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.
Highlights
Male and female adult mosquitoes regularly feed on plant nectar, intaking carbohydrates for their energy reserves [1,2]
In addition to blood feeding, they can feed on sugar sources to get carbohydrates for their energy reserves
The sugar solution is periodically relocated from the crop to the midgut for digestion according to metabolic/physiological needs (S1 Fig; [2,30,31])
Summary
Male and female adult mosquitoes regularly feed on plant nectar, intaking carbohydrates for their energy reserves [1,2]. The blood meal is largely used to provide proteins (i.e. amino acids), necessary for the synthesis of yolk proteins and for reproductive output [3]. This blood meal requirement for reproduction, and the fact that a female mosquito can take several blood meals throughout its adult life, results in Ae. aegypti being a vector of numerous arthropod-borne viruses (arboviruses). When a mosquito ingests a blood meal from an arbovirusinfected vertebrate host, the arbovirus initially infects the mosquito gut, disseminates to other tissues before reaching the salivary glands. Once the salivary glands are infected, the arbovirus can be transmitted to a new vertebrate host during a subsequent blood meal. Arboviruses transmitted by mosquitoes, such as dengue (DENV), chikungunya (CHIKV), and Zika (ZIKV) viruses, constitute a substantial worldwide public health threat and economic burden with an increasing population at risk due to an expansion of their geographical range and an unprecedented emergence of epidemic arboviral diseases [4,5,6,7,8]
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