Temperature modulates the dissemination potential of Microsporidia MB, a malaria-blocking endosymbiont of Anopheles mosquitoes
Otieno, F. G.; Barreaux, P.; Belvinos, A. S.; Makhulu, E. E.; Onchuru, T. O.; Wairimu, A. W.; Omboye, S. M.; King'ori, C. N.; Mawuko, S. B.; Kebira, A. N.; Herren, J. K.
10.1101/2024.11.15.623820 bioRxivShow abstract
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.
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