Background Microbial acquisition and development of the gut microbiota impact the establishment of a healthy host-microbes symbiosis. Compared with other animals, the eusocial bumblebees and honeybees possess a simple, recurring, and similar set of gut microbiota. However, all bee gut phylotypes have high strain-level diversity. Gut communities of different bee species are composed of host-specific groups of strains. The variable genomic regions among strains of the same species often confer critical functional differences, such as carbon source utilization, essential for the natural selection of specific strains. The annual bumblebee colony founded by solitary queens enables tracking the transmission routes of gut bacteria during development stages. Results Here, we first showed the changes in the microbiome of individual bumblebees across their holometabolous life cycle. Some core gut bacteria persist throughout different stages of development. Gut microbiota of newly emerged workers always resembles those of their queens, suggesting a vertical transmission of strains from queens to the newborn workers. We then follow the dynamic changes in the gut community by comparing strain-level metagenomic profiles of queen-worker pairs longitudinally collected across different stages of the nest development. Species composition of both queen and worker shifts with the colony’s growth, and the queen-to-worker vertical inheritance of specific strains was identified. Finally, comparative metagenome analysis showed clear host-specificity for microbes across different bee hosts. Species from honeybees often possess a higher level of strain variation, and they also exhibited more complex gene repertoires linked to polysaccharide digestion. Our results demonstrate bacterial transmission events in bumblebee, highlighting the role of social interactions in driving the microbiota composition. Conclusions By the community-wide metagenomic analysis based on the custom genomic database of bee gut bacteria, we reveal strain transmission events at high resolution and the dynamic changes in community structure along with the colony development. The social annual life cycle of bumblebees is key for the acquisition and development of the gut microbiota. Further studies using the bumblebee model will advance our understanding of the microbiome transmission and the underlying mechanisms, such as strain competition and niche selection.

Background Honey bee gut microbiota transmitted via social interactions are beneficial to the host health. Although the microbial community is relