Abstract

BackgroundPhlebotomine sand flies transmit the haemoflagellate Leishmania, the causative agent of human leishmaniasis. The Leishmania promastigotes are confined to the gut lumen and are exposed to the gut microbiota within female sand flies. Here we study the colonisation resistance of yeast and bacteria in preventing the establishment of a Leishmania population in sand flies and the ability of Leishmania to provide colonisation resistance towards the insect bacterial pathogen Serratia marcescens that is also pathogenic towards Leishmania.MethodsWe isolated microorganisms from wild-caught and laboratory-reared female Lutzomyia longipalpis, identified as Pseudozyma sp. Asaia sp. and Ochrobactrum intermedium. We fed the females with a sugar meal containing the microorganisms and then subsequently fed them with a bloodmeal containing Leishmania mexicana and recorded the development of the Leishmania population. Further experiments examined the effect of first colonising the sand fly gut with L. mexicana followed by feeding with, Serratia marcescens, an insect bacterial pathogen. The mortality of the flies due to S. marcescens was recorded in the presence and absence of Leishmania.ResultsThere was a reduction in the number of flies harbouring a Leishmania population that had been pre-fed with Pseudozyma sp. and Asaia sp. or O. intermedium. Experiments in which L. mexicana colonised the sand fly gut prior to being fed an insect bacterial pathogen, Serratia marcescens, showed that the survival of flies with a Leishmania infection was significantly higher compared to flies without Leishmania infection.ConclusionsThe yeast and bacterial colonisation experiments show that the presence of sand fly gut microorganisms reduce the potential for Leishmania to establish within the sand fly vector. Sand flies infected with Leishmania were able to survive an attack by the bacterial pathogen that would have killed the insect and we concluded that Leishmania may benefit its insect host whilst increasing the potential to establish itself in the sand fly vector. We suggest that the increased ability of the sand fly to withstand a bacterial entomopathogen, due to the presence of the Leishmania, may provide an evolutionary pressure for the maintenance of the Leishmania-vector association.Electronic supplementary materialThe online version of this article (doi:10.1186/1756-3305-7-329) contains supplementary material, which is available to authorized users.

Highlights

  • Phlebotomine sand flies transmit the haemoflagellate Leishmania, the causative agent of human leishmaniasis

  • In the first part of our study, we explored the effects of yeast and bacterial colonisation of the female sand fly gut on the subsequent establishment of Leishmania in the gut of the vector

  • Isolated from the gut of female sand flies collected in a region endemic for visceral leishmaniasis and O. intermedium, present in our sand fly colony

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Summary

Introduction

Phlebotomine sand flies transmit the haemoflagellate Leishmania, the causative agent of human leishmaniasis. Female phlebotomine sand flies are the primary vectors for transmission of the medically important haemoflagellate Leishmania between their mammalian hosts [1,2]. The concept of colonisation resistance is well established in vertebrate gut systems [9] This is the ability of the gut microbiota to prevent the development of invasive microorganisms, commonly potential pathogens, by a combination of direct microbial interaction and indirect actions of the mucosal immune system. A role for insect gut bacteria in colonisation resistance towards medically important parasites has been established in other insects [10,11,12,13,14] In these studies, the gut microbiota may reduce transmission of the medically important parasite rather than prevent development of an insect pathogen. The microorganisms used for the investigation were the bacteria Asaia sp., Ochrobactrum intermedium and a yeastlike fungus Pseudozyma sp. from the gut of field-caught or lab-reared Lu. longipalpis

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