Temperate conditions restrict Japanese encephalitis virus infection to the mid-gut and prevents systemic dissemination in Culex pipiens mosquitoes

Abstract Japanese encephalitis virus (JEV), a mosquito-borne flavivirus, is the main cause of viral encephalitis in Asia. However, with changing climate JEV has the potential to emerge in novel temperate regions. Here, we have assessed the vector competence of the temperate mosquito Culex pipiens f....

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Main Authors: Arran J. Folly, Daniel Dorey-Robinson, Luis M. Hernández-Triana, Stuart Ackroyd, Beatriz Vidana, Fabian Z. X. Lean, Daniel Hicks, Alejandro Nuñez, Nicholas Johnson
Format: Article
Language:English
Published: Nature Portfolio 2021-03-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-021-85411-2
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author Arran J. Folly
Daniel Dorey-Robinson
Luis M. Hernández-Triana
Stuart Ackroyd
Beatriz Vidana
Fabian Z. X. Lean
Daniel Hicks
Alejandro Nuñez
Nicholas Johnson
author_facet Arran J. Folly
Daniel Dorey-Robinson
Luis M. Hernández-Triana
Stuart Ackroyd
Beatriz Vidana
Fabian Z. X. Lean
Daniel Hicks
Alejandro Nuñez
Nicholas Johnson
author_sort Arran J. Folly
collection DOAJ
description Abstract Japanese encephalitis virus (JEV), a mosquito-borne flavivirus, is the main cause of viral encephalitis in Asia. However, with changing climate JEV has the potential to emerge in novel temperate regions. Here, we have assessed the vector competence of the temperate mosquito Culex pipiens f. pipiens to vector JEV genotype III at temperatures representative of those experienced, or predicted in the future during the summer months, in the United Kingdom. Our results show that Cx. pipiens is susceptible to JEV infection at both temperatures. In addition, at 25 °C, JEV disseminated from the midgut and was recovered in saliva samples, indicating the potential for transmission. At a lower temperature, 20 °C, following an incubation period of fourteen days, there were reduced levels of JEV dissemination and virus was not detected in saliva samples. The virus present in the bodies of these mosquitoes was restricted to the posterior midgut as determined by microscopy and viable virus was successfully recovered. Apart from the influence on virus dissemination, mosquito mortality was significantly increased at the higher temperature. Overall, our results suggest that temperature is a critical factor for JEV vector competence and infected-mosquito survival. This may in turn influence the vectorial capacity of Cx. pipiens to vector JEV genotype III in temperate areas.
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spelling doaj.art-69c0bfeeb62649338633c44a4afadc512022-12-21T22:55:38ZengNature PortfolioScientific Reports2045-23222021-03-0111111010.1038/s41598-021-85411-2Temperate conditions restrict Japanese encephalitis virus infection to the mid-gut and prevents systemic dissemination in Culex pipiens mosquitoesArran J. Folly0Daniel Dorey-Robinson1Luis M. Hernández-Triana2Stuart Ackroyd3Beatriz Vidana4Fabian Z. X. Lean5Daniel Hicks6Alejandro Nuñez7Nicholas Johnson8Arbovirus Research Team, Virology Department, Animal and Plant Health AgencyArbovirus Research Team, Virology Department, Animal and Plant Health AgencyArbovirus Research Team, Virology Department, Animal and Plant Health AgencyPathology Department, Animal and Plant Health AgencyPathology Department, Animal and Plant Health AgencyPathology Department, Animal and Plant Health AgencyPathology Department, Animal and Plant Health AgencyPathology Department, Animal and Plant Health AgencyArbovirus Research Team, Virology Department, Animal and Plant Health AgencyAbstract Japanese encephalitis virus (JEV), a mosquito-borne flavivirus, is the main cause of viral encephalitis in Asia. However, with changing climate JEV has the potential to emerge in novel temperate regions. Here, we have assessed the vector competence of the temperate mosquito Culex pipiens f. pipiens to vector JEV genotype III at temperatures representative of those experienced, or predicted in the future during the summer months, in the United Kingdom. Our results show that Cx. pipiens is susceptible to JEV infection at both temperatures. In addition, at 25 °C, JEV disseminated from the midgut and was recovered in saliva samples, indicating the potential for transmission. At a lower temperature, 20 °C, following an incubation period of fourteen days, there were reduced levels of JEV dissemination and virus was not detected in saliva samples. The virus present in the bodies of these mosquitoes was restricted to the posterior midgut as determined by microscopy and viable virus was successfully recovered. Apart from the influence on virus dissemination, mosquito mortality was significantly increased at the higher temperature. Overall, our results suggest that temperature is a critical factor for JEV vector competence and infected-mosquito survival. This may in turn influence the vectorial capacity of Cx. pipiens to vector JEV genotype III in temperate areas.https://doi.org/10.1038/s41598-021-85411-2
spellingShingle Arran J. Folly
Daniel Dorey-Robinson
Luis M. Hernández-Triana
Stuart Ackroyd
Beatriz Vidana
Fabian Z. X. Lean
Daniel Hicks
Alejandro Nuñez
Nicholas Johnson
Temperate conditions restrict Japanese encephalitis virus infection to the mid-gut and prevents systemic dissemination in Culex pipiens mosquitoes
Scientific Reports
title Temperate conditions restrict Japanese encephalitis virus infection to the mid-gut and prevents systemic dissemination in Culex pipiens mosquitoes
title_full Temperate conditions restrict Japanese encephalitis virus infection to the mid-gut and prevents systemic dissemination in Culex pipiens mosquitoes
title_fullStr Temperate conditions restrict Japanese encephalitis virus infection to the mid-gut and prevents systemic dissemination in Culex pipiens mosquitoes
title_full_unstemmed Temperate conditions restrict Japanese encephalitis virus infection to the mid-gut and prevents systemic dissemination in Culex pipiens mosquitoes
title_short Temperate conditions restrict Japanese encephalitis virus infection to the mid-gut and prevents systemic dissemination in Culex pipiens mosquitoes
title_sort temperate conditions restrict japanese encephalitis virus infection to the mid gut and prevents systemic dissemination in culex pipiens mosquitoes
url https://doi.org/10.1038/s41598-021-85411-2
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