The role of skin microbiota in the attractiveness of humans to the malaria mosquito Anopheles gambiae Giles

N.O. Verhulst

Research output: Thesisinternal PhD, WU

Abstract

Malaria is one of the most serious infectious diseases in the world. The African mosquito Anopheles gambiae sensu stricto (henceforth termed An. gambiae) is highly competent for malaria parasites and preferably feeds on humans inside houses, which make it one of the most effective vectors of the disease. Human body odours are presumably the most important cues that enable An. gambiae to find its host. Knowledge on the odours that mediate the host-seeking behaviour of malaria vectors is expected to contribute to novel intervention methods for disease control.
The skin microbiota plays an important role in the production of human body odours and the human microbial and chemical signature displays a qualitative and quantitative correlation. Several studies have indicated a possible role of skin bacteria in the production of volatiles attractive to mosquitoes. The principle goal of this thesis was to understand the role of the human skin microbiota in mosquito-host interactions and to identify which compounds produced by these micro-organisms are involved in the attraction of An. gambiae to humans.
Skin bacteria isolated from human feet and grown in vitro on agar plates attracted An. gambiae and this attraction was affected by incubation time and dilution of the skin microbiota. Semi-field experiments showed similar results and field experiments in Kenya suggested that skin bacterial volatiles also attract other disease vectors. Volatiles produced by five bacterial species common on the human skin showed that volatile blends produced by some species, including Staphylococcus epidermidis, were more attractive than blends produced by other species. Volatiles produced by Pseudomonas aeruginosa did not affect the behaviour of An. gambiae.
Analysis of the volatiles produced by human skin microbiota grown in vitro led to the identification of 16 compounds, the majority of which had an effect on An. gambiae behaviour. 3-Methyl-1-butanol enhanced the attractiveness of a synthetic blend by a factor of three, and could be used to increase mosquito trap catches for monitoring or vector control purposes. 2-Phenylethanol decreased mosquito catches of a synthetic blend and may act as a spatial repellent.
In order to examine the interaction between the microbiota on the skin and human attractiveness to mosquitoes, skin emanation and skin microbiota samples were taken from 48 individuals. The skin emanations from the individuals varied significantly in attractiveness to An. gambiae and several compounds originating from the skin were associated with individuals that were highly attractive or less attractive to mosquitoes. Individuals with a higher abundance of bacteria on their skin were more attractive to An. gambiae, whereas individuals with a higher diversity of skin microbiota were less attractive. Staphylococcus spp. were associated with individuals that were highly attractive and Pseudomonas spp. with individuals that were less attractive to mosquitoes. Human Leukocyte Antigens (HLA) genes are considered to influence the human body odour profile and HLA profile analysis of the 48 human individuals indicated that these genes may also affect the attractiveness of humans to mosquitoes.
The studies described in this thesis show that volatiles produced by the human skin microbiota play an important role in the host-seeking behaviour of An. gambiae and the abundance and composition of the skin microbiota determine an individual’s attractiveness to mosquitoes. Optimised blends of the compounds identified can be used in push-pull strategies for the manipulation of mosquitoes, thereby reducing the number of malaria mosquitoes, the human-biting frequency, and the intensity of Plasmodium transmission. Research on the role of skin microbiota in the host-seeking behaviour and host preference of biting insects may lead to a better understanding of vector-host interactions and contribute to the fight against vector-borne diseases.

Original languageEnglish
QualificationDoctor of Philosophy
Awarding Institution
  • Wageningen University
Supervisors/Advisors
  • Takken, Willem, Promotor
  • Dicke, Marcel, Promotor
Award date9 Dec 2010
Place of PublicationS.l.
Print ISBNs9789085858300
Publication statusPublished - 2010

Keywords

  • anopheles gambiae
  • man
  • odours
  • bacteria
  • attractants
  • host-seeking behaviour
  • volatile compounds
  • in vitro
  • in vivo experimentation

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