King'ori, C. N. | Search bioRxiv

bioRxiv2025

Changes in the Anopheles arabiensis transcriptome and gut microbiota profiles associated with Microsporidia MB

Microsporidia MB is an endosymbiotic microbe found in Anopheles mosquito populations. This symbiont can block Plasmodium transmission in mosquitoes, and it can spread through mosquito populations and be sustained over generations by vertical and horizontal transmission. These characteristics make Microsporidia MB a potential candidate for symbiont-based malaria vector control. However, the mechanistic basis of interactions between Microsporidia MB and Anopheles arabiensis is poorly characterized. We investigated how the presence of Microsporidia MB affects transcriptomics profiles and the gut microbiota composition and diversity in non-blood-fed and blood-fed (24, 48 and 72 hours post blood meal) An. arabiensis mosquitoes. We observed that mosquito infection with Microsporidia MB upregulated farnesoic acid O-methyltransferase, a gene linked to juvenile hormone biosynthesis in the non-blood-fed mosquitoes. In addition, blood feeding in Microsporidia MB positive mosquitoes was associated with an activation of immune-related genes 24 hours after a blood meal, where several genes including the lipopolysaccharide tumor necrosis factor gene were upregulated. Interestingly, we also observed that Microsporidia MB positivity was associated with a microbiota shift to favor the proliferation of microbes including Pseudomonas and Serratia 24 hours post blood meal. There were indications of immune system activation in Microsporidia MB positive mosquitoes up to 48 hours after a blood meal where factors such as the peptidoglycan recognition SC2-like and lysozyme c-1 were upregulated. Notably, an upregulated immune system at this time point was associated with downregulation of genes associated with metabolism and the restoration of Serratia, Pseudomonas and other key microbes to relative abundances similar to those recorded in non-blood-fed mosquitoes. At the 72-hour time point, Microsporidia MB positive mosquitoes exhibited a downregulation of genes associated with immunity, including cecropins and defensins, while metabolic processes were predominantly upregulated. Our results provide insights into the effect of Microsporidia MB infection on the An. arabiensis gene expression and gut microbiota profiles. This work will contribute to mechanistic insights into symbiont-mediated malaria transmission blocking.

systems biology↗

bioRxiv2024

Temperature modulates the dissemination potential of Microsporidia MB, a malaria-blocking endosymbiont of Anopheles mosquitoes

The endosymbiont Microsporidia MB is a promising malaria control strategy that inhibits the development of Plasmodium naturally in Anopheles mosquitoes. To be successful, it would be necessary to significantly increase the prevalence of Microsporidia MB in populations of malaria mosquitoes to decrease the malaria transmission potential of the mosquito population. However, very little is known about the role of temperature in driving the prevalence of Microsporidia MB infections in mosquito populations. By rearing mosquito larvae under four air temperature regimes (22{degrees}C, 27{degrees}C, 32{degrees}C and 37{degrees}C), we show that warm temperatures favour the growth of Microsporidia MB infected larvae. In addition, Microsporidia MB infected larvae developed faster compared to the uninfected offspring of the same mothers. Starting with 10 Microsporidia MB infected mothers, our population growth model showed that, at 32{degrees}C, it would take 15-35 days to reach a population of 1000 Microsporidia MB infected mothers; this represents a dissemination potential of 4.7, 1.3 and 1.7 times higher compared to 22{degrees}C, 27{degrees}C and 37{degrees}C, respectively. Despite a relatively high mosquito mortality rate (20% more compared to 27{degrees}C), 32{degrees}C was estimated the best temperature for rearing Microsporidia MB infected larvae due to the shorter development time and high infection rate. This study gives insight into the favourable conditions for Microsporidia MB mass rearing and potential release strategies in malarious regions. ImportanceMalaria parasites transmitted by Anopheles mosquitoes cause a life-threatening disease, imposing a massive toll on human health and economic sustainability in sub-Saharan Africa. Relying only on insecticide- and drug-based control products whose efficacy has been eroded by resistance to control malaria is not sufficient anymore. New innovative approaches are urgently needed and Microsporidia MB, a naturally occurring symbiont across Africa is capable of inhibiting Plasmodium transmission in Anopheles gambiae s.l.. Its success in adverting a rebound of malaria cases will depend on the infection dynamic of the symbiont over time and space. Through experimental studies on field derived mosquitoes and mathematical modelling, we demonstrate that Microsporidia MB dissemination potential increase with temperature within a viable range for Anopheles mosquitoes, due to trade-offs between mosquito development and survival and the symbiont growth. Future studies should now investigate how fluctuating temperatures modulate the Plasmodium transmission blocking performance in nature.

microbiology↗