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

Almire, F., Terhzaz, S. , Terry, S., McFarlane, M. , Gestuveo, R. J., Szemiel, A. M., Varjak, M. , McDonald, A., Kohl, A. and Pondeville, E. (2021) Sugar feeding protects against arboviral infection by enhancing gut immunity in the mosquito vector Aedes aegypti. PLoS Pathogens, 17(9), e1009870. (doi: 10.1371/journal.ppat.1009870) (PMID:34473801) (PMCID:PMC8412342)

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Abstract

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.

Item Type:Articles
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Mcdonald, Dr Melanie and Terhzaz, Dr Selim and Gestuveo, Mr Rommel and Almire, Ms Floriane and Terry, Mrs Sandra and Szemiel, Dr Agnieszka and Mcdonald, Mrs Alma and Varjak, Dr Margus and Pondeville, Dr Emilie and Kohl, Professor Alain
Creator Roles:
Almire, F.Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Validation, Visualization, Writing – original draft, Writing – review and editing
Terhzaz, S.Investigation, Writing – review and editing
Terry, S.Investigation, Project administration
Gestuveo, R.Investigation, Writing – review and editing
Varjak, M.Resources, Writing – review and editing
Mcdonald, A.Investigation
Kohl, A.Funding acquisition, Writing – review and editing
Pondeville, E.Conceptualization, Data curation, Formal analysis, Investigation, Funding acquisition, Methodology, Project administration, Supervision, Validation, Visualization, Writing – original draft, Writing – review and editing
McFarlane, M.Investigation, Writing – review and editing
Szemiel, A. M.Investigation, Resources, Writing – review and editing
Authors: Almire, F., Terhzaz, S., Terry, S., McFarlane, M., Gestuveo, R. J., Szemiel, A. M., Varjak, M., McDonald, A., Kohl, A., and Pondeville, E.
College/School:College of Medical Veterinary and Life Sciences > Institute of Infection Immunity and Inflammation
Journal Name:PLoS Pathogens
Publisher:Public Library of Science
ISSN:1553-7366
ISSN (Online):1553-7374
Published Online:02 September 2021
Copyright Holders:Copyright © 2021 Almire et al.
First Published:First published in PLoS Pathogens 17(9): e1009870
Publisher Policy:Reproduced under a Creative Commons License
Related URLs:
Data DOI:10.5525/gla.researchdata.1094

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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
656551Arbovirus interactions with arthropod hostsAlain KohlMedical Research Council (MRC)MC_UU_12014/8MVLS III - CENTRE FOR VIRUS RESEARCH