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Background  Malaria exerts a tremendous socioeconomic impact worldwide despite current control efforts, and novel disease transmission-blocking strategies are urgently needed. The  Enterobacter  bacterium  Esp_Z , which is naturally harboured in the mosquito midgut, can inhibit the development of  Plasmodium  parasites prior to their invasion of the midgut epithelium through a mechanism that involves oxidative stress. Here, a multifaceted approach is used to study the tripartite interactions between the mosquito,  Esp_Z  and  Plasmodium,  towards addressing the feasibility of using sugar-baited exposure of mosquitoes to the  Esp_Z  bacterium for interruption of malaria transmission.    Methods  The ability of  Esp_Z  to colonize  Anopheles gambiae  midguts harbouring microbiota derived from wild mosquitoes was determined by qPCR. Upon introduction of  Esp_Z  via nectar feeding, the permissiveness of colonized mosquitoes to  Plasmodium falciparum  infection was determined, as well as the impact of  Esp_Z  on mosquito fitness parameters, such as longevity, number of eggs laid and number of larvae hatched. The genome of  Esp_Z  was sequenced, and transcriptome analyses were performed to identify bacterial genes that are important for colonization of the mosquito midgut, as well as for ROS-production. A gene expression analysis of members of the oxidative defence pathway of  Plasmodium berghei  was also conducted to assess the parasite’s oxidative defence response to  Esp_Z  exposure.    Results   Esp_Z  persisted for up to 4 days in the  An. gambiae  midgut after introduction via nectar feeding, and was able to significantly inhibit  Plasmodium  sporogonic development. Introduction of this bacterium did not adversely affect mosquito fitness. Candidate genes involved in the selection of a better fit  Esp_Z  to the mosquito midgut environment and in its ability to condition oxidative status of its surroundings were identified, and parasite expression data indicated that  Esp_Z  is able to induce a partial and temporary shutdown of the ookinetes antioxidant response.    Conclusions   Esp_Z  is capable of inhibiting sporogonic development of  Plasmodium  in the presence of the mosquito’s native microbiota without affecting mosquito fitness. Several candidate bacterial genes are likely mediating midgut colonization and ROS production, and inhibition of  Plasmodium  development appears to involve a shutdown of the parasite’s oxidative defence system. A better understanding of the complex reciprocal tripartite interactions can facilitate the development and optimization of an  Esp_Z -based malaria control strategy.    Electronic supplementary material  The online version of this article (doi:10.1186/s12936-016-1468-2) contains supplementary material, which is available to authorized users.

Functional genomic analyses of Enterobacter, Anopheles and Plasmodium reciprocal interactions that impact vector competence