Composition of human skin microbiota affects attractiveness to malaria mosquitoes

Abstract

The African malaria mosquito Anopheles gambiae sensu stricto continues to play an important role in malaria transmission, which is aggravated by its high degree of anthropophily, making it among the foremost vectors of this disease. In the current study we set out to unravel the strong association between this mosquito species and human beings, as it is determined by odorant cues derived from the human skin. Microbial communities on the skin play key roles in the production of human body odour. We demonstrate that the composition of the skin microbiota affects the degree of attractiveness of human beings to this mosquito species. Bacterial plate counts and 16S rRNA sequencing revealed that individuals that are highly attractive to An. gambiae s.s. have a significantly higher abundance, but lower diversity of bacteria on their skin than individuals that are poorly attractive. Bacterial genera that are correlated with the relative degree of attractiveness to mosquitoes were identified. The discovery of the connection between skin microbial populations and attractiveness to mosquitoes may lead to the development of new mosquito attractants and personalized methods for protection against vectors of malaria and other infectious diseases.

Figure 1. Relative attractiveness to An. gambiae of 48 individuals.

Bars show the attractiveness parameter estimate results from the Generalized Linear Model (GLM) used to investigate the relative attractiveness of each individual to An. gambiae. Individuals were classified as highly attractive (HA, blue bars) when their mean relative attractiveness was significantly higher than the mean relative attractiveness of each individual in the group classified as poorly attractive (PA, red bars) (GLM, p<0.05). Error bars represent the standard error of the mean from six replications.

Figure 2. Skin bacterial abundance and relative attractiveness to An. gambiae.

Correlation between the number of bacteria (log), determined by counts of colony forming units (CFUs) on non-selective plates and the relative attractiveness of the individuals. The relative attractiveness is expressed as the number of mosquitoes caught in the trapping device releasing the odour of the tested individual divided by the total number of mosquitoes trapped in both trapping devices . The red line indicates the fitted relationship according to the Generalized Linear Model (GLM).

Figure 3. Rarefaction curves showing average bacterial diversity from poorly attractive (PA,) and highly attractive (HA) individuals.

P-value for the difference in diversity score between PA (dashed red line) and HA (solid blue line) individuals is given at three sampling depths (not calculated for higher numbers of sequences, because the samples from some individuals did not yield more than 1500 sequences).

Figure 4. Multivariate data analysis of the bacterial profiles of poorly attractive (PA) and highly attractive (HA) individuals.

Partial least squares discriminant analysis (PLS-DA) loading plot based on the relative abundance of bacterial genera in the microbiota profiles of poorly attractive (PA) and highly attractive (HA) individuals. Bacterial genera closer to HA or PA in the plot are more closely correlated to either HA or PA individuals. PLS 1 (R²X = 0.370, R²Y = 0.682, Q² = 0.553) and PLS 2 (R²X = 0.102, R²Y = 0.260, Q² = 0.424) are given. Genera that significantly contribute to the prediction of the model are indicated in blue (HA individuals) and red (PA individuals) (based on 95% confidence intervals, Figure S3). Some sequences could only be identified to division (D), class (C), order (O) or family (F).