Influence of Age of Infection on the Gut Microbiota in Worker Honey Bees (Apis mellifera iberiensis) Experimentally Infected with Nosema ceranae

The gut microbiota of honey bees has received increasing interest in the past decades due to its crucial role in their health, and can be disrupted by pathogen infection. <i>Nosema ceranae</i> is an intracellular parasite that affects the epithelial cells of the midgut, altering gut homeostasis and representing a major threat to honey bees. Previous studies indicated that younger worker bees are more susceptible to experimental infection by this parasite, although the impact of infection and of age on the gut bacterial communities remains unclear. To address this, honey bees were experimentally infected with a consistent number of <i>N. ceranae</i> spores at various ages post-emergence (p.e.) and the gut bacteria 7 days post-infection (p.i.) were analysed using real-time quantitative PCR, with the results compared to non-infected controls. Infected bees had a significantly higher proportion and load of <i>Gilliamella apicola</i>. In respect to the age of infection, the bees infected just after emergence had elevated loads of <i>G. apicola</i>, <i>Bifidobacterium asteroides</i>, <i>Bombilactobacillus</i> spp., <i>Lactobacillus</i> spp., <i>Bartonella apis</i>, and <i>Bombella apis</i>. Moreover, the <i>G. apicola</i> load was higher in bees infected at nearly all ages, whereas older non-infected bees had higher loads of <i>Bifidobacterium asteroides</i>, <i>Bombilactobacillus</i> spp., <i>Lactobacillus</i> spp., <i>Ba. apis</i>, and <i>Bo apis</i>. These findings suggest that <i>N. ceranae</i> infection and, in particular, the age of bees at infection modulate the gut bacterial community, with <i>G. apicola</i> being the most severely affected species.