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Thank you for visiting nature. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser or turn off compatibility mode in Internet Explorer.

In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript. Honeybees are highly social insects with a rich behavioral repertoire and are a versatile model for neurobiological research. Their gut microbiota comprises a limited number of host-restricted bacterial phylotypes that are important for honeybee health.

However, it remains unclear how specific gut members affect honeybee behaviors. Here, we find that antibiotic exposure disturbs the gut community and influences honeybee phenotypes under field conditions. Using laboratory-generated gnotobiotic bees, we show that a normal gut microbiota is required for olfactory learning and memory abilities. Brain transcriptomic profiling reveals distinct brain gene expression patterns between microbiota-free and conventional bees. Subsequent metabolomic analyses of both hemolymph and gut samples show that the microbiota mainly regulates tryptophan metabolism.

Our results indicate that host-specific Lactobacillus strains promote memory behavior by transforming tryptophan to indole derivatives that activate the host aryl hydrocarbon receptor. Our findings highlight the contributions of specific gut members to honeybee neurological processes, thus providing a promising model to understand host-microbe interactions.

The gut microbiota plays a significant role in modulating host development and physiology, including metabolism and immune functions. Recent studies have shown the effects of symbiotic microbes on the central nervous system CNS and behavioral processes in humans and several animal systems.

Microbes can impact the host brain through various pathways, such as immune modulation, and via microbial metabolites implicated in regulating the gut-brain axis 1. Although it is unclear whether the neurotransmitters produced by certain gut bacteria e.

For example, various short-chain fatty acids derived from microbial fermentation were suggested to regulate the rate-limiting enzymes involved in neurotransmitter biosynthesis 2.

Specifically, it has been documented that the gut microbiota modulates tryptophan Trp metabolism and that the produced serotonin, kynurenine Kyn , and indolic compounds profoundly affect gut-brain interactions 3. Although the functional connection between the microbiota and neurophysiology has been widely recognized, most recent studies have focused on mammalian and nonsocial-insect models. It is challenging to elucidate the contribution of individual gut members in mammals, which is partly due to the complex and unpredictable compositions of the gut community and the difficulty of maintaining and manipulating gnotobiotic animals 4.

Thus, models exhibiting high sociality and a specialized gut community would be ideal to fully understand the relationship between the gut microbiota and host social behaviors. The honeybee Apis mellifera is an important agricultural pollinator for wild plants and crops, and studies have focused on bee health to prevent colony losses.

In addition, the honeybee is a eusocial insect with distinct behavioral structures characterized by a complex range of interactive behaviors. It has been widely used as a model of perception, cognition, and social behaviors 5.

Most bacterial genera include closely related species with high strain-level diversity. Typically, two genera of lactic acid bacteria, Lactobacillus Firm5 and Firm4 Bombilactobacillus 7 , are the most abundant, followed by Gilliamella , Snodgrassella , and Bifidobacterium.

Bee gut bacteria inhabit diverse nutritional niches, play specific roles in the bee gut, and are beneficial for host nutrition, immune homeostasis, and pathogen resistance 8. Although the impact of the gut community on honeybee health is relatively clear, few studies have searched for potential links between the gut microbiota and honeybee behaviors.

Recent studies showed that gnotobiotic honeybees with a conventional CV gut microbiota had higher sugar sensitivity than microbiota-free MF bees 9. Monocolonization with Bifidobacterium asteroides , the key polysaccharide degrader in the bee gut, elevates the concentration of juvenile hormone III derivatives in the gut, which may regulate host development These findings strongly suggest that the honeybee gut microbiota may contribute to host brain physiology and behavioral phenotypes.

A recent study showed that oral supplementation with bee gut Lactobacillus increased the level of glycerophospholipids in the hemolymph and promoted the memory of bumblebees However, the contributions of particular gut members to honeybee behaviors via the regulation of metabolism remain unclear.

