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The honey bee <i>Apis mellifera</i> is exposed to a variety of biotic and abiotic stressors, such as the highly prevalent microsporidian parasite <i>Nosema</i> (<i>Vairimorpha) ceranae</i> and neonicotinoid insecticides. Both can affect honey bee physiology and microbial gut communities, eventually reducing its lifespan. They can also have a combined effect on the insect’s survival. The use of bacterial probiotics has been proposed to improve honey bee health, but their beneficial effect remains an open question. In the present study, western honey bees were experimentally infected with <i>N. ceranae</i> spores, chronically exposed to the neonicotinoid thiamethoxam, and/or supplied daily with the homofermentative bacterium <i>Pediococcus acidilactici</i> MA18/5M thought to improve the honey bees’ tolerance to the parasite. Deep shotgun metagenomic sequencing allowed the response of the gut microbiota to be investigated with a taxonomic resolution at the species level. All treatments induced significant changes in honey bee gut bacterial communities. <i>Nosema ceranae</i> infection increased the abundance of <i>Proteus mirabilis</i>, <i>Frischella perrara</i>, and <i>Gilliamella apicola</i> and reduced the abundance of <i>Bifidobacterium asteroides</i>, <i>Fructobacillus fructosus</i>, and <i>Lactobacillus</i> spp. Supplementation with <i>P. acidilactici</i> overturned some of these alterations, bringing back the abundance of some altered species close to the relative abundance found in the controls. Surprisingly, the exposure to thiamethoxam also restored the relative abundance of some species modulated by <i>N. ceranae</i>. This study shows that stressors and probiotics may have an antagonistic impact on honey bee gut bacterial communities and that <i>P. acidilactici</i> may have a protective effect against the dysbiosis induced by an infection with <i>N. ceranae.</i>