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

Abstract

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 localization 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 localized to the cytoplasm of the developing oocyte. In male An. arabiensis , Microsporidia MB is localized 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. There was a significant change in Microsporidia MB levels in female and male An. arabiensis gonads, where intensity tended to decrease as mosquitoes aged. However, the intensities did not significantly change in the male or female guts. Altogether, the high specificity of Microsporidia MB tissue localization patterns and changes in infection prevalence and intensity suggest adaptation to maximize transmission and avirulence in Anopheles arabiensis . IMPORTANCE Microsporidia MB is a symbiont with a 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 tissue tropism and localization patterns of Microsporidia MB , which are relevant to its 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 maximize transmission and avirulence in Anopheles arabiensis . These findings provide the foundation for understanding the factors that may affect Microsporidia MB transmission efficiency. This will contribute to the development of strategies to maximize Microsporidia MB transmission to establish and sustain a high prevalence of the symbiont in Anopheles mosquito populations for malaria transmission blocking.