The Pass-on Effect of Tetracycline-Induced Honey Bee (Apis mellifera) Gut Community Dysbiosis

Abstract

Gut microbial community plays an important role in the regulation of insect health. Antibiotic treatment is powerful to fight bacterial infections, while it also causes collateral damage to gut microbiome, which may have long-lasting consequences for host health. However, current studies on honey bees mainly focus on the impact of direct exposure to antibiotics on individual bees, and little is known about the impact of social transmission of antibiotic-induced gut community disorder in honey bee colonies. In order to provide insight into the potential pass-on effect of antibiotic-induced dysbiosis, we colonized newly emerged germ-free workers with either normal or tetracycline-treated gut community and analyzed the gut bacteria composition. We also treated workers with low dosage of tetracycline to evaluate its impact on honey bee gut microbiota. Our results showed that the tetracycline-treated gut community caused disruption of gut community in their receivers, while the direct exposure to the low dosage of tetracycline had no significant effect. In addition, no significant difference was observed on the mortality rate of A. mellifera workers with different treatments. These results suggest that though the residue of antibiotic treatment may not have direct effect on honey bee gut community, the gut microbiota dysbiosis caused by high dosage of antibiotic treatment has a cascade effect on the gut community of the nestmates in honeybee colonies.

Experimental inheritance of antibiotic acquired dysbiosis affects host phenotypes across generations

“…Antibiotic exposure causes dysbiosis, with effects on host health ( Francino, 2016 ; Neuman et al, 2018 ), the resistome (genes involved in resistance responses), and gut bacterial diversity ( Li et al, 2019 ; Xu et al, 2020 ). We found that short-term dysbiosis could be transferred to subsequent worker bee generations which is in line with previous experiments in honey bees and flies ( Ourry et al, 2020 ; Jia et al, 2022 ). In our experiment, tetracycline disrupted the normally stable bee gut community, which did not recover over subsequent generations even after antibiotic administration was ceased.…”

“…Consistent with the direct action of antibiotics on bacteria, we observed substantial changes in the honey bee gut community after tetracycline exposure. While in previous studies, antibiotics were shown to affect the honey bee microbiome ( Powell et al, 2021 ; Tian et al, 2012 ; Moullan et al, 2015 ; Li et al, 2017 ; Raymann et al, 2017 ; Baffoni et al, 2021 ; Jia et al, 2022 ), it rarely led to the total collapse of bacterial species as we observed in our design. At the end of the first cycle, four bacterial genera disappeared from guts of antibiotic-fed bees ( Figure 5 and Supplementary Figure S9 ).…”

“…Also, honey bees used in the studies may differ genetically, in their surrounding environment and likely in their colony’s chemical exposure histories which can affect the microbial strain composition ( Tian et al, 2012 ; Ellegaard and Engel, 2019 ; Wu et al, 2021 ). Low antibiotic intake (10 ug/mL) after emergence did not show to affect the later establishment of the microbiome in honey bees ( Jia et al, 2022 ). However, we used previously published higher concentrations ( Raymann et al, 2017 ) which were administered immediately after emergence, which could affect the uncolonized gut environment and the overall response of a microbiome.…”

“…In addition, honey bees are important pollinators and are exposed to diverse chemicals in the agricultural landscape as well as by beekeepers. It could be shown that antibiotics have strong effects on the honey bee microbiome ( Powell et al, 2021 ; Tian et al, 2012 ; Moullan et al, 2015 ; Li et al, 2017 ; Raymann et al, 2017 ; Baffoni et al, 2021 ; Jia et al, 2022 ) and that such dysbiosis can even be experimentally transferred between workers ( Jia et al, 2022 ).…”

Antimicrobial Activity from Putative Probiotic Lactic Acid Bacteria for the Biological Control of American and European Foulbrood Diseases

“…Moreover, long-lasting treatments and their common use in prophylaxis, as well as failing to eliminate bacterial spores, may cause or accelerate mechanisms of antibiotic resistance [ 25 , 26 , 27 , 28 ]. Additionally, antibiotics may leave residues in hive products [ 29 , 30 , 31 ] and also cause honey bee gut community dysbiosis [ 32 , 33 , 34 ]. On this matter, a growing number of research studies have revealed the relationship between disease states and variation in the native microbiome of honey bees, suggesting that the integrity of the microbiome correlates with disease susceptibility and, on a more general level, with the health status of honey bees [ 11 , 31 , 35 , 36 , 37 , 38 , 39 ].…”