Localization and tissue tropism of the symbiont
Microsporidia MB
in the germ line and somatic tissues of
Anopheles arabiensis
Authors: Makhulu Edward E. , Onchuru Thomas O. , Gichuhi Joseph , Otieno Fidel G. , Wairimu Anne W. , Muthoni Joseph N. , Koekemoer Lizette , Herren Jeremy K. 
Published: December 2023

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.