Antibiotics in ingested human blood affect the mosquito microbiota and capacity to transmit malaria

Abstract

Malaria reduction is most efficiently achieved by vector control whereby human populations at high risk of contracting and transmitting the disease are protected from mosquito bites. Here, we identify the presence of antibiotics in the blood of malaria-infected people as a new risk of increasing disease transmission. We show that antibiotics in ingested blood enhance the susceptibility of Anopheles gambiae mosquitoes to malaria infection by disturbing their gut microbiota. This effect is confirmed in a semi-natural setting by feeding mosquitoes with blood of children naturally infected with Plasmodium falciparum. Antibiotic exposure additionally increases mosquito survival and fecundity, which are known to augment vectorial capacity. These findings suggest that malaria transmission may be exacerbated in areas of high antibiotic usage, and that regions targeted by mass drug administration programs against communicable diseases may necessitate increased vector control.

Early gut colonizers shape parasite susceptibility and microbiota composition in honey bee workers

“…Such dynamics are not unprecedented; experimental manipulation of microbiota has been shown to affect eukaryotic gut parasite population sizes in other insect models, such as populations of the apicomplexan parasite Plasmodium in mosquito hosts (64). In bumble bees, correlations between the size and composition of core gut microbiota and trypanosomatid populations have been observed (36,37), as well as host genotype-dependent variation to trypanosomatid susceptibility (65,66).…”

The microbiome modulates arbovirus transmission in mosquitoes

“…While a mechanistic understanding of these tripartite interactions is desirable, the development of high throughput in vitro assays capable of assessing host–microbe–pathogen interactions will undoubtedly be useful in this regard [67,68]. Alarmingly, recent work suggests it is possible that the medicinal use of antibiotics and other products is also perturbing the microbiota within mosquitoes [69 •• ,70]. Mosquitoes that fed upon humans treated with antibiotics were shown to have an altered microbiome compared to mosquitoes imbibing a blood meal from humans not using antibiotics [69 •• ].…”

“…Alarmingly, recent work suggests it is possible that the medicinal use of antibiotics and other products is also perturbing the microbiota within mosquitoes [69 •• ,70]. Mosquitoes that fed upon humans treated with antibiotics were shown to have an altered microbiome compared to mosquitoes imbibing a blood meal from humans not using antibiotics [69 •• ]. Similarly, the expulsion of antibiotics and other personal products from humans into the environment was shown in laboratory experiments to modify the larval microbiome of mosquitoes [70].…”

How micronutrients influence the physiology of mosquitoes

“…The symbiotic relationships between mosquitoes and several microorganisms have important implications in mosquitoes’ nutrition, physiology and behavior [61], as well as in mosquito immunity and vector competence [62,63]. In mosquitoes, antibiotic treatment affects reproductive output, indirectly implying an important role of microbiota in reproductive fitness [64,65]. The endosymbiotic bacteria of the genus Wolbachia are one of the most successful symbiont bacteria in the terrestrial ecosystem.…”