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

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. Graphical Abstract

ThePlasmodiumtransmission-blocking symbiont,Microsporidia MB, is vertically transmitted throughAnopheles arabiensisgermline stem cells

“…As demonstrated in other insect-symbiont associations (39–41), the presence of Microsporidia MB may elicit A. arabiensis’ immune response which then directly interferes with the establishment of the symbiont before it colonizes the primary sites of infection where it may be protected from the host immune responses. Also, environmental factors such as temperature and humidity that are known to influence the occurrence and transmission of different endosymbionts including microsporidian symbionts in different insects are likely to affect the establishment of Microsporidia MB (42–44).…”