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. 2024 Apr 11;17(1):187.
doi: 10.1186/s13071-024-06254-0.

High temperatures and low humidity promote the occurrence of microsporidians (Microsporidia) in mosquitoes (Culicidae)

Artur Trzebny  1 , Olena Nahimova  2   3 , Miroslawa Dabert  2
Affiliations

High temperatures and low humidity promote the occurrence of microsporidians (Microsporidia) in mosquitoes (Culicidae)

Artur Trzebny et al. Parasit Vectors. .

Abstract

Background: In the context of climate change, a growing concern is that vector-pathogen or host-parasite interactions may be correlated with climatic factors, especially increasing temperatures. In the present study, we used a mosquito-microsporidian model to determine the impact of environmental factors such as temperature, humidity, wind and rainfall on the occurrence rates of opportunistic obligate microparasites (Microsporidia) in hosts from a family that includes important disease vectors (Culicidae).

Methods: In our study, 3000 adult mosquitoes collected from the field over 3 years were analysed. Mosquitoes and microsporidia were identified using PCR and sequencing of the hypervariable V5 region of the small subunit ribosomal RNA gene and a shortened fragment of the cytochrome c oxidase subunit I gene, respectively.

Results: DNA metabarcoding was used to identify nine mosquito species, all of which were hosts of 12 microsporidian species. The prevalence of microsporidian DNA across all mosquito samples was 34.6%. Microsporidian prevalence in mosquitoes was more frequent during warm months (> 19 °C; humidity < 65%), as was the co-occurrence of two or three microsporidian species in a single host individual. During warm months, microsporidian occurrence was noted 1.6-fold more often than during the cold periods. Among the microsporidians found in the mosquitoes, five (representing the genera Enterocytospora, Vairimorpha and Microsporidium) were positively correlated with an increase in temperature, whereas one (Hazardia sp.) was significantly correlated with a decrease in temperature. Threefold more microsporidian co-occurrences were recorded in the warm months than in the cold months.

Conclusions: These results suggest that the susceptibility of mosquitoes to parasite occurrence is primarily determined by environmental conditions, such as, for example, temperatures > 19 °C and humidity not exceeding 62%. Collectively, our data provide a better understanding of the effects of the environment on microsporidian-mosquito interactions.

Keywords: Environmental indicators; Global warming; Metabarcoding; Mosquito vectors; Next-generation sequencing; Parasitic infections.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
The abundance of each mosquito species in the samples used in this study (right axis). Mosquito species are indicated by the legend at the top of the figure. The red line shows the average monthly temperature (left axis). Months are marked as cold (blue) and warm (red). Cold months were defined as temperature < 19 °C and humidity > 65%; warm months were defined as temperature > 19 °C and humidity < 65%
Fig. 2
Fig. 2
Correlation plots between microsporidian DNA-positive mosquitoes and a temperature (°C), b humidity (%), c wind (m/s) and d rainfall (mm). The R value indicates the Pearson’s correlation coefficient statistic, the p value is statistically significant, the shadowed area shows the 95% confidence interval, and the black line is the regression line. The month and year of the data points are indicated according to the legend at the bottom
Fig. 3
Fig. 3
Raincloud plots (i.e. combined violin plots, box plots and dot plots) for the contribution of infected mosquitoes relative to cold or warm months: a for the mosquito pool without dividing into females and males and b separately for females and males, collected in cold (blue) and warm (red) months. The dot plots show the proportion of infected mosquitoes (jittered horizontally). Each dot is the individual proportion of a particular species with a particular sex in a single month. The box plots show the extremes (whisker tails), interquartile range (box boundaries) and median (horizontal line). The violin plots show the probability density of the data. Symbols (asterisks or 'ns') indicate Bonferroni p-value (B) and Holm p-value (H) (B/H). Double asterisks (**) indicate statistical significance at p < 0.01; ns, no statistical significance
Fig. 4
Fig. 4
Occurrence of microsporidian species found in total (All), male and female mosquitoes collected during the cold and warm months. Comparative statistics are presented in Additional file 1: Tables S12 and S13
Fig. 5
Fig. 5
Spearman’s correlation coefficient between the occurrence of microsporidians and environmental factors: a temperature, b humidity, c wind and d rainfall. The thickness of line indicates the correlation coefficient. Solid lines indicate statistical significance at p < 0.05; dashed lines indicate no statistical significance. For correlation values and their statistical significance, see Additional file 1: Table S6. Abbreviations of microsporidian species: A. sa, Amblyospora salinaria; A. st, A. stimuli; A. sp.1, Amblyospora sp.1; A. sp.2, Amblyospora sp.2; En. ar, Enterocytospora artemiae; H. sp., Hazardia sp.; M. sp. BLAT1, Microsporidium sp. BLAT1; M. sp. PL01, Microsporidium sp. PL01; V. ad, Vairimorpha adaliae; V. sp., Vairimorpha sp. CHW–2007a
Fig. 6
Fig. 6
a Raincloud plots for the number of microsporidian co-infections during cold and warm months. The dot plots show all the data (jittered horizontally). The box plots show the extremes (whisker tails), interquartile range (box boundaries) and median (horizontal line). The violin plots show the probability density of the data. Symbols (asterisks or 'ns') indicate Bonferroni p value (B) and Holm p value (H) (B/H). Double asterisks (**) indicate statistical significance at p < 0.01; ns, no statistical significance. b UpSet plot of microsporidian co-infections. The bar plot on the left shows the number of co-infected individuals of each microsporidian species. The dot plot on the right shows the number of unique co-infection combinations; connected dots show a microsporidian co-infection combination. The upper bar plot shows the number of infected mosquitoes for each co-infection combination. Bar colour indicates the number of mosquito individuals in which a particular pattern of co-infection was observed; blue indicates cold months, and red indicates warm months
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