Abstract
The susceptibility of Anopheles mosquitoes to Plasmodium infections relies on complex interactions between the insect vector and the malaria parasite. A number of studies have shown that the mosquito innate immune responses play an important role in controlling the malaria infection and that the strength of parasite clearance is under genetic control, but little is known about the influence of environmental factors on the transmission success. We present here evidence that the composition of the vector gut microbiota is one of the major components that determine the outcome of mosquito infections. A. gambiae mosquitoes collected in natural breeding sites from Cameroon were experimentally challenged with a wild P. falciparum isolate, and their gut bacterial content was submitted for pyrosequencing analysis. The meta-taxogenomic approach revealed a broader richness of the midgut bacterial flora than previously described. Unexpectedly, the majority of bacterial species were found in only a small proportion of mosquitoes, and only 20 genera were shared by 80% of individuals. We show that observed differences in gut bacterial flora of adult mosquitoes is a result of breeding in distinct sites, suggesting that the native aquatic source where larvae were grown determines the composition of the midgut microbiota. Importantly, the abundance of Enterobacteriaceae in the mosquito midgut correlates significantly with the Plasmodium infection status. This striking relationship highlights the role of natural gut environment in parasite transmission. Deciphering microbe-pathogen interactions offers new perspectives to control disease transmission.
Highlights
Understanding how Plasmodium-Anopheles interactions contribute to the mosquito vector competence has received great attention lately, and the increasing knowledge promises to contribute to the development of new malaria control strategies [1,2,3]
Instead of eliciting immune responses leading to reduced levels of parasite burden, the experiments conducted by Cirimotich et al [24] revealed that the inhibition of Plasmodium development by commensal microbiota occurs through production of reactive oxygen species by the Enterobacter bacteria that directly target Plasmodium parasites in the midgut [17,24]
Variability in P. falciparum infection levels indicates that parasite transmission is the result of complex interactions between vectors and parasites, which rely on both genetic and environmental factors
Summary
Understanding how Plasmodium-Anopheles interactions contribute to the mosquito vector competence has received great attention lately, and the increasing knowledge promises to contribute to the development of new malaria control strategies [1,2,3]. Malaria still remains a serious health problem in developing African countries, causing more than 1 million deaths annually. Almost all these deaths are caused by the parasite Plasmodium falciparum whose major vector in Africa is Anopheles gambiae, which is widely distributed throughout the afro-tropical belt. Cirimotich et al [24] recently described an Enterobacter bacterium isolated from wild mosquitoes in Zambia that confers refractoriness to P. falciparum infection. Mechanisms mediating this refractory phenotype remain elusive. Instead of eliciting immune responses leading to reduced levels of parasite burden, the experiments conducted by Cirimotich et al [24] revealed that the inhibition of Plasmodium development by commensal microbiota occurs through production of reactive oxygen species by the Enterobacter bacteria that directly target Plasmodium parasites in the midgut [17,24]
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