Microbiota-driven, strain-specific Asaia colonisation modulates mosquito vector competence

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Abstract

Microbiota-based mosquito control strategies are founded on the ability of bacterial symbionts to modify host biology and/or pathogen transmission. However, symbionts do not operate in isolation. Their colonisation, persistence and biological effects arise within a complex ecological network comprising the host and its resident microbiota. We hypothesized that colonisation success is not only an intrinsic property of a bacterial symbiont but emerges from interactions between bacterial strain, host background, and the native microbial community. To test this, we compared recolonisation by endogenous and exogenous Asaia strains in the invasive mosquito Aedes koreicus using wild-type and axenic mosquitoes to experimentally manipulate the microbial composition. We found that endogenous and exogenous strains followed distinct colonisation trajectories. Depletion of the resident microbiota selectively rescued colonisation by the endogenous strain, whereas both strains successfully disseminated to transmission-relevant tissues despite contrasting early gut dynamics. Furthermore, these strain-specific colonisation dynamics were associated with increased Semliki Forest virus (SFV) transmission and enhanced adult longevity, particularly following colonisation by the exogenous strain. Our findings indicate that resident microbial communities act as selective ecological filters that shape symbiont colonisation in a strain-dependent manner. More broadly, this study demonstrates that the biological effects of mosquito symbionts emerge from interactions between bacterial strains and the microbial community context, providing an ecological framework for the rational and effective development of microbiota-based vector control strategies.

Importance

Bacterial symbionts are increasingly being explored as tools to reduce mosquito-borne disease; however, their effects can vary depending on the mosquito host and its microbial community. Thus, a deeper understanding of the interactions among symbionts, their host, and resident microbiota is needed. In this work, we show that resident bacteria can determine whether different Asaia strains successfully establish in the invasive mosquito Aedes koreicus , demonstrating that symbiont establishment is shaped by interactions within the microbial community rather than by the introduced bacterium alone. Furthermore, successful colonisation was associated with changes in virus transmission and mosquito longevity. These findings show that the microbial environment of a mosquito is an important factor to consider when developing symbiont-based approaches for controlling mosquito-borne diseases.

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