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

Abstract

The Anopheles symbiont, Microsporidia MB, is maternally inherited and has a strong malaria transmission-blocking phenotype in Anopheles arabiensis. Microsporidia MB is also vertically transmitted, sexually transmitted and avirulent. These characteristics are expected to promote its spread through mosquito populations, enhancing the potential of Microsporidia MB as a candidate for the development of a symbiont-mediated malaria transmission blocking strategy. We found that the patterns of Microsporidia MB localisation over the development of An. arabiensis indicate accumulation in tissues linked to its transmission, specifically the male and female gonadal tissues. Transovarial vertical transmission of Microsporidia MB occurs in the female An. arabiensis ovary when Microsporidia MB becomes localised to the cytoplasm of the developing oocyte. In male An. arabiensis, Microsporidia MB is localised in the testis and vas deferens. Notably, a high intensity of Microsporidia MB can also be observed in the An. arabiensis adult but not larval gut. The levels of Microsporidia MB found in the female ovary are linked to the progression of oogenesis, increasing after blood feeding initiates the development of eggs. The levels of Microsporiodia MB in the male and female gonadal and gut tissue do not increase as mosquitoes age. Altogether, the high specificity of Microsporidia MB tissue localisation patterns and changes in infection prevalence and intensity suggest adaptation to maximise transmission and avirulence in Anopheles arabiensis. ImportanceMicrosporidia MB is a symbiont with strong malaria transmission-blocking phenotype in Anopheles arabiensis. It spreads in mosquito populations through mother-to-offspring and sexual transmission. The ability of Microsporidia MB to block Plasmodium transmission together with its ability to spread within Anopheles populations 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 of Microsporidia MB transmission. We find that Microsporidia MB accumulates in Anopheles arabiensis tissues 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 in Anopheles arabiensis. These findings provide the foundation for understanding the factors that affect Microsporidia MB transmission efficiency. This will contribute to the establishment of strategies to maximize Microsporidia MB transmission for Anopheles mosquito population replacement and malaria transmission blocking.