Herein, we investigated the role of the gut microbiota in altering honeybee behavioral phenotypes in the field.

Our experiments showed that a conventional gut microbiota was needed for learning and memory abilities. Metabolic analyses of both gut and hemolymph samples suggested the effect of gut symbionts on host Trp metabolism.

By generating monocolonized bees with symbiont isolates, we confirmed that bee gut Lactobacillus strains with aromatic amino acid aminotransferase ArAT convert Trp to an indolic aryl hydrocarbon receptor AhR agonist and improve learning and memory behaviors in an AhR-dependent manner.

First, we explored whether perturbation of the gut microbiota disturbs honeybee phenotypes under field conditions. To generate a single-cohort colony, we labeled newly emerged bees with color tags and placed them in empty hives with laying queens. One week after establishment of the hives, three hives were treated with tetracycline in wild honey, and the other three hives control group were fed wild honey on the same treatment schedule Fig.

We counted the number of capped brood cells and assessed the posttreatment survival of adult bees by counting the number of remaining marked bees.

Typically, honeybee eggs hatch into larvae within 3—4 days, and the larval stage lasts for 6 days. We started to check the status of pupation 12 days after egg laying Day 15; Fig.

Although there were an increasing number of capped brood cells in the control hives, no single capped brood was observed in the treatment group on Days 17, 18, and 19 Fig. The number of recovered adult bees was not significantly different between the control and treatment groups either before Day 6 or after Day 13 and 19 antibiotic treatment Fig. Developing eggs and larvae were present in the brood cells in control hives Fig.

However, only a few eggs were observed in the treatment group, and none of these hatched even after 19 days. Moreover, the rectums of bees from the control groups were full of yellow pollen, while those of treated bees were more translucent. This suggested a lack of pollen in the gut of treated bees, which could be evidence of bee malnutrition. Altogether, these results indicated that antibiotic-treated bees were less capable of rearing broods, while survivorship was not affected by tetracycline exposure during the experiment.

Age-controlled bees were treated with tetracycline for 5 days Days 7—11 in the hive and recovered for 7 days Days 11— Differences between antibiotic-treated bees and the control group were tested by multiple two-tailed t -test with Benjamini-Hochberg correction in b and c. Differences between control and antibiotic-treated groups were tested by two-sided Mann-Whitney u test.

Error bars represent min and max. Source data are provided as a Source Data file. We further characterized the composition of the gut community at both the genus and species levels through metagenomic sequencing. Although the gut community composition displayed no significant difference at pretreatment sampling points, significant changes were observed after antibiotic exposure Day 11; Fig. After recovery for 7 days Day 19 , the gut compositions were even more divergent.

The treatment group had a higher fraction of Gilliamella , while the relative abundance of Bifidobacterium was reduced. Moreover, tetracycline treatment affected the genus- and species-level compositions of all core gut members Fig. Specifically, the relative abundances of the four species of Lactobacillus Firm5 were most strongly affected by antibiotic exposure. The relative abundances of Lactobacillus apis , Lactobacillus helsingborgensis , and Lactobacillus melliventris were reduced in the antibiotic treatment group, while that of Lactobacillus kullabergensis was increased Fig.

The ability to discriminate and remember odors is critical for honeybee social behaviors, such as labor division, feeding organization, kin recognition, and mating Since we observed altered hive phenotypes under field conditions, we then examined whether gut microbiota colonization affects the olfactory learning and memory abilities of bees in the laboratory.

Although the honeybees learned the nonanol odor, the efficiency differed among groups, and the learning rate was higher for the CV bees Supplementary Fig. This percentage is similar to that for hive bees performing an olfactory learning task in a previous test In contrast, the proportion of individuals that remembered the odor was significantly lower in the antibiotic treatment group.

Surprisingly, no MF bee exhibited successful memory behavior, suggesting that the gut microbiota can affect honeybee learning and memory abilities. Bees responded to only the nonanol odor were considered successful.

