Egg-laying by female Aedes aegypti shapes the bacterial communities of breeding sites

BMC Biology, 21:97, 2023

Katherine D. Mosquera, Luis Eduardo Martínez Villegas, Gabriel Rocha Fernandes, Mariana Rocha David, Rafael Maciel-de-Freitas, Luciano A. Moreira, Marcelo G. Lorenzo,

Abstract

Background

Aedes aegypti, the main arboviral mosquito vector, is attracted to human dwellings and makes use of human-generated breeding sites. Past research has shown that bacterial communities associated with such sites undergo compositional shifts as larvae develop and that exposure to different bacteria during larval stages can have an impact on mosquito development and life-history traits. Based on these facts, we hypothesized that female Ae. aegypti shape the bacteria communities of breeding sites during oviposition as a form of niche construction to favor offspring fitness.

Results

To test this hypothesis, we first verified that gravid females can act as mechanical vectors of bacteria. We then elaborated an experimental scheme to test the impact of oviposition on breeding site microbiota. Five different groups of experimental breeding sites were set up with a sterile aqueous solution of larval food, and subsequently exposed to (1) the environment alone, (2) surface-sterilized eggs, (3) unsterilized eggs, (4) a non-egg laying female, or (5) oviposition by a gravid female. The microbiota of these differently treated sites was assessed by amplicon-oriented DNA sequencing once the larvae from the sites with eggs had completed development and formed pupae. Microbial ecology analyses revealed significant differences between the five treatments in terms of diversity. In particular, between-treatment shifts in abundance profiles were detected, showing that females induce a significant decrease in microbial alpha diversity through oviposition. In addition, indicator species analysis pinpointed bacterial taxa with significant predicting values and fidelity coefficients for the samples in which single females laid eggs. Furthermore, we provide evidence regarding how one of these indicator taxa, Elizabethkingia, exerts a positive effect on the development and fitness of mosquito larvae.

Conclusions

Ovipositing females impact the composition of the microbial community associated with a breeding site, promoting certain bacterial taxa over those prevailing in the environment. Among these bacteria, we found known mosquito symbionts and showed that they can improve offspring fitness if present in the water where eggs are laid. We deem this oviposition-mediated bacterial community shaping as a form of niche construction initiated by the gravid female.

Keywords

Aedes aegypti, Microbiota, Breeding sites, Oviposition, Niche construction



Detection of profile shifts on microbial communities induced by oviposition-related inputs. An experimental scheme was elaborated to dissect the effects of the act of oviposition from other sources affecting microbial profiles observed after mosquito-water interactions. DNA extracted from water samples belonging to five different treatments was subjected to amplicon-oriented sequencing to characterize the structure of their bacterial communities. Treatment 1 (T1): environmental control (type I water plus sterilized food). Treatment 2 (T2): manually-deposited sterilized mosquito eggs. Treatment 3 (T3): manually-deposited non-sterilized eggs. Treatment 4 (T4): single sugar-fed females interacting with container water. Treatment 5 (T5): single gravid female (72 h post-blood-feeding) allowed to lay eggs

DOI: https://doi.org/10.1186/s12915-023-01605-2