Abstract

BackgroundHost-seeking of the African malaria mosquito, Anopheles gambiae sensu stricto, is guided by human odours. The precise nature of the odours, and the composition of attractive blends of volatiles, remains largely unknown. Skin microbiota plays an important role in the production of human body odours. It is hypothesized that host attractiveness and selection of An. gambiae is affected by the species composition, density, and metabolic activity of the skin microbiota. A study is presented in which the production and constituency of volatile organic compounds (VOCs) by human skin microbiota is examined and the behavioural responses of An. gambiae to VOCs from skin microbiota are investigated.MethodsBlood agar plates incubated with skin microbiota from human feet or with a reference strain of Staphylococcus epidermidis were tested for their attractiveness to An. gambiae in olfactometer bioassays and indoor trapping experiments. Entrained air collected from blood agar plates incubated with natural skin microbiota or with S. epidermidis were analysed using GC-MS. A synthetic blend of the compounds identified was tested for its attractiveness to An. gambiae. Behavioural data were analysed by a χ2-test and GLM. GC-MS results were analysed by fitting an exponential regression line to test the effect of the concentration of bacteria.ResultsMore An. gambiae were caught with blood agar plates incubated with skin bacteria than with sterile blood agar plates, with a significant effect of incubation time and dilution of the skin microbiota. When bacteria from the feet of four other volunteers were tested, similar effects were found. Fourteen putative attractants were found in the headspace of the skin bacteria. A synthetic blend of 10 of these was attractive to An. gambiae.ConclusionsThe discovery that volatiles produced by human skin microorganisms in vitro mediate An. gambiae host-seeking behaviour creates new opportunities for the development of odour-baited trapping systems. Additionally, identification of bacterial volatiles provides a new method to develop synthetic blends, attractive to An. gambiae and possibly other anthropophilic disease vectors.

Highlights

  • Host-seeking of the African malaria mosquito, Anopheles gambiae sensu stricto, is guided by human odours

  • The skin microbiota plays an important role in the production of human body odours [5] and without bacteria human sweat is odourless [6]

  • If host-selection by An. gambiae is based on the species composition, metabolic activity and/or density of the skin microbiota, this will bear a direct impact on the number of bites received per person and the resulting risk of infection [1]

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Summary

Introduction

Host-seeking of the African malaria mosquito, Anopheles gambiae sensu stricto, is guided by human odours. Skin microbiota plays an important role in the production of human body odours. It is hypothesized that host attractiveness and selection of An. gambiae is affected by the species composition, density, and metabolic activity of the skin microbiota. Visual and physical cues play a role in the host-seeking behaviour of An. gambiae, host-seeking is mainly accomplished by odour-mediated anemotaxis in which volatile organic compounds (VOCs) of human origin provide essential cues [1]. The skin microbiota plays an important role in the production of human body odours [5] and without bacteria human sweat is odourless [6]. If host-selection by An. gambiae is based on the species composition, metabolic activity and/or density of the skin microbiota, this will bear a direct impact on the number of bites received per person and the resulting risk of infection [1]. The nonrandom nature of host selection remains poorly understood, yet has an important impact on exposure to disease [10]

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