An integrated overview of the midgut bacterial flora composition of Phlebotomus perniciosus, a vector of zoonotic visceral leishmaniasis in the Western Mediterranean Basin

Abstract

BackgroundThe Leishmania developmental life cycle within its sand fly vector occurs exclusively in the lumen of the insect’s digestive tract in the presence of symbiotic bacteria. The composition of the gut microbiota and the factors that influence its composition are currently poorly understood. A set of factors, including the host and its environment, may influence this composition. It has been demonstrated that the insect gut microbiota influences the development of several human pathogens, such as Plasmodium falciparum. For sand flies and Leishmania, understanding the interactions between the parasite and the microbial environment of the vector midgut can provide new tools to control Leishmania transmission.Methodology/Principal findingsThe midguts of female Phlebotomus perniciosus from laboratory colonies or from the field were collected during the months of July, September and October 2011 and dissected. The midguts were analyzed by culture-dependent and culture-independent methods. A total of 441 and 115 cultivable isolates were assigned to 30 and 11 phylotypes from field-collected and colonized P. perniciosus, respectively. Analysis of monthly variations in microbiota composition shows a species diversity decline in October, which is to the end of the Leishmania infantum transmission period. In parallel, a compilation and a meta-analysis of all available data concerning the microbiota of two Psychodidae genera, namely Phlebotomus and Lutzomyia, was performed and compared to P. perniciosus, data obtained herein. This integrated analysis did not reveal any substantial divergences between Old and New world sand flies with regards to the midgut bacterial phyla and genera diversity. But clearly, most bacterial species (>76%) are sparsely distributed between Phlebotominae species.Conclusion/SignificanceOur results pinpoint the need for a more exhaustive understanding of the bacterial richness and abundance at the species level in Phlebotominae sand flies in order to capture the role of midgut bacteria during Leishmania development and transmission. The occurrence of Bacillus subtilis in P. perniciosus and at least two other sand fly species studied so far suggests that this bacterial species is a potential candidate for paratransgenic or biolological approaches for the control of sand fly populations in order to prevent Leishmania transmission.

Leishmania, microbiota and sand fly immunity

“…In a recent publication focusing on the identification of resident microbiota of Phlebotomus perniciosus from the Western Mediterranean region, the authors performed a network analysis which suggests a pattern of interactions between sand flies and their microbiota ( Fig. 1 ) (Fraihi et al , 2017 ). The knowledge of the presence of a given bacterial species on various sand fly species might help in the development of paratransgenic bacteria targeting multiple vectors.…”

“…The network representation suggests some relationships between the 11 studied New World and Old World sand fly species and the bacteria inhabiting their gut. Bacillus thuringiensis was isolated from L. evansi and P. chinensis , two sand fly species belonging to the New World and Old World, respectively (Fraihi et al , 2017 ). …”

“…A study of the microbial gut content of Phlebotomus perniciosus collected in Tunis used culture-dependent and -independent techniques for bacteria identification (Fraihi et al , 2017 ). When authors compared gut contents from field-caught and colony-reared insects they found that Stenotrophomonas maltophilia , Bacillus sp.…”

“…and Lysinibacillus sp. are common to both groups of insects, suggesting that control strategies developed under laboratory conditions might be useful in the field (Fraihi et al , 2017 ). In the same report, the authors show that variations in the resident microbiota are influenced by the sand fly species and particularities of niches where these insects live.…”

“…Acinetobacter baumanii , E. coli , Stenotrophamonas maltophila , B. subtilis , Staphylococcus epidermidis , Acinetobacter sp., Enterobacter sp., Klebsiella ozaenae and Serratia sp. are shared among at least three phlebotomine insects from Old and New World (Fraihi et al , 2017 ).…”