15(9), 1817; https://0-doi-org.brum.beds.ac.uk/10.3390/v15091817 - 26 Aug 2023
Viewed by 1100
Abstract
Midges are widely distributed globally and can transmit various human and animal diseases through blood-sucking. As part of this study, 259,300 midges were collected from four districts in Yunnan province, China, to detect the viral richness and diversity using metavirome analysis techniques. As [...] Read more.
Midges are widely distributed globally and can transmit various human and animal diseases through blood-sucking. As part of this study, 259,300 midges were collected from four districts in Yunnan province, China, to detect the viral richness and diversity using metavirome analysis techniques. As many as 26 virus families were detected, and the partial sequences of bluetongue virus (BTV), dengue virus (DENV), and Getah virus (GETV) were identified by phylogenetic analysis and PCR amplification. Two BTV gene fragments, 866 bps for the VP2 gene of BTV type 16 and 655 bps for the VP5 gene of BTV type 21, were amplified. The nucleotide sequence identities of the two amplified BTV fragments were 94.46% and 98.81%, respectively, with two classical BTV-16 (GenBank: JN671907) and BTV-21 strains (GenBank: MK250961) isolated in Yunnan province. Furthermore, the BTV-16 DH2021 strain was successfully isolated in C6/36 cells, and the peak value of the copy number reached 3.13 × 107 copies/μL after five consecutive BHK-21 cell passages. Moreover, two 2054 bps fragments including the E gene of DENV genotype Asia II were amplified and shared the highest identity with the DENV strain isolated in New Guinea in 1944. A length of 656 bps GETV gene sequence encoded the partial capsid protein, and it shared the highest identity of 99.68% with the GETV isolated from Shandong province, China, in 2017. Overall, this study emphasizes the importance of implementing prevention and control strategies for viral diseases transmitted by midges in China. Full article
(This article belongs to the Special Issue Culicoides-Borne Viruses 2023)
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10 pages, 722 KiB  
Article
Characterization of Epizootic Hemorrhagic Disease Virus Serotype 8 in Naturally Infected Barbary Deer (Cervus elaphus barbarus) and Culicoides (Diptera: Ceratopogonidae) in Tunisia
by Sarah Thabet, Soufien Sghaier, Thameur Ben Hassine, Darine Slama, Raja Ben Osmane, Ridha Ben Omrane, Wiem Mouelhi, Massimo Spedicato, Alessandra Leone, Liana Teodori, Valentina Curini, Moncef Othmani, Shadia Berjaoui, Paola Ripà, Makram Orabi, Bassem Belhaj Mohamed, Ayda Sayadi, Sonia Ben Slama, Maurilia Marcacci, Giovanni Savini, Alessio Lorusso and Salah Hammamiadd Show full author list remove Hide full author list
Viruses 2023, 15(7), 1567; https://0-doi-org.brum.beds.ac.uk/10.3390/v15071567 - 18 Jul 2023
Cited by 3 | Viewed by 1657
Abstract
Epizootic hemorrhagic disease (EHD) is a Culicoides-borne disease of domestic and wild ruminants caused by EHD virus (EHDV). This virus circulates in multiple serotypes. In late September 2021, a novel strain belonging to EHDV-8 was reported in cattle farms in Central–Western Tunisia, [...] Read more.
Epizootic hemorrhagic disease (EHD) is a Culicoides-borne disease of domestic and wild ruminants caused by EHD virus (EHDV). This virus circulates in multiple serotypes. In late September 2021, a novel strain belonging to EHDV-8 was reported in cattle farms in Central–Western Tunisia, and in the fall of 2022, the same virus was also detected in Italy and Spain. In the present study, we described EHDV-8 occurrence in deer and, a preliminary identification of the potential Culicoides species responsible for virus transmission in selected areas of Tunisia. EHDV-8 was identified in deer carcasses found in 2021 and 2022 in the national reserve of El Feidja, Jendouba, Northwestern Tunisia, and isolated on cell culture. Instead, insect vectors were collected in October 2021 only in the areas surrounding the city of Tozeur (Southern Tunisia) where EHDV-8 cases in cattle were confirmed. Morphological identification showed that 95% of them belonged to the Culicoides kingi and Culicoides oxystoma species and both species tested positive for EHDV-8 RNA. C. imicola was not detected in this collection and EHDV-8 RNA was not evidenced in vector pools collected in 2020, prior to official EHDV-8 emergence. EHDV whole genome sequences were also obtained directly from infected biological samples of deer and positive vectors. EHDV-8 sequences obtained from deer and vectors share a nucleotide identity ranging from 99.42 to 100% and amino acid identity from 99.18 to 100% across all genome segments with the EHDV-8/17 TUN2021 reference sequence. Full article
(This article belongs to the Special Issue Culicoides-Borne Viruses 2023)
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Review

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28 pages, 2775 KiB  
Review
Revisiting the Importance of Orthobunyaviruses for Animal Health: A Scoping Review of Livestock Disease, Diagnostic Tests, and Surveillance Strategies for the Simbu Serogroup
by Tiffany W. O’Connor, Paul M. Hick, Deborah S. Finlaison, Peter D. Kirkland and Jenny-Ann L.M.L. Toribio
Viruses 2024, 16(2), 294; https://0-doi-org.brum.beds.ac.uk/10.3390/v16020294 - 15 Feb 2024
Viewed by 1193
Abstract
Orthobunyaviruses (order Bunyavirales, family Peribunyaviridae) in the Simbu serogroup have been responsible for widespread epidemics of congenital disease in ruminants. Australia has a national program to monitor arboviruses of veterinary importance. While monitoring for Akabane virus, a novel orthobunyavirus was detected. [...] Read more.
Orthobunyaviruses (order Bunyavirales, family Peribunyaviridae) in the Simbu serogroup have been responsible for widespread epidemics of congenital disease in ruminants. Australia has a national program to monitor arboviruses of veterinary importance. While monitoring for Akabane virus, a novel orthobunyavirus was detected. To inform the priority that should be given to this detection, a scoping review was undertaken to (1) characterise the associated disease presentations and establish which of the Simbu group viruses are of veterinary importance; (2) examine the diagnostic assays that have undergone development and validation for this group of viruses; and (3) describe the methods used to monitor the distribution of these viruses. Two search strategies identified 224 peer-reviewed publications for 33 viruses in the serogroup. Viruses in this group may cause severe animal health impacts, but only those phylogenetically arranged in clade B are associated with animal disease. Six viruses (Akabane, Schmallenberg, Aino, Shuni, Peaton, and Shamonda) were associated with congenital malformations, neurological signs, and reproductive disease. Diagnostic test interpretation is complicated by cross-reactivity, the timing of foetal immunocompetence, and sample type. Serological testing in surveys remains a mainstay of the methods used to monitor the distribution of SGVs. Given significant differences in survey designs, only broad mean seroprevalence estimates could be provided. Further research is required to determine the disease risk posed by novel orthobunyaviruses and how they could challenge current diagnostic and surveillance capabilities. Full article
(This article belongs to the Special Issue Culicoides-Borne Viruses 2023)
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