In-depth proteomic profiling of the brains of honeybees from the MF and CV groups identified a total of 3, proteins, 2, of which were detected in both the MF and CV groups Supplementary Fig.

Notably, the muscarinic acetylcholine receptor mAChR involved in the cholinergic neurotransmitter system that processes olfactory signals 16 was upregulated in the CV bees Supplementary Fig. A splicing factor, U2af28, was upregulated in CV brains, implying altered splicing of genes in the brain. Since the olfactory learning and memory behaviors of honeybees are primarily associated with the gene expression profile in the brain 17 , we explored the changes in the transcriptome induced by the gut microbiota.

We found that the odorant-binding protein Obp14 and olfactory receptor Or , which are essential for the detection and identification of specific odors 18 , 19 , were upregulated in the CV group Fig. Three major royal jelly protein MRJP family genes mrjp 1 , mrjp 2 , mrjp 7 and the hexamerin HEX70a involved in bee caste determination 20 , 21 were also upregulated. Enrichment analysis of the differentially expressed genes showed that KEGG pathways, including the linoleic, alpha-linolenic, arachidonic acid, and glycerophospholipid metabolic pathways, were upregulated in the brains of microbiota-colonized bees Fig.

To determine the key metabolites regulated by gut symbionts potentially impacting the circulatory system 2 , we performed quasi-targeted metabolomic analysis of honeybee hemolymph samples. In total, metabolites were identified in the MF and CV bees Supplementary Data 4 , and the metabolic signatures of the hemolymph samples were significantly different between the two groups Fig. Interestingly, KEGG pathway enrichment analysis highlighted that metabolites involved in amino acid metabolic pathways, such as tryptophan, serine, and valine metabolism, were regulated by the gut microbiota.

Notably, the tryptophan metabolism pathway was either up- or downregulated by gut microbes. Thus, we wished to identify the metabolites belonging to this pathway that were altered. A volcano plot showed that the levels of both tryptophan and indoleacrylic acid IA were elevated in the CV bee hemolymph, while the level of Kyn was increased, when the gut microbiota was depleted Fig.

Genes encoded by the host are shown in blue. Genes encoded by the gut bacteria are shown in red. Indole derivatives acting as AhR ligands are shown in orange. Group differences were tested by two-sided Mann-Whitney u test. Dietary Trp can be catabolized by gut bacteria into a variety of indole derivatives, such as IA and indoleacetic acid IAA , which are key components for intestinal homeostasis 22 Fig.

Alternatively, Trp is metabolized through the Kyn pathway mediated by host enzymes, which leads to the production of Kyn and kynurenic acid KA. These results indicated that the gut microbiota suppressed Trp metabolism through the Kyn pathway, which has been widely associated with neurodegenerative diseases It has been documented that the gut microbiota mostly affects amino acid metabolism pathways in the gut. We revisited our metabolomic data obtained from different gut compartments of the CV and MF bees 9.

Although IA was not detected with our previous metabolomic approach, the levels of both Trp and IAA were increased in the ileum and rectum Fig. Interestingly, none of these indices were altered between the CV and MF bees within the midgut, which is colonized by few microbes.

Similarly, antibiotic treatment under field conditions inhibited the microbial indole pathway and shifted Trp metabolism toward the production of Kyn in the gut Supplementary Fig. Altogether, these results indicated that the honeybee gut microbiota mostly influenced Trp metabolism by transforming Trp to indole derivatives and limiting the host Kyn pathway.

Indole derivatives are generated via the indole pathway by many human intestinal anaerobic bacteria, which encode functional ArATs Fig. ArAT is a key enzyme that is conserved in many bacterial species, but not all of these species can convert Trp to aroma compounds Interestingly, we found that only strains of Lactobacillus Firm5 and Bombilactobacillus and one strain of Bombiscardovia coagulans family Bifidobacteriaceae had ArAT subfamily I genes