Polyphenol-Rich Diets Exacerbate AMPK-Mediated Autophagy, Decreasing Proliferation of Mosquito Midgut Microbiota, and Extending Vector Lifespan

Abstract

BackgroundMosquitoes feed on plant-derived fluids such as nectar and sap and are exposed to bioactive molecules found in this dietary source. However, the role of such molecules on mosquito vectorial capacity is unknown. Weather has been recognized as a major determinant of the spread of dengue, and plants under abiotic stress increase their production of polyphenols.ResultsHere, we show that including polyphenols in mosquito meals promoted the activation of AMP-dependent protein kinase (AMPK). AMPK positively regulated midgut autophagy leading to a decrease in bacterial proliferation and an increase in vector lifespan. Suppression of AMPK activity resulted in a 6-fold increase in midgut microbiota. Similarly, inhibition of polyphenol-induced autophagy induced an 8-fold increase in bacterial proliferation. Mosquitoes maintained on the polyphenol diet were readily infected by dengue virus.ConclusionThe present findings uncover a new direct route by which exacerbation of autophagy through activation of the AMPK pathway leads to a more efficient control of mosquito midgut microbiota and increases the average mosquito lifespan. Our results suggest for the first time that the polyphenol content and availability of the surrounding vegetation may increase the population of mosquitoes prone to infection with arboviruses.

Midgut Mitochondrial Function as a Gatekeeper for Malaria Parasite Infection and Development in the Mosquito Host

“…In D. melanogaster, upregulation of AMPK in the midgut significantly extended lifespan (Ulgherait et al, 2014). In A. aegypti, a diet supplemented with polyphenols increased lifespan, in part through AMPK activation (Nunes et al, 2016). Our studies, however, did not replicate polyphenol-dependent life extension in A. stephensi, suggesting that these two mosquito species may have intriguing differences in longevity regulation (Johnson and Riehle, 2015).…”

Mosquito phytophagy – sources exploited, ecological function, and evolutionary transition to haematophagy

“…f. instead of a 10% sucrose solution or other plant nectar with lower protein content (but unknown sugar content) (Chen & Kearney, ). Polyphenols added to the diet of A. aegypti enhanced the autophagy in midgut cells, decreased midgut microbiota and increased mosquito longevity (Nunes et al, ). Moreover, adult female A. aegypti lived longer when they consumed aqueous extracts of pollen which can be present in nectar (Todd & Vansell, ) instead of a 10% sucrose solution, and some females even laid eggs when fed an aqueous extract of maize pollen, but not when fed a 10% sucrose solution (Eischen & Foster, ).…”

“…The underlying mechanisms that attract mosquitoes to plant tissue are barely understood but recent electrophysiological recordings revealed several classes of plant chemicals that may be involved as well as species‐specific sensitivity of mosquitoes to these chemicals (Nyasembe et al, ). Differential odour profiles of damaged and intact plants (Smith & Beck, ; Beck et al, ; Copolovici & Niinemets, ), and of water‐stressed and well‐watered plants (Copolovici & Niinemets, ; Salerno et al, ), may help mosquitoes select and feed on damaged or stressed plants (Junnila et al, ; Stone & Foster, ), which may offer more nutritional benefits to mosquitoes than healthy plants (Nunes et al, ). Applying molecular techniques, such as DNA barcoding, to identify plant genes in mosquito samples, holds great promise to determine the type of plant tissue mosquitoes feed on as well as the relative frequency of their plant feeding (Nyasembe et al, ).…”

The impact of metagenomic interplay on the mosquito redox homeostasis

“…Consistent with this, AMPK inhibition resulted in increased bacterial proliferation. The AMPK mediated midgut autophagy was involved in the microbial modulation [122]. Interestingly, resveratrol feeding had inconsistent effects on lifespan of An.…”