Malagasy flea microbiota results from a combination of vertically transmitted and environmentally acquired microbes

Fleas (Insecta, Siphonaptera) are the known vectors of serious bacterial pathogens, such as Yersinia pestis and Rickettsia typhi. The microbiota of fleas has been poorly investigated although it has a known influence on vector competence. Here, we report and analyse the microbiota of 577 flea specimens from Madagascar, a hotspot of plague transmission. Importantly, endemic Malagasy fleas show low host specificity, allowing addressing the importance of vertebrate host species in microbiota composition, as well as that of abiotic variables. We describe through Illumina sequencing of 2 hypervariable regions of 16 S rDNA the bacterial composition of 577 flea specimens of Madagascar. We address the importance of biotic (mammalian host and flea species) and abiotic (season and sampling site) variables on bacterial community composition. Bacterial composition appears driven by flea species and season, but interestingly not by the flea's vertebrate hosts. These results suggest that the flea microbiota is at least in part acquired before they become adult, possibly in the immature off-host stages. Taken together, our results suggest that the microbiota of sampled fleas are composed of bacterial taxa with vertical transmission, such as Wolbachia which are prevalent in the present dataset, together with several bacterial taxa for which the occurrence is driven by environment factors, especially season and habitat. Given the importance of the microbiota in vector competence, we discuss the epidemiological consequences of environmentally-driven acquisition of microbiota in fleas on plague transmission in Madagascar.