Missing Microbes in Bees: How Systematic Depletion of Key Symbionts Erodes Immunity

Daisley, Brendan A.; Chmiel, John A.; Pitek, Andrew P.; Thompson, Graham; Reid, Gregor

doi:10.1016/j.tim.2020.06.006

Cited by 90 publications

(77 citation statements)

References 97 publications

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“…This evidence cumulatively supports that timely use of probiotics may help in the re-establishment of a healthy microbiota following OTC exposure and concurs with the proposition that immunostimulatory Lactobacillus spp. can 'reset' dysbiotic microbiota phenotypes 58 . Thus, while it has been long known that probiotics can induce an immune response in honey bees 37 , the functionality of probiotics in modulating AMPs with microbiota-shaping properties is only now becoming apparent.…”

Section: Discussionmentioning

confidence: 99%

Lactobacillus spp. attenuate antibiotic-induced immune and microbiota dysregulation in honey bees

et al. 2020

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Widespread antibiotic usage in apiculture contributes substantially to the global dissemination of antimicrobial resistance and has the potential to negatively influence bacterial symbionts of honey bees (Apis mellifera). Here, we show that routine antibiotic administration with oxytetracycline selectively increased tetB (efflux pump resistance gene) abundance in the gut microbiota of adult workers while concurrently depleting several key symbionts known to regulate immune function and nutrient metabolism such as Frischella perrera and Lactobacillus Firm-5 strains. These microbial changes were functionally characterized by decreased capped brood counts (marker of hive nutritional status and productivity) and reduced antimicrobial capacity of adult hemolymph (indicator of immune competence). Importantly, combination therapy with three immunostimulatory Lactobacillus strains could mitigate antibiotic-associated microbiota dysbiosis and immune deficits in adult workers, as well as maximize the intended benefit of oxytetracycline by suppressing larval pathogen loads to near-undetectable levels. We conclude that microbial-based therapeutics may offer a simple but effective solution to reduce honey bee disease burden, environmental xenobiotic exposure, and spread of antimicrobial resistance.

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Section: Discussionmentioning

confidence: 99%

Lactobacillus spp. attenuate antibiotic-induced immune and microbiota dysregulation in honey bees

et al. 2020

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“…Vairimorpha ceranae infection may modulate the host's core bacteria by affecting polysaccharide digestion, in addition to the hypothesized immune modulations [45]. Polysaccharides are digested in the honey bee midgut in varying degrees.…”

Section: Discussionmentioning

confidence: 99%

“…Although niche competition among the core bacteria might explain the decrease of Lactobacillus spp., additional modulations are probably involved. Immune response or other physiological functions modulated by V. ceranae infection may involve the core bacteria, and inhibiting immune responses could bene t some bacteria species, especially S. alvi and G. apicola that are not immune neutral [45].…”

Section: Discussionmentioning

confidence: 99%

Vairimorpha Ceranae Alters Honey Bee Microbiota Composition and Sustain the Survival of Adult Honey Bees

