Plasmodium falciparum gametocyte-induced volatiles enhance attraction of Anopheles mosquitoes in the field

Yared Debebe,Rickard Ignell,Sharon Rose Hill,Habte Tekie,Göran Birgersson

doi:10.1186/s12936-020-03378-3

Yared Debebe, Rickard Ignell + Show 3 more

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https://doi.org/10.1186/s12936-020-03378-3

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Abstract

BackgroundPlasmodium parasites manipulate the interaction between their mosquito and human hosts. Patients infected with gametocytes attract anopheline mosquitoes differentially compared to healthy individuals, an effect associated with an increased release of attractive volatile cues. This odour-driven manipulation is partly mediated by the gametocyte-specific metabolite, (E)-4-hydroxy-3-methyl-but-2-enyl pyrophosphate (HMBPP), which induces increased release of select aldehydes and terpenes from red blood cells and results in the enhanced attraction of host-seeking mosquitoes, which are vectors of malaria. This study investigates the effect of the HMBPP-induced volatiles on the attraction of wild Anopheles mosquitoes to humans under field conditions.MethodsThe efficacy of the HMBPP-induced odour blend to attract Anopheles was evaluated in a 4 × 6 Latin rectangular study design indoors using baited Suna traps. Furthermore, to assess the efficacy of the HMBPP-induced odour blend in (1) augmenting the attractiveness of human odour, and (2) attracting Anopheles mosquitoes in the absence of human odour, a two-choice assay using host decoy traps (HDTs) was used and evaluated using binomial generalized regression.ResultsTraps baited with the HMBPP-induced odour blend attracted and caught both Anopheles arabiensis and Anopheles pharoensis females in a dose-dependent manner in the presence of background human odour, up to 2.5 times that of an unbaited trap. Given a choice between human odour and human odour laden with the HMBPP-induced odour blend, mosquitoes differentially preferred traps augmented with the HMBPP-induced odour blend, which caught twice as many female An. arabiensis. Traps baited with the HMBPP-induced odour blend but lacking the background of human odour were not effective in attracting and catching mosquitoes.ConclusionThe findings of the present study revealed that the HMBPP-induced odour blend, when augmented with human body odour, is attractive to anopheline mosquitoes and could be used as a complementary vector control tool along with existing strategies.

Highlights

Plasmodium parasites manipulate the interaction between their mosquito and human hosts
hydroxy-3-methyl-but-2-enyl pyrophosphate (HMBPP)‐induced volatiles attract Anopheles mosquitoes A total of 2114 Anopheles mosquitoes were captured in odour-baited and control traps, belonging to two species, An. arabiensis and An. pharoensis, over the 24 experimental nights
While the number of An. arabiensis captured per night significantly increased with an increasing release rate of the HMBPP-induced odour blend (GLM; χ2 = 12.89; P = 0.0049), there was no overall effect of release rate on the number of An. pharoensis caught (GLM; χ2 = 6.84; P = 0.077; Fig. 2)

Summary

Introduction

Plasmodium parasites manipulate the interaction between their mosquito and human hosts. Patients infected with gametocytes attract anopheline mosquitoes differentially compared to healthy individuals, an effect associated with an increased release of attractive volatile cues This odour-driven manipulation is partly mediated by the gametocyte-specific metabolite, (E)-4-hydroxy-3-methyl-but-2-enyl pyrophosphate (HMBPP), which induces increased release of select aldehydes and terpenes from red blood cells and results in the enhanced attraction of host-seeking mosquitoes, which are vectors of malaria. Debebe et al Malar J (2020) 19:327 sensu lato [1, 2, 4,5,6] and in South America, Anopheles darlingi [3] This manipulation is most clearly observed in the change in host odour profile of gametocyte-infected patients, resulting in the doubling of the attractiveness of these patients to malaria vectors, compared to uninfected healthy persons [1, 2, 4,5,6,7]. These volatiles were hypothesized to be emitted from gametocyte-infected persons [8], and subsequent studies have recently demonstrated an altered profile of these, and other, volatiles emanating from both the breath and skin of gametocyte-infected children [4,5,6,7]

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