Abstract
A host’s immune system plays a central role in shaping the composition of the microbiota and, in return, resident microbes influence immune responses. Symbiotic associations of the maternally transmitted bacterium Wolbachia occur with a wide range of arthropods. It is, however, absent from the dengue and Zika vector mosquito Aedes aegypti in nature. When Wolbachia is artificially forced to form symbiosis with this new mosquito host, it boosts the basal immune response and enhances the mosquito’s resistance to pathogens, including dengue, Zika virus and malaria parasites. The mechanisms involved in establishing a symbiotic relationship between Wolbachia and A. aegypti, and the long-term outcomes of this interaction, are not well understood. Here, we have demonstrated that both the immune deficiency (IMD) and Toll pathways are activated by the Wolbachia strain wAlbB upon its introduction into A. aegypti. Silencing the Toll and IMD pathways via RNA interference reduces the wAlbB load. Notably, wAlbB induces peptidoglycan recognition protein (PGRP)-LE expression in the carcass of A. aegypti, and its silencing results in a reduction of symbiont load. Using transgenic mosquitoes with stage-specific induction of the IMD and Toll pathways, we have shown that elevated wAlbB infection in these mosquitoes is maintained via maternal transmission. These results indicate that host innate immunity is utilized to establish and promote host-microbial symbiosis. Our results will facilitate a long-term projection of the stability of the Wolbachia–A. aegypti mosquito system that is being developed to control dengue and Zika virus transmission to humans.
Highlights
Mosquitoes transmit numerous devastating human diseases such as Zika, dengue and malaria
Using transgenic mosquitoes with stage-specific induction of the immune deficiency (IMD) and Toll pathways, we have shown that elevated wAlbB infection in these mosquitoes is maintained via maternal transmission
It is unknown whether deficiency (IMD) signaling pathways activate two boosting the immune response prevents overdistinct nuclear factor-kappaB-IkB transcription fac- proliferation of Wolbachia or promotes the establishtors, REL1 and REL2, respectively, to induce the ment and maintenance of symbiosis with this expression of antimicrobial peptides
Summary
Symbiotic associations of the maternally transmitted bacterium Wolbachia occur with a wide range of arthropods. It is, absent from the dengue and Zika vector mosquito Aedes aegypti in nature. Using transgenic mosquitoes with stage-specific induction of the IMD and Toll pathways, we have shown that elevated wAlbB infection in these mosquitoes is maintained via maternal transmission. These results indicate that host innate immunity is utilized to establish and promote host-microbial symbiosis. Our results will facilitate a long-term projection of the stability of the Wolbachia–A. aegypti mosquito system that is being developed to control dengue and Zika virus transmission to humans. The ISME Journal (2018) 12, 277–288; doi:10.1038/ismej.2017.174; published online 3 November 2017
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