Zhang¹,

Su²,

Wang³

et al. 2020

Preprint

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Background: Vairimorpha (Nosema) ceranae is the most common eukaryotic gut pathogen in honey bees, Apis mellifera. Infection is typically chronic but may result in mortality. Additional factors may be involved in mortality, including the honey bee gut microbiota. Previous studies of V. ceranae and gut microbiota identified positive associations between core bacteria and V. ceranae infection. These possibly synergistic or mutualistic associations are often disregarded because some core bacteria act as probiotic symbionts. Methods: To clarify the effects caused by the positive associations, we added isomaltooligosaccharide (IMO), a prebiotic also found in honey, to alter the interactions between V. ceranae and gut bacteria. Mortality and sugar consumption of the caged bees were monitored. Infection intensities and gut bacteria were examed after 12 days post inoculation, the plateau phase of infection. The gut bacteria were evaluated using both qPCR and 16S rDNA sequencing.Results: We confirmed that V. ceranae infections alone significantly enhance several core bacterial populations, including Bifidobacterium spp., Snodgrassella alvi, and Gilliamella apicola in the honey bee hindgut microbiota. Moreover, the qPCR results suggested that V. ceranae infected bees had significantly higher bacterial microbiota populations. In addition to the enhanced core bacteria, Commensalibacter and Bartonella were significantly increased in the fecal microbiome. Infected bees fed IMO had significantly higher V. ceranae spore counts but lower mortality; however, infected bees fed IMO did not have significant changes in gut bacteria populations compared to those fed only sucrose, but feeding IMO further reduced the fecal microbiome alpha-diversity. Conclusions: The microbiota alterations caused by infection were similar to the microbiota differences found between summer bees and winter bees, the latter of which have longer lifespans, and feeding IMO increased this similarity. Our results indicated that the interactions between gut bacteria and V. ceranae not only enhanced both the pathogen and bacteria populations but also sustained the host survival. This mutualistic interaction potentially enhances disease transmission and avoids social immune responses of the honey bee hosts.

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“…Thus, they are applied to blossoming crops and may subsequently appear in high amounts in larval provisions in bee nests. However, there is a lack of knowledge on the effects of fungicides on the fermentation processes in honeybee pollen and on the gut bacterial microbiome [28][29][30]33]. The herbicide glyphosate was proven to substantially affect the gut microbiome in bees [31,32].…”

Section: Implication For Bee Healthmentioning

confidence: 99%

“…Bees are exposed to pesticides via pollen, nectar and water consumption [17][18][19][20][21], potentially by soil material used for nest construction [22][23][24]. They may encounter acute or chronic toxic effects of pesticides [25][26][27], or indirect impacts through affecting the beneficial bee gut microbiome [28][29][30][31][32][33] and the resistence to pathogens [34][35][36][37] or reduced forage sources in the landscape owing to the use of herbicides [38]. Risk assessment of acute exposure to pesticides used to be generally performed on honeybees [39].…”

Section: Introductionmentioning

confidence: 99%

Domestic Gardens Mitigate Risk of Exposure of Pollinators to Pesticides—An Urban-Rural Case Study Using a Red Mason Bee Species for Biomonitoring

Šlachta

Erban

Votavová³

et al. 2020

Sustainability

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Domestic gardens supply pollinators with valuable habitats, but the risk of exposure to pesticides has been little investigated. Artificial nesting shelters of a red mason bee species (Osmia bicornis) were placed in two suburban gardens and two commercial fruit orchards to determine the contamination of forage sources by pesticides. Larval pollen provisions were collected from a total of 14 nests. They consisted mainly of pollen from oaks (65–100% weight/sample), Brassicaceae (≤34% w/s) and fruit trees (≤1.6% w/s). Overall, 30 pesticides were detected and each sample contained a mixture of 11–21 pesticide residues. The pesticide residues were significantly lower in garden samples than in orchard samples. The difference was attributed mainly to the abundant fungicides pyrimethanil and boscalid, which were sprayed in fruit orchards and were present on average at 1004 ppb and 648 ppb in orchard samples, respectively. The results suggested that pollinators can benefit from domestic gardens by foraging from floral sources less contaminated by pesticides than in adjacent croplands.

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Missing Microbes in Bees: How Systematic Depletion of Key Symbionts Erodes Immunity

Cited by 90 publications

References 97 publications

Lactobacillus spp. attenuate antibiotic-induced immune and microbiota dysregulation in honey bees

Lactobacillus spp. attenuate antibiotic-induced immune and microbiota dysregulation in honey bees

Vairimorpha Ceranae Alters Honey Bee Microbiota Composition and Sustain the Survival of Adult Honey Bees

Domestic Gardens Mitigate Risk of Exposure of Pollinators to Pesticides—An Urban-Rural Case Study Using a Red Mason Bee Species for Biomonitoring

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