Host-environment interplay shapes fungal diversity in mosquitoes

Authors: TAWIDIAN, PATIL - Kansas State University; COON, KERRI - University Of Wisconsin; JUMPPONEN, ARI - Kansas State University; Cohnstaedt, Lee; MICHEL, KRISTIN - Kansas State University

Submitted to: mSphere
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/8/2021
Publication Date: N/A
Citation: N/A

Interpretive Summary: Aquatic immature mosquito larvae are exposed to bacteria and fungi as they develop prior to emergence as adults. The consequences of bacterial exposure and the following colonization of the mosquito by bacteria has large consequences to the mosquitoes ability to transmit pathogens as an adult while taking blood meals. However the consequences of fungal infection is very poorly studied. This study examines the diversity and colonization of fungus during the mosquitoes life history. Genetic sequences of fungal mitochondrial genes were used to identify and classify the fungi in the water and in the Aedes albopictus larval mosquitoes. An unprecedented variation in the fungi was found in the water of containers and this was a different combination of fungi than was found in the mosquito gut and other tissues, although the gut fungi were more similar to the water fungi diversity. The midgut is the major factor filtering the assembly of fungi found in the mosquito and not the environment. These results also identify mosquito feeding behavior and fungal mode of nutrition as potential drivers of tissue-specific fungi after environmental acquisition. IMPORTANCE The Asian tiger mosquito, Aedes albopictus, is the dominant mosquito species in the USA and an important vector of viruses of major public health concern. One aspect of mosquito control to curb mosquito-borne diseases has been the use of biological control agents such as fungal pathogens targeting insects. Recent studies also demonstrate the impact of mosquito-associated microbial communities on various mosquito traits, including vector competence. However, while much research attention has been dedicated to understanding the diversity and function of mosquito-associated bacterial communities, relatively little is known about mosquito-associated fungal communities. A better understanding of the factors that drive fungal diversity and assembly in mosquitoes will be essential for future efforts to target mosquito microbes and fungi for mosquito and mosquito-borne disease control.

Technical Abstract: Mosquito larvae encounter diverse assemblages of bacteria (i.e. ‘microbiota’) and fungi (i.e. ‘mycobiota’) in the aquatic environments they develop in. However, while a number of studies have addressed the diversity and function of microbiota in mosquito life history, relatively little is known about mosquito-mycobiota interactions outside of several key fungal entomopathogens. In this study, we used high-throughput sequencing of ITS2 gene amplicons to provide the first simultaneous characterization of the mycobiota in field-collected Aedes albopictus larvae and their associated aquatic environments. Our results reveal unprecedented variation in mycobiota among adjacent but discrete larval breeding habitats. Our results also reveal distinct mycobiota assembly in the mosquito gut versus other tissues, with gut-associated fungal communities being most similar to those present in the environment where larvae feed. Altogether, our results identify the environment as the dominant factor shaping mosquito mycobiota with no evidence of environmental filtering of the gut mycobiota. These results also identify mosquito feeding behavior and fungal mode of nutrition as potential drivers of tissue-specific mycobiota assembly after environmental acquisition. IMPORTANCE The Asian tiger mosquito, Aedes albopictus, is the dominant mosquito species in the USA and an important vector of arboviruses of major public health concern. One aspect of mosquito control to curb mosquito-borne diseases has been the use of biological control agents such as fungal entomopathogens. Recent studies also demonstrate the impact of mosquito-associated microbial communities on various mosquito traits, including vector competence. However, while much research attention has been dedicated to understanding the diversity and function of mosquito-associated bacterial communities, relatively little is known about mosquito-associated fungal communities. A better understanding of the factors that drive mycobiota diversity and assembly in mosquitoes will be essential for future efforts to target mosquito micro- and mycobiomes for mosquito and mosquito-borne disease control.