Sugar feeding protects against arboviral infection by enhancing gut immunity in the mosquito vector Aedes aegypti.

As mosquito females require a blood meal to reproduce, they can act as vectors of numerous pathogens, such as arboviruses (e.g. Zika, dengue and chikungunya viruses), which constitute a substantial worldwide public health burden. In addition to blood meals, mosquito females can also take sugar meals...

Full description

Saved in:
Bibliographic Details
Main Authors: Floriane Almire, Selim Terhzaz, Sandra Terry, Melanie McFarlane, Rommel J Gestuveo, Agnieszka M Szemiel, Margus Varjak, Alma McDonald, Alain Kohl, Emilie Pondeville
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2021-09-01
Series:PLoS Pathogens
Online Access:https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1009870&type=printable
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849469877043068928
author Floriane Almire
Selim Terhzaz
Sandra Terry
Melanie McFarlane
Rommel J Gestuveo
Agnieszka M Szemiel
Margus Varjak
Alma McDonald
Alain Kohl
Emilie Pondeville
author_facet Floriane Almire
Selim Terhzaz
Sandra Terry
Melanie McFarlane
Rommel J Gestuveo
Agnieszka M Szemiel
Margus Varjak
Alma McDonald
Alain Kohl
Emilie Pondeville
author_sort Floriane Almire
collection DOAJ
description As mosquito females require a blood meal to reproduce, they can act as vectors of numerous pathogens, such as arboviruses (e.g. Zika, dengue and chikungunya viruses), which constitute a substantial worldwide public health burden. In addition to blood meals, mosquito females can also take sugar meals to get carbohydrates for their energy reserves. It is now recognised that diet is a key regulator of health and disease outcome through interactions with the immune system. However, this has been mostly studied in humans and model organisms. So far, the impact of sugar feeding on mosquito immunity and in turn, how this could affect vector competence for arboviruses has not been explored. Here, we show that sugar feeding increases and maintains antiviral immunity in the digestive tract of the main arbovirus vector Aedes aegypti. Our data demonstrate that the gut microbiota does not mediate the sugar-induced immunity but partly inhibits it. Importantly, sugar intake prior to an arbovirus-infected blood meal further protects females against infection with arboviruses from different families. Sugar feeding blocks arbovirus initial infection and dissemination from the gut and lowers infection prevalence and intensity, thereby decreasing the transmission potential of female mosquitoes. Finally, we show that the antiviral role of sugar is mediated by sugar-induced immunity. Overall, our findings uncover a crucial role of sugar feeding in mosquito antiviral immunity which in turn decreases vector competence for arboviruses. Since Ae. aegypti almost exclusively feed on blood in some natural settings, our findings suggest that this lack of sugar intake could increase the spread of mosquito-borne arboviral diseases.
format Article
id doaj-art-a90bb17098b84dda9b34aaed704a73c5
institution Kabale University
issn 1553-7366
1553-7374
language English
publishDate 2021-09-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS Pathogens
spelling doaj-art-a90bb17098b84dda9b34aaed704a73c52025-08-20T03:25:19ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742021-09-01179e100987010.1371/journal.ppat.1009870Sugar feeding protects against arboviral infection by enhancing gut immunity in the mosquito vector Aedes aegypti.Floriane AlmireSelim TerhzazSandra TerryMelanie McFarlaneRommel J GestuveoAgnieszka M SzemielMargus VarjakAlma McDonaldAlain KohlEmilie PondevilleAs mosquito females require a blood meal to reproduce, they can act as vectors of numerous pathogens, such as arboviruses (e.g. Zika, dengue and chikungunya viruses), which constitute a substantial worldwide public health burden. In addition to blood meals, mosquito females can also take sugar meals to get carbohydrates for their energy reserves. It is now recognised that diet is a key regulator of health and disease outcome through interactions with the immune system. However, this has been mostly studied in humans and model organisms. So far, the impact of sugar feeding on mosquito immunity and in turn, how this could affect vector competence for arboviruses has not been explored. Here, we show that sugar feeding increases and maintains antiviral immunity in the digestive tract of the main arbovirus vector Aedes aegypti. Our data demonstrate that the gut microbiota does not mediate the sugar-induced immunity but partly inhibits it. Importantly, sugar intake prior to an arbovirus-infected blood meal further protects females against infection with arboviruses from different families. Sugar feeding blocks arbovirus initial infection and dissemination from the gut and lowers infection prevalence and intensity, thereby decreasing the transmission potential of female mosquitoes. Finally, we show that the antiviral role of sugar is mediated by sugar-induced immunity. Overall, our findings uncover a crucial role of sugar feeding in mosquito antiviral immunity which in turn decreases vector competence for arboviruses. Since Ae. aegypti almost exclusively feed on blood in some natural settings, our findings suggest that this lack of sugar intake could increase the spread of mosquito-borne arboviral diseases.https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1009870&type=printable
spellingShingle Floriane Almire
Selim Terhzaz
Sandra Terry
Melanie McFarlane
Rommel J Gestuveo
Agnieszka M Szemiel
Margus Varjak
Alma McDonald
Alain Kohl
Emilie Pondeville
Sugar feeding protects against arboviral infection by enhancing gut immunity in the mosquito vector Aedes aegypti.
PLoS Pathogens
title Sugar feeding protects against arboviral infection by enhancing gut immunity in the mosquito vector Aedes aegypti.
title_full Sugar feeding protects against arboviral infection by enhancing gut immunity in the mosquito vector Aedes aegypti.
title_fullStr Sugar feeding protects against arboviral infection by enhancing gut immunity in the mosquito vector Aedes aegypti.
title_full_unstemmed Sugar feeding protects against arboviral infection by enhancing gut immunity in the mosquito vector Aedes aegypti.
title_short Sugar feeding protects against arboviral infection by enhancing gut immunity in the mosquito vector Aedes aegypti.
title_sort sugar feeding protects against arboviral infection by enhancing gut immunity in the mosquito vector aedes aegypti
url https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1009870&type=printable
work_keys_str_mv AT florianealmire sugarfeedingprotectsagainstarboviralinfectionbyenhancinggutimmunityinthemosquitovectoraedesaegypti
AT selimterhzaz sugarfeedingprotectsagainstarboviralinfectionbyenhancinggutimmunityinthemosquitovectoraedesaegypti
AT sandraterry sugarfeedingprotectsagainstarboviralinfectionbyenhancinggutimmunityinthemosquitovectoraedesaegypti
AT melaniemcfarlane sugarfeedingprotectsagainstarboviralinfectionbyenhancinggutimmunityinthemosquitovectoraedesaegypti
AT rommeljgestuveo sugarfeedingprotectsagainstarboviralinfectionbyenhancinggutimmunityinthemosquitovectoraedesaegypti
AT agnieszkamszemiel sugarfeedingprotectsagainstarboviralinfectionbyenhancinggutimmunityinthemosquitovectoraedesaegypti
AT margusvarjak sugarfeedingprotectsagainstarboviralinfectionbyenhancinggutimmunityinthemosquitovectoraedesaegypti
AT almamcdonald sugarfeedingprotectsagainstarboviralinfectionbyenhancinggutimmunityinthemosquitovectoraedesaegypti
AT alainkohl sugarfeedingprotectsagainstarboviralinfectionbyenhancinggutimmunityinthemosquitovectoraedesaegypti
AT emiliepondeville sugarfeedingprotectsagainstarboviralinfectionbyenhancinggutimmunityinthemosquitovectoraedesaegypti