Changes in the Anopheles arabiensis transcriptome and gut microbiota profiles associated with the endosymbiotic...

Microsporidia MB is an endosymbiotic microbe found in Anopheles mosquito populations. This symbiont can block Plasmodium transmission in mosquitoes, and it can spread through mosquito populations and be sustained over generations by vertical and horizontal transmission. These characteristics make Microsporidia MB a potential candidate for symbiont-based malaria vector control. However, the mechanistic basis of interactions between Microsporidia MB and Anopheles arabiensis is poorly characterized. We investigated how the presence of Microsporidia MB affects transcriptomics profiles and the gut microbiota composition and diversity in non-blood-fed and blood-fed (24-, 48- and 72-hours post blood meal) An. arabiensis mosquitoes.

We observed that mosquito infection with Microsporidia MB upregulated farnesoic acid O-methyltransferase, a gene linked to juvenile hormone biosynthesis in the non-blood-fed mosquitoes. In addition, blood feeding in Microsporidia MB positive mosquitoes was associated with an activation of immune-related genes 24 h after a blood meal, where several genes including the lipopolysaccharide tumor necrosis factor gene were upregulated. Interestingly, we also observed that Microsporidia MB positivity was associated with a microbiota shift to favor the proliferation of microbes including Pseudomonas and Serratia 24 h post blood meal. There were indications of immune system activation in Microsporidia MB positive mosquitoes up to 48 h after a blood meal where factors such as the peptidoglycan recognition SC2-like and lysozyme c-1 were upregulated. Notably, an upregulated immune system at this time point was associated with downregulation of genes associated with metabolism and the restoration of Serratia, Pseudomonas and other key microbes to relative abundances similar to those recorded in non-blood-fed mosquitoes. At the 72-hour time point, Microsporidia MB positive mosquitoes exhibited a downregulation of genes associated with immunity, including cecropins and defensins, while metabolic processes were predominantly upregulated.

Our results provide insights into the effect of Microsporidia MB infection on the An. arabiensis gene expression and gut microbiota profiles. This work will contribute to mechanistic insights into symbiont-mediated malaria transmission blocking.