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

Abstract

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. Nosema ceranae 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 N. ceranae 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 Gilliamella apicola. In respect to the age of infection, the bees infected just after emergence had elevated loads of G. apicola, Bifidobacterium asteroides, Bombilactobacillus spp., Lactobacillus spp., Bartonella apis, and Bombella apis. Moreover, the G. apicola load was higher in bees infected at nearly all ages, whereas older non-infected bees had higher loads of Bifidobacterium asteroides, Bombilactobacillus spp., Lactobacillus spp., Ba. apis, and Bo apis. These findings suggest that N. ceranae infection and, in particular, the age of bees at infection modulate the gut bacterial community, with G. apicola being the most severely affected species.

Bee-Associated Beneficial Microbes—Importance for Bees and for Humans

“…Although there are short-term shifts in the microbial taxa present in A. mellifera , it has been described that the adult honeybee’s microbiota is dominated (up to 99.9%) by 9–10 bee-associated bacterial clusters, each representing a complex of related strains that are transmitted through social interactions between individuals, with five species’ clusters forming the main core of the bee gut community, albeit with different relative abundances differing among studies [ 19 , 20 , 21 , 22 ]. Principle reported ubiquitous Gram-negative species were Snodgrassella alvi (phylum Pseudomonadota) and Gilliamella apicola (phylum Proteobacteria), while ubiquitous and abundant Gram-positive species were represented by two species clusters, namely, Lactobacillus mellifer / mellis clade (formerly Firm-4 clade) and Lactobacillus melliventris clade (formerly Firm-5 clade), both from Firmicutes phylum, with Bifidobacterium asteroides -related species cluster (phylum Actinobacteria) also being present in most adult bees [ 20 , 22 , 23 , 24 , 25 ]. Additional phylotypes that are less consistent across colonies (non-core) and are not necessarily present in every individual include the Frischella , Bartonella , Commensalibacter , Bombella , Fructobacillus and Apibacter species [ 6 , 22 , 23 , 26 , 27 ].…”