New insights into host-microbe interactions have drawn unprecedented attention to the microbial world in animals, both invertebrates and vertebrates. Gut microbiota plays an essential role in brain physiology and behaviors. Due to the difficulty of maintaining gnotobiotic animals, it is challenging to elucidate the contribution of individual gut members.
Honey bees provide a simple model to understand the relationship between gut bacteria and social brains. Honey bees live in colonies and exhibit complex social, navigational, and communication behaviors and a relatively rich cognitive repertoire. Honey bees, like humans, are eusocial animals with a specialized gut microbiota developed over millions of years of coevolution. The honeybee has been used to model learning and memory formation, highlighting its utility for neuroscience research, in particular for understanding the basis of cognition.
Pioneering research has identified influences of the gut microbiota on behaviors. Zheng et al. found that gut microbiota is essential for the gustatory response. Vernier et al. showed that nestmate recognition cues are defined by gut bacteria, possibly via modulation of host metabolism or by the direct generation of colony-specific blends of cuticular hydrocarbons.
To find out how gut microbiota modulates honey bee behaviors, Zhang et al. used antibiotics to perturb the gut microbiota of bees under field conditions. Hive phenotypes, including the numbers of developing larva and capped brood cells, were disturbed. The relative abundances of the four species of Lactobacillus Firm5 were most strongly affected by antibiotic exposure. These results suggest that gut microbiota may influence honey bee hive behaviors. The ability to discriminate and remember odors is critical for honeybee social behaviors. Using gnotobiotic bees reared in the lab, it showed that conventional gut microbiota is required for olfactory learning and memory abilities. RNA-seq revealed that many major royal jelly protein genes essential for learning abilities were upregulated, suggesting that gut bacteria regulate brain gene expression and promote bee learning and memory. One way gut microbiota could impact the host brain is through microbial metabolites implicated in regulating the “gut-brain axis”. Interestingly, metabolomic analyses of both hemolymph and gut samples show that the microbiota mainly regulates the tryptophan metabolism of honey bees. Bee-specific Lactobacillus strains promote memory behavior by transforming tryptophan into indole derivatives that activate the host aryl hydrocarbon receptor.
The study by Zhang et al. highlights the contributions of specific gut members to honeybee neurological processes, thus providing a promising model to investigate mechanisms of microbiota-gut-brain communication.
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