Localisation and tissue tropism of the symbiont Microsporidia MB in the germ line and somatic tissues of Anopheles arabiensis

Abstract

AbstractTheAnophelessymbiont,Microsporidia MB, is maternally inherited and has a strong malaria transmission-blocking phenotype inAnopheles arabiensis. Microsporidia MBis also vertically transmitted, sexually transmitted and avirulent. These characteristics are expected to promote its spread through mosquito populations, enhancing the potential ofMicrosporidia MBas a candidate for the development of a symbiont-mediated malaria transmission blocking strategy. We found that the patterns ofMicrosporidia MBlocalisation over the development ofAn. arabiensisindicate accumulation in tissues linked to its transmission, specifically the male and female gonadal tissues. Transovarial vertical transmission ofMicrosporidia MBoccurs in the femaleAn. arabiensisovary whenMicrosporidia MBbecomes localised to the cytoplasm of the developing oocyte. In maleAn. arabiensis, Microsporidia MBis localised in the testis and vas deferens. Notably, a high intensity ofMicrosporidia MBcan also be observed in theAn. arabiensisadult but not larval gut. The levels ofMicrosporidia MBfound in the female ovary are linked to the progression of oogenesis, increasing after blood feeding initiates the development of eggs. The levels ofMicrosporiodia MBin the male and female gonadal and gut tissue do not increase as mosquitoes age. Altogether, the high specificity ofMicrosporidia MBtissue localisation patterns and changes in infection prevalence and intensity suggest adaptation to maximise transmission and avirulence inAnopheles arabiensis.ImportanceMicrosporidia MBis a symbiont with strong malaria transmission-blocking phenotype inAnopheles arabiensis. It spreads in mosquito populations through mother-to-offspring and sexual transmission. The ability ofMicrosporidia MBto blockPlasmodiumtransmission together with its ability to spread withinAnophelespopulations and its avirulence to the host makes it a very attractive candidate for developing a key strategy to stop malaria transmissions. Here, we report the basis ofMicrosporidia MBtransmission. We find thatMicrosporidia MBaccumulates inAnopheles arabiensistissues linked to its sexual and vertical transmission. Its prevalence and intensity in the tissues over the mosquito life cycle suggest adaptation to maximise transmission and avirulence inAnopheles arabiensis. These findings provide the foundation for understanding the factors that affectMicrosporidia MBtransmission efficiency. This will contribute to the establishment of strategies to maximizeMicrosporidia MBtransmission forAnophelesmosquito population replacement and malaria transmission blocking.