Nutritional stress compromises mosquito fitness and antiviral immunity, while enhancing dengue virus infection susceptibility

Authors: YAN, JIAYUE - Illinois Natural History Survey; KIM, CHANG-HYUN - Illinois Natural History Survey; CHESSER, LETA - Illinois Natural History Survey; Ramirez, Jose; STONE, CHRIS - Illinois Natural History Survey

Submitted to: Communications Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/27/2023
Publication Date: 11/6/2023
Citation: Yan, J., Kim, C., Chesser, L., Ramirez, J.L., Stone, C.M. 2023. Nutritional stress compromises mosquito fitness and antiviral immunity, while enhancing dengue virus infection susceptibility. Communications Biology. 6. Article 1123. https://doi.org/10.1038/s42003-023-05516-4.
DOI: https://doi.org/10.1038/s42003-023-05516-4

Interpretive Summary: Mosquitoes often encounter environments with different levels of available nutrients. A proper nutrition is not only critical for insect growth, but it also determines their ability to fight microbial infections. This study investigated the effect of poor nutrition on mosquito longevity, reproduction, and on their ability to be infected by dengue virus. Results from this study indicate that mosquitoes that had limited nutrition had smaller adult size, short longevity and diminished reproduction. Furthermore, smaller mosquitoes and those that lacked nutrition as adults, were more likely to get infected with dengue virus. Analysis of gene expression indicated that nutrition-deprived mosquitoes had an impaired immune response that likely contributed to their susceptibility to dengue virus. This study highlights the critical role that mosquito nutrition plays in driving the transmission of mosquito-borne diseases.

Technical Abstract: Diet-induced nutritional stress plays a key role in regulating health and disease outcomes, primarily because of its interaction with the immune system. Such interactions have been investigated extensively in human and other vertebrate model organisms, while less is known regarding the impacts on mosquito vectors and their interactions with pathogens. In mosquitoes, diet-induced nutritional stress may affect their vectorial capacity, a measure of mosquito’s potential to transmit pathogens, likely through its impact on phenotypic traits, infection susceptibility and immune performance. However, how these three factors are affected by both larval and adult nutritional stress remains unclear. Here, we manipulated mosquito diet to create two levels of nutrition at both larval and adult stages and evaluated the effects of low nutrition (nutritional stress) on life history traits, vector competence for dengue virus, and antiviral immune gene expression in the mosquito Aedes aegypti. We demonstrate that nutritional stress during larval and adult stages negatively affects adult size and survival, respectively, and synergistically reduce the fecundity of Ae. aegypti. Mosquitoes that experienced nutritional stress as adults, but not as larvae, were more susceptible to becoming infected with dengue virus after ingesting an infectious blood meal, but developed lower viral titers than their unstressed counterparts. Smaller mosquitoes were also more likely to become infected. In addition, the mosquito immune response to dengue virus infection appears to be suppressed by both larval and adult nutritional stress with distinct involvement of key immune signaling pathways. Overall, our findings demonstrate a crucial role of nutritional stress in mosquito life history traits, infection outcome and immune response which in turn influence vectorial capacity for dengue virus. Since nutrition is often limited in natural settings, our findings underscore the critical role that mosquito nutrition plays in driving the transmission of mosquito-borne diseases.