Shifts in the microbiota associated with male mosquitoes (Aedes aegypti) exposed to an obligate gut fungal symbiont (Zancudomyces culisetae)

Jonas Frankel-Bricker

doi:10.1038/s41598-020-69828-9

Abstract

Research characterizing arthropod-associated microbiota has revealed that microbial dynamics can have an important impact on host phenotypic traits. The influence of fungi on these interactions are emerging as targets for research, especially in organisms associated with global human health. A recent study demonstrated colonization of a widespread gut fungus (Zancudomyces culisetae) in a larval mosquito (Aedes aegypti) digestive tract affected microbiomes in larvae and newly emerged adult females (Frankel-Bricker et al. Appl Environ Microbiol, 2020. https://doi.org/10.1128/AEM.02334-19) but did not investigate these processes in males. The objective of the study presented here was to assess fungal influences on adult male mosquito microbiomes to enable a more complete assessment of fungal–bacterial–host interactions in the A. aegypti–Z. culisetae system. Sequencing of 16S rRNA gene amplicons from microbiomes harbored in adult males directly after emerging from pupae revealed larval fungal exposure significantly decreased overall microbial community diversity, altered microbiome composition and structure, and decreased within-group microbiome variation across individuals. Further, bacteria in the family Burkholderiaceae were present in high abundance in fungal-exposed males, likely contributing to the disparate microbiota between treatment groups. Comparisons between male and the female microbiomes analyzed in Frankel-Bricker et al. (2020), showed distinct shifts in bacterial communities incurred by larval exposure to fungi, potentially revealing sex-specific fungal–bacterial–host dynamics in A. aegypti. These findings highlight the complex role a gut fungus can play in influencing the microbial communities harbored in an important insect and emphasize the significance of accounting for an organism’s sex when studying fungal–bacterial–host dynamics.

Highlights

Mosquitoes harbor communities of microbes that impact host phenotypic t raits[1,2]
Larval fungal colonization was found to reduce the variation of bacterial community diversity and distribution across individuals, differentially affect the transference efficacy of certain bacterial taxa from larvae to adults, and increase the overall diversity of initial microbiomes acquired by newly emerged adult females
Complex fungal–bacterial–host interactions were revealed, the study did not investigate whether similar dynamics took place in male mosquitoes

Summary

Introduction

Mosquitoes harbor communities of microbes that impact host phenotypic t raits[1,2]. Studies investigating factors that contribute to microbial community dynamics provide valuable biological insights into these insects of global significance. The same bacteria exhibit distinct interactions dependent on their presence in either the testes or o varies[33] These sex-specific dynamics are affected by temporal factors during larval development[34], suggesting unique features of these organs, such as morphological or physiological characteristics, influence certain microbial interactions. A key interpretation of these patterns was that morphological (expansion of fungal tissue) and physiological (altered nutrient dynamics in the digestive tract) disturbances resulting from fungal colonization of the larval h indgut[47,48] could have altered microbial interactions and spatial distributions of bacteria[49], leading to differential transstadial transmission outcomes of certain bacteria and disparate initial adult female microbiomes in the presence or absence of the fungus. Maleassociated microbial communities may respond differently to fungal colonization of the larval digestive tract due to unique anatomical characteristics, this concept has never been studied

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