In nature, female mosquitoes take successive blood meals during which they are exposed to a variety of microbes present in the host. In Africa, Trypanosoma parasites, causing trypanosomiases, are sympatric with the malaria parasites. In recent work, we showed that pre-exposure of Anopheles mosquitoes to Trypanosoma enhances their vector competence to malaria parasites, reduces their reproductive fitness and modulates their bacterial gut flora.
During a blood meal, female Anopheles mosquitoes are potentially exposed to diverse microbes in addition to the malaria parasite, Plasmodium. Human and animal African trypanosomiases are frequently co-endemic with malaria in Africa. It is not known whether exposure of Anopheles to trypanosomes influences their fitness or ability to transmit Plasmodium. Using cell and molecular biology approaches, we found that Trypanosoma brucei brucei parasites survive for at least 48h in the midgut of the major malaria vector Anopheles coluzzii after uptake of an infectious blood meal. This transient survival of trypanosomes in the midgut is correlated with an alteration in the abundance of the enteric bacterial flora in Anopheles coluzzii. Using a developmental biology approach, we found that the presence of live trypanosomes in mosquito midguts also reduces their reproductive fitness, as it impairs the viability of laid eggs by affecting their hatching in water. Furthermore, we found that Anopheles exposure to trypanosomes enhances their vector competence for Plasmodium, as it increases their infection prevalence. The increased susceptibility to Plasmodium was microbiome-dependent, while the reproductive fitness cost was dependent only on the presence of live trypanosomes, but independent of the microbiome. Transcriptomic analysis revealed that expression of only two Anopheles immune genes are modulated during trypanosome exposure, suggesting that the mosquito immune system is not or weakly elicited by Trypanosoma. Taken together, these results demonstrate multiple effects upon Anopheles vector competence for Plasmodium caused by eukaryotic microbes interacting with the host and its microbiome, which may in turn have implications for malaria control strategies in co-endemic areas.
This study is part of the priority scientific area Emerging infectious diseases of the Institut Pasteur's strategic plan for 2019-2023.