Experimental Nosema ceranae infection is associated with microbiome changes in the midguts of four species of Apis (honey bees)

Abstract

Nosema ceranae is a unicellular microsporidian causing ventricular cell lysis in host Apis species. We hypothesized that the gut microbiota of honey bees, A. cerana, A. dorsata, A. florea, and A. mellifera, is disrupted by N. ceranae infection. Correspondingly, we investigated the impact of N. ceranae infection on gut populations of Bifidobacterium sp. and Apilactobacillus kunkeei in the selected Apis species. The bacteria populations were compared using a culture-dependent method and employing 16S rRNA gene sequencing between bees infected with 2.0 × 105 N. ceranae spores and those remaining uninfected. The number of N. ceranae spores per bee and the ratio of infected gut cells to uninfected cells were measured at five and ten days post infection (p.i.). N. ceranae spore load at ten days p.i. was significantly greater than at five days p.i. and was varied with species’ body size. For each of the four Apis species, N. ceranae treated bees had lower survival than did the control bees. Moreover, A. florae had the largest infection ratio of all the species. Across all Apis species, N. ceranae infected individuals had significantly lower mean numbers of Bifidobacterium sp. and A. kunkeei than did uninfected ones. Among infected bees, the average number of both bacteria was significantly greatest in A. dorsata and lowest in A. cerana. Overall, N. ceranae infection was associated with histopathological damage and also with lower populations of Bifidobacterium sp. and A. kunkeei in the midguts of the tested honey bee species.