New evidence showing that the destruction of gut bacteria by antibiotic treatment could increase the honey bee’s vulnerability to Nosema infection

Abstract

It has become increasingly clear that gut bacteria play vital roles in the development, nutrition, immunity, and overall fitness of their eukaryotic hosts. We conducted the present study to investigate the effects of gut microbiota disruption on the honey bee’s immune responses to infection by the microsporidian parasite Nosema ceranae. Newly emerged adult workers were collected and divided into four groups: Group I—no treatment; Group II—inoculated with N. 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 bacterial community as there was no significant difference in the density and composition of gut bacteria between Group I and Group II. However, the elimination of gut bacteria by antibiotic (Groups III and IV) negatively impacted the functioning of the honey bees’ immune system as evidenced by the expression of genes encoding antimicrobial peptides abaecin, defensin1, and hymenoptaecin that showed the following ranking: Group I > Group II > Group III > Group IV. In addition, significantly higher Nosema levels were observed in Group IV than in Group II, suggesting that eliminating gut bacteria weakened immune function and made honey bees more susceptible to Nosema infection. Based on Group IV having displayed the highest mortality rate among the four experimental groups indicates that antibiotic treatment in combination with stress, associated with Nosema infection, significantly and negatively impacts honey bee survival. The present study adds new evidence that antibiotic treatment not only leads to the complex problem of antibiotic resistance but can impact honey bee disease resistance. Further studies aimed at specific components of the gut bacterial community will provide new insights into the roles of specific bacteria and possibly new approaches to improving bee health.

The honey bee gut microbiota: strategies for study and characterization

“…The Nosema infection did not significantly alter the composition or quantity of bacteria in the hindgut, probably owing to ‘niche separation’, in which there is minimal interaction between the bacteria of the gut and Nosema spores. In addition to the down‐regulation of the immune system, Li et al () also found that the magnitude of the negative effect of the antibiotics on the health of the bees was greater than that of the Nosema infection; this corroborates findings by Raymann et al () that suggest antibiotic disruption of the bee microbiota is generally harmful. Other studies have found direct antagonism between members of the Ap.…”

“…There is also evidence that antibiotics may selectively deplete some microbial species more than others, leading to shifts in composition (Gilliam, ; Raymann et al ., ). A study by Li et al () found that Ap. mellifera bees whose microbiota had been eliminated by antibiotics were more susceptible to infection by N. ceranae (a common honey bee pathogen), probably owing to negative impacts on the immune system, as illustrated by a reduction in the expression of genes encoding AMPs.…”

“…Ap. mellifera ’s microbial community has been found to be intricately tied to immune stimulation (Li et al ., ), metabolic functioning (Lee et al ., ; Wang et al ., ; Zheng et al ., ; ) and resistance to pathogens (Evans and Armstrong, ; Koch and Schmid‐Hempel, ; Schwarz et al ., ; Li et al ., ; Kwong et al ., ), which has been recently reviewed (Raymann and Moran, ).…”

The impact of yeast presence in nectar on bumble bee behavior and fitness

“…Most studies have been correlational (e.g., Hong‐Li et al. , Bosmans et al. ) and the precise mechanisms of how endosymbionts enhance resistance are still poorly understood.…”

Honey bee trypanosomatid parasite dynamically changes the transcriptome during the infection of honey bee and modifies the host physiology

“…Primers described in previous reports (De Gregoris et al 2011, Powell et al 2014) were used to quantify universal bacteria and phylum-specific Firmicutes . The honey bee β - actin gene was used as a reference (Li et al 2017). The statistical analysis was carried out by unpaired t -test (two-tailed).…”