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It was recently shown 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 In leaf-cutting ants and termites, gut microbiota suppression by antibiotics also influences the recognition behavior toward nestmates, which may be directed by bacterial metabolites as recognition cues in the feces 43 , Nevertheless, the effect of the gut community is driven mainly by microbial metabolism, specifically the amino acid and lipid metabolic pathways, which can further influence the circulation system of the host 45 , Recently, gut Trp metabolism was found to be associated with neuropsychiatric disorders in humans and a Drosophila model, characterized by reduced plasma levels of Trp 47 and high IDO1 activity We found that the levels of Trp and the indole derivatives were also elevated in the CV bee gut and hemolymph compared to their bacteria-free counterparts.
Trp metabolism in the gut mainly involves the conversion of Trp into indole derivatives by resident bacteria and the production of Kyn mediated by host enzymes The indole pyruvate route is one of the main pathways for indolic compound synthesis.
ArAT is a key enzyme converting Trp to indole derivatives conserved in many bacterial species, including lactobacilli from the human intestine The honeybee gut harbors two major groups of lactobacilli, Bomilactobacillus and Lactobacillus , which are two recently reclassified bacterial genera formerly known as Lactobacillus Firm4 and Firm5, respectively 7.
They are the most abundant gut members prevalent in both honeybees and bumblebees. We found that ArATs were present in the genomes of both Bomilactobacillus and Lactobacillus , and these were closely related to that from L. Lactobacilli rely primarily on the availability of easily fermentable sugars and amino acids. Lactobacillus strains encode genes related to carbohydrate metabolism, suggesting that they are also essential fermenters in the honeybee gut.
However, lactobacilli are also auxotrophic for amino acids and switch from sugar to Trp as a major energy source, catabolizing Trp to indole derivatives under carbohydrate-limiting conditions Indeed, our in vivo test showed that L.
Notably, not all strains of honeybee lactobacilli harbor ArAT genes. Multiple species have been defined within the bee Lactobacillus and Bombilactobacillus groups, and further strain-level variations have been repeatedly reported for honeybee gut species 51 , This suggests that the distinct nutritional adaptations of bee gut species may facilitate niche differentiation, allowing the coexistence of closely related members in the bee gut Multiple indole derivatives have been identified as agonists of AhR, a ligand-activated transcription factor playing important roles in human health In both Caenorhabditis elegans and Drosophila melanogaster , indoles produced by the microbiota extend the host lifespan via AhR and induce a youthful gene expression profile Honeybees also possess a gene LOC encoding AhR, but its functions, such as the xenobiotic tolerance found in other insects 55 , are still not clear.
We found that colonization by L. This indicates that the activation of AhR relies on the indole derivatives generated by gut bacteria. Moreover, L. The role of AhR in the regulation of the immune response has been extensively studied, while its participation in the gut-brain axis remains elusive Experiments using honeybees as a new model with a manipulated microbiota will help us reveal the underlying mechanisms, specifically the potential of AhR as a therapeutic target for human social pathologies It has been shown that gut microorganisms may influence social behaviors across diverse animal hosts Honeybees are colonial and highly social organisms with multiple characteristic behaviors, offering an experimental tool to investigate the relationship between the microbiota and host brain functions and uncover the causal mechanisms underlying sociability.
While our results indicated the critical role of specialized bee gut symbionts in the learning and memory ability implicated in other complex social behaviors 12 , further evaluation of the effect of the microbiota on different behaviors, such as kin recognition and social organization, would assist in fully understanding the mechanisms underlying gut-brain interactions. The development of genetic tools for manipulating both the bee host and gut bacteria would facilitate the investigation of the molecular basis of host-microbe interactions via the gut-brain axis.
Insects: honeybees Apis mellifera used in this study were from colonies maintained in the experimental apiary of the China Agricultural University. There is no current requirement regarding insect care and use in research. Honeybees were cared for daily with adequate food during the experimental period. For tissue collection, bees were collected gently and immediately euthanized by CO 2 anesthesia before dissection to reduce any unnecessary duress. Microbiota-free MF bees were obtained as described by Zheng et al.
Late-stage pupae were removed manually from brood frames and placed in sterile plastic bins. Then MF and CV bees were provided sterilized sucrose 0. Then MF and Firm5 bees were provided sterilized sucrose 0. All bees used here all came from the same colony.
Bees coming from the same cup cage were considered as one replicate of each group. Colonization levels of MF and Firm5 bees were determined by colony-forming units from dissected guts, as described by Kwong et al. The copy number of plasmids was determined by performing standard curves on serial dilutions of plasmids containing the target sequence. Each plate contained a positive control and a water control. Honeybee brains were collected using a dissecting microscope Canon. Individual bee was fixed on beeswax using two insect needles through the thorax.
After removing the head cuticle, the whole brain was placed on a glass slide and soaked in RNAlater Thermo; Waltham, MA, USA or proteinase inhibitor Roche; Mannheim, Germany for gene expression profiling, proteome analysis, and neurotransmitters concentration quantification. Then hypopharyngeal glands, salivary glands, three simple eyes, and two compound eyes were carefully removed.
MF, CV, and Firm5 bees were generated as described above. Experiments of olfactory learning and memory were performed as previously described 13 , 14 with modifications Fig. Then, they were mounted to a modified 0. The whole experiment was performed in a room with a stable light source at room temperature. Bees that do not show PER to sucrose were removed for further experiments. The odor was produced by pricking holes on a 0.
During conditioning, a harnessed bee was placed in front of an exhaust fan to prevent odor build-up in subsequent experiments. Any bee that responded with a conditioned response on the first trial was removed from the experiment during the experiment.
Bees in a low physical condition or dying were removed for further test. The order of presentation was randomized across subjects. A clean and tasteless injector was delivered to the bee after each odor test to exclude visual memory of reward during olfactory conditioning. Bees extending the proboscis only to nonanol odor were considered as successful individuals Fig. Bees that do not show PER to sucrose were discarded from the data.
The fieldwork took place in at the apiary of China Agricultural University, Beijing, China, and the experiment was performed twice in July and August, respectively.
To observe the effect of gut microbiota on the hive phenotypes with the same age, two treatment groups each containing three independent single-cohort colonies for were set up as previously described Briefly, brood frames were collected from a single hive, and adult bees were brushed off. In two days, about 1, bees emerged from each frame in the incubator, and we labeled individuals with colored tags on their thorax.
All newly emerged bees were then introduced to new empty hives together with a newly mated laying queen Two hives for control and treatment were established. The antibiotic treatment lasted for 5 days. The number of capped brood cells was counted every day, and post-treatment survival in the hive was assessed by counting the number of remaining marked bees of the whole hive Marked bees for both control and treatment groups were collected from each hive at time points of Day 7, 11, and 19 following the setup of hives, and the hind guts and brain tissue were dissected.
The topical treatment on the abdomen with AhR antagonist was performed as previously described 63 , 64 with modifications. Then the learning and memory ability of treated bees were measured as described above. After behavior test, gut samples were collected for further analysis. The A. Bee individuals of either control or antibiotic groups were sampled on Day 7, 11, and 19 during the hive experiment Fig.
Total genomic DNA of the gut microbiota was extracted from the whole gut homogenate using the CTAB-based method as previously described 9. Beijing, China for shotgun metagenome sequencing. A custom bee gut bacteria genomic database was generated based on bacterial isolates from honeybees and bumblebees Supplementary Data 1.
The sequencing quality of individual samples was assessed using FastQC v0. Gene expression was quantified using HTSeq v0. In contrast, reads aligned to multiple positions or overlapping with more than one gene are discarded. Differential gene expression analysis was performed using the DESeq2 package 68 in R.
We modeled read counts following a negative binomial distribution with normalized counts and dispersion. The proportion of the gene counts in the sample to the concentration of cDNA was scaled by a normalization factor using the median-of-ratios method. The variability between replicates is modeled by the dispersion parameter using empirical Bayes shrinkage estimation. For each gene, we fit a generalized linear model to get the overall expression strength of the gene and the log 2-fold change between CV and MF groups.
For significance testing, differential gene expression is determined by the Wald test. The resulting p-values were corrected for multiple comparisons using the Benjamini-Hochberg FDR method To get a better annotation of the honeybee reference genome, we re-annotate it using eggNOG-mapper v5. The proteome analysis was performed as described by Meng et al.
Briefly, three biological replicates per treatment group were analyzed for each group of bees. The search parameters were: parent ion tolerance, 15 ppm; fragment tolerance, 0. The analysis was performed by comparing an input data set of identified proteins to all functionally annotated GO categories in the entire genome of Apis mellifera from UniProt.
Then, the Bonferroni step-down was used to correct the p-value to control FDR. Functional grouping of the terms was based on the GO hierarchy. The tree-level was ranged from 3 to 8, and the kappa score level was 0.
Eluent A was 0. Detection of the experimental samples using MRM was based on Novogene in-house database. Q3 daughter was used for the quantification. Q1 parent ion , Q3, retention time, declustering potential, and collision energy were used for metabolite identification. A total of compounds were identified in the hemolymph and gut samples. Metabolites identified in the gut of MF and CV bees were obtained from previous study 9.
Metabolomics data analysis was then performed using MetaboAnalyst 4. Comparison of the learning and memory results was tested by Chi-squared test. Comparisons of normalized and raw metabolite data, and the expression level of TDO and AhR genes of different groups were made by Mann—Whitney u test.
The exact value of n representing the number of groups in the experiments described was indicated in the figure legends. Any additional biological replicates are described within the Methods and the Results.
Further information on research design is available in the Nature Research Reporting Summary linked to this article. All data supporting the findings of this study are available in the manuscript or supplementary information. Source data are provided with this paper.
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