Midgut Microbiota of the Malaria Mosquito Vector Anopheles gambiae and Interactions with Plasmodium falciparum Infection

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.

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“…The filtering steps were performed using the QIIME pipeline 34 . Strict dereplication (clustering of duplicate sequences) was performed on the filtered sequences, and they were then sorted by decreasing number of abundance [35][36][37] . For each metagenome, the clustering of OTUs was performed with 97% identity.…”

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“…Gut microbiota are also key to the infection process itself (Boissière et al, 2012;Borriello, 1990;Broderick et al, 2006;Charroux and Royet, 2012;Cirimotich et al, 2011;Harp et al, 1992;Weiss and Aksoy, 2011;Wilks and Golovkina, 2012). Microbes from the gut can directly interact with parasites through the secretion of inhibitory compounds.…”