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Title: New evidence showing that the destruction of gut bacteria by antibiotic treatment could increase the honeybee's vulnerability to Nosema infection

Author
item LI, JIANGHONG - Fujian Agricultural & Forestry University
item Evans, Jay
item LI, WENFENG - Zhejiang University
item ZHAO, YAZHOU - Chinese Academy Of Agricultural Sciences
item DeGrandi-Hoffman, Gloria
item HUANG, SHAOKANG - Fujian Agricultural & Forestry University
item LI, ZHIGUO - Fujian Agricultural & Forestry University
item Hamilton, Michele
item Chen, Yanping - Judy

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/20/2017
Publication Date: 11/10/2017
Citation: Li, J., Evans, J.D., Li, W., Zhao, Y., Hoffman, G.D., Huang, S., Li, Z., Hamilton, M.C., Chen, Y. 2017. New evidence showing that the destruction of gut bacteria by antibiotic treatment could increase the honeybee's vulnerability to Nosema infection. PLoS One. 12(11):e0187505. https://doi.org/10.1371/journal.pone.0187505.
DOI: https://doi.org/10.1371/journal.pone.0187505

Interpretive Summary: Thousands of different species of bacteria live in the guts of humans and other animals including insects and play an important role in the well-being of their hosts. Antibiotics indiscriminately wipe out both good and bad bacteria, leading to antibiotic resistance and causing other potential health problems. In the present study, we evaluated the effects that gut bacteria depletion from antibiotics have on honey bee immune responses, susceptibility to invasion by pathogens, and life expectancy. Our results showed that the disruption of gut bacteria by antibiotic treatment could cause lowe honeybee Immunity, leaving honeybees more susceptible to Nosema disease infection, and thereby shortening their lifespan. This study highlights the potential harm of using antibiotics in beehives and also calls for more research to develop new disease therapeutic strategies for controlling bee diseases. The results from our study should be of interest to researchers, graduate students, apiary inspectors, and beekeepers worldwide.

Technical Abstract: It has become increasingly clear that gut bacteria play vital roles in the development, nutrition, immunity, and overall fitness of their eukaryotic hosts. There are eight bacterial phylotypes that stably colonize in the gut of honeybees and have been related to various aspects of bee health. We conducted the present study to investigate the effects that disruption of gut bacteria might have on the honeybee's immune responses to infection by the microsporidian parasite Nosema ceranae. Newly emergedadult workers were collected and divided into four groups: Group I - no treatment; Group II - inoculated with Nosema ceranae, Group III - antibiotic treatment, and Group IV - antibiotic treatment after inoculation with N. ceranae. Our study showed that Nosema infection did not cause obvious disruption of the gut bacteria as there was no significant difference in the density and composition of the gut bacteria between Group I and Group II. Further, our study showed that the elimination of gut bacteria by antibiotics (Groups III and IV) could negatively impact the functioning of the honeybees' immune system as evidenced by the fact that the level of expression of genes encoding antimicrobial peptides abaecin, defensin, and hymenoptaecin showed the following ranking: Group I > Group II > Group III > Group IV. Based on the fact that significantly higher Nosema levels of were seen in Group IV than in Group II, we concluded that the antibiotic effects on the composition of gut microbial communities weakened immune function and made honeybees more susceptible to Nosema infection. The highest mortality rate was observed in Group IV clearly indicating that antibiotic treatment in combination with stress associated with Nosema infection significantly and negatively impact the survivorship of honeybees. The present study adds new evidence that antibiotic treatment not only leads to the complex problem of antibiotic resistance but also damages gut microbial communities that help regulate immune function in honeybees. Further studies to gain a better understanding of how specific bacteria species shape the immune system will lead to new approaches in improving bee health.