Competition between Usutu virus and West Nile virus during simultaneous and sequential infection of Culex pipiens mosquitoes

Usutu virus (USUV) and West Nile virus (WNV) are closely related mosquito-borne flaviviruses that are mainly transmitted between bird hosts by vector mosquitoes. Infections in humans are incidental but can cause severe disease. USUV is endemic in large parts of Europe, while WNV mainly circulates in...

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Main Authors: Haidong Wang, Sandra R. Abbo, Tessa M. Visser, Marcel Westenberg, Corinne Geertsema, Jelke J. Fros, Constantianus J. M. Koenraadt, Gorben P. Pijlman
Format: Article
Language:English
Published: Taylor & Francis Group 2020-01-01
Series:Emerging Microbes and Infections
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Online Access:https://www.tandfonline.com/doi/10.1080/22221751.2020.1854623
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author Haidong Wang
Sandra R. Abbo
Tessa M. Visser
Marcel Westenberg
Corinne Geertsema
Jelke J. Fros
Constantianus J. M. Koenraadt
Gorben P. Pijlman
author_facet Haidong Wang
Sandra R. Abbo
Tessa M. Visser
Marcel Westenberg
Corinne Geertsema
Jelke J. Fros
Constantianus J. M. Koenraadt
Gorben P. Pijlman
author_sort Haidong Wang
collection DOAJ
description Usutu virus (USUV) and West Nile virus (WNV) are closely related mosquito-borne flaviviruses that are mainly transmitted between bird hosts by vector mosquitoes. Infections in humans are incidental but can cause severe disease. USUV is endemic in large parts of Europe, while WNV mainly circulates in Southern Europe. In recent years, WNV is also frequently detected in Northern Europe, thereby expanding the area where both viruses co-circulate. However, it remains unclear how USUV may affect the future spread of WNV and the likelihood of human co-infection. Here we investigated whether co-infections with both viruses in cell lines and their primary mosquito vector, Culex pipiens, affect virus replication and transmission dynamics. We show that USUV is outcompeted by WNV in mammalian, avian and mosquito cells during co-infection. Mosquitoes that were exposed to both viruses simultaneously via infectious blood meal displayed significantly reduced USUV transmission compared to mosquitoes that were only exposed to USUV (from 15% to 3%), while the infection and transmission of WNV was unaffected. In contrast, when mosquitoes were pre-infected with USUV via infectious blood meal, WNV transmission was significantly reduced (from 44% to 17%). Injection experiments established the involvement of the midgut in the observed USUV-mediated WNV inhibition. The competition between USUV and WNV during co-infection clearly indicates that the chance of concurrent USUV and WNV transmission via a single mosquito bite is low. The competitive relation between USUV and WNV may impact virus transmission dynamics in the field and affect the epidemiology of WNV in Europe.
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spelling doaj-art-1ee91336e8564f3ab82affe351d9546d2025-08-20T02:12:20ZengTaylor & Francis GroupEmerging Microbes and Infections2222-17512020-01-01912642265210.1080/22221751.2020.1854623Competition between Usutu virus and West Nile virus during simultaneous and sequential infection of Culex pipiens mosquitoesHaidong Wang0Sandra R. Abbo1Tessa M. Visser2Marcel Westenberg3Corinne Geertsema4Jelke J. Fros5Constantianus J. M. Koenraadt6Gorben P. Pijlman7Laboratory of Virology, Wageningen University & Research, Wageningen, NetherlandsLaboratory of Virology, Wageningen University & Research, Wageningen, NetherlandsLaboratory of Entomology, Wageningen University & Research, Wageningen, NetherlandsDutch National Plant Protection Organization (NPPO-NL), Wageningen, NetherlandsLaboratory of Virology, Wageningen University & Research, Wageningen, NetherlandsLaboratory of Virology, Wageningen University & Research, Wageningen, NetherlandsLaboratory of Entomology, Wageningen University & Research, Wageningen, NetherlandsLaboratory of Virology, Wageningen University & Research, Wageningen, NetherlandsUsutu virus (USUV) and West Nile virus (WNV) are closely related mosquito-borne flaviviruses that are mainly transmitted between bird hosts by vector mosquitoes. Infections in humans are incidental but can cause severe disease. USUV is endemic in large parts of Europe, while WNV mainly circulates in Southern Europe. In recent years, WNV is also frequently detected in Northern Europe, thereby expanding the area where both viruses co-circulate. However, it remains unclear how USUV may affect the future spread of WNV and the likelihood of human co-infection. Here we investigated whether co-infections with both viruses in cell lines and their primary mosquito vector, Culex pipiens, affect virus replication and transmission dynamics. We show that USUV is outcompeted by WNV in mammalian, avian and mosquito cells during co-infection. Mosquitoes that were exposed to both viruses simultaneously via infectious blood meal displayed significantly reduced USUV transmission compared to mosquitoes that were only exposed to USUV (from 15% to 3%), while the infection and transmission of WNV was unaffected. In contrast, when mosquitoes were pre-infected with USUV via infectious blood meal, WNV transmission was significantly reduced (from 44% to 17%). Injection experiments established the involvement of the midgut in the observed USUV-mediated WNV inhibition. The competition between USUV and WNV during co-infection clearly indicates that the chance of concurrent USUV and WNV transmission via a single mosquito bite is low. The competitive relation between USUV and WNV may impact virus transmission dynamics in the field and affect the epidemiology of WNV in Europe.https://www.tandfonline.com/doi/10.1080/22221751.2020.1854623Usutu virusWest Nile viruscompetitionmosquitovector competence
spellingShingle Haidong Wang
Sandra R. Abbo
Tessa M. Visser
Marcel Westenberg
Corinne Geertsema
Jelke J. Fros
Constantianus J. M. Koenraadt
Gorben P. Pijlman
Competition between Usutu virus and West Nile virus during simultaneous and sequential infection of Culex pipiens mosquitoes
Emerging Microbes and Infections
Usutu virus
West Nile virus
competition
mosquito
vector competence
title Competition between Usutu virus and West Nile virus during simultaneous and sequential infection of Culex pipiens mosquitoes
title_full Competition between Usutu virus and West Nile virus during simultaneous and sequential infection of Culex pipiens mosquitoes
title_fullStr Competition between Usutu virus and West Nile virus during simultaneous and sequential infection of Culex pipiens mosquitoes
title_full_unstemmed Competition between Usutu virus and West Nile virus during simultaneous and sequential infection of Culex pipiens mosquitoes
title_short Competition between Usutu virus and West Nile virus during simultaneous and sequential infection of Culex pipiens mosquitoes
title_sort competition between usutu virus and west nile virus during simultaneous and sequential infection of culex pipiens mosquitoes
topic Usutu virus
West Nile virus
competition
mosquito
vector competence
url https://www.tandfonline.com/doi/10.1080/22221751.2020.1854623
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