Environmental yeasts differentially impact the development and oviposition behavior of the Asian tiger mosquito Aedes albopictus.

Background: While the Asian tiger mosquito (Aedes albopictus), a known vector of many arboviruses, establishes symbiotic associations with environmentally acquired yeasts, their impact on mosquito biology remains poorly investigated. To better understand these associations, we hypothesized that waterborne yeasts colonizing the larval gut differentially support mosquito development based on their capacity to produce riboflavin or recycle nitrogen waste into proteins by secreting uricase, as B vitamins and amino acids are crucial for mosquito development. To address this hypothesis, we used axenic and gnotobiotic insects to gauge the specific impact of different environmental yeasts on Ae. albopictus development and survival. We then evaluated whether the observed variations across yeast species could be linked to differential uricolytic activities and varying quantities of riboflavin and proteins in insecta. Finally, given that mosquito oviposition site selection favors conditions that enhance offspring performance, we tested whether yeasts that promote faster development mediate oviposition site selection by gravid females.

Results: Differences in mosquito development times were observed based on the environmental yeast used. Yeasts like Rhodotorula mucilaginosa and Aureobasidium pullulans promoted rapid development and were associated with improved survival. Conversely, yeasts such as Torulaspora delbrueckii and Martiniozyma asiatica, which led to slower development, produced smaller adults. Notably, R. mucilaginosa, which promoted the fastest development, provided high riboflavin intakes and enhance nitrogenous waste recycling and protein synthesis through strong uricolytic-ureolytic activity. Behavioral experiments indicated that yeasts promoting rapid development "attract gravid females.

Conclusions: Our findings highlight that a set of environmental yeasts present in natural larval breeding sites can be associated with improved mosquito development and survival by enhancing nutritional intake, thereby attracting gravid females. Variations in mosquito development time are likely linked to the differential levels of riboflavin production and nitrogenous waste recycling capacities among yeast species. This study opens new perspectives on the trophic interactions between mosquitoes and their mycobiota, emphasizing the importance of nitrogen-containing molecules such as essential amino acids, proteins, or vitamins provided by the mycobiota. Video Abstract.