Leishmania, microbiota and sand fly immunity

Abstract

In this review, we explore the state-of-the-art of sand fly relationships with microbiota, viruses and Leishmania, with particular emphasis on the vector immune responses. Insect-borne diseases are a major public health problem in the world. Phlebotomine sand flies are proven vectors of several aetiological agents including viruses, bacteria and the trypanosomatid Leishmania, which are responsible for diseases such as viral encephalitis, bartonellosis and leishmaniasis, respectively. All metazoans in nature coexist intimately with a community of commensal microorganisms known as microbiota. The microbiota has a fundamental role in the induction, maturation and function of the host immune system, which can modulate host protection from pathogens and infectious diseases. We briefly review viruses of public health importance present in sand flies and revisit studies done on bacterial and fungal gut contents of these vectors. We bring this information into the context of sand fly development and immune responses. We highlight the immunity mechanisms that the insect utilizes to survive the potential threats involved in these interactions and discuss the recently discovered complex interactions among microbiota, sand fly, Leishmania and virus. Additionally, some of the alternative control strategies that could benefit from the current knowledge are considered.

Keywords: Leishmania; microbiota; sand fly; vector–microbe interaction; viruses.

Fig. 1.

Network analysis showing the shared bacteria species found in sand flies. Phlebotomus sand flies are identified by squares surrounded by green and bacteria found in Lutzomyia sand flies identified with squares surrounded by blue. Coloured circles represent bacteria species that are shared between sand flies species. White circles represent bacteria species that are unique to each of the sand flies species and are listed inside large rectangles. 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).

Fig. 2.

Lutzomyia longipalpis gut microbiota. Network analysis showing bacteria genera found in L. longipalpis obtained from field collections or laboratory-reared colonies. Feeding regimens are indicated: field (unknown feeding conditions), sucrose, blood, or infected by Leishmania (laboratory artificial feeding). Coloured border rectangles indicate bacteria genera found under each feeding regimen or shared between them. References used: Oliveira et al. (2000); Perira et al. (2001); Gouveia et al. (2008); McCarthy et al. (2011); Sant'Anna et al. (2012); Kelly et al. (2017); Pires et al. (2017).

Fig. 3.

New World field sand flies microbiota. Network analysis showing bacteria genera found in L. intermedia, L. longipalpis, L. evansi, L. cruzi, and N. neivai (syn. L. neivai) obtained exclusively from field collection studies. References used: Oliveira et al. (2000); Gouveia et al. (2008); McCarthy et al. (2011); Sant'Anna et al. (2012); Machado et al. (2014); Monteiro et al. (2016); and Vivero et al. (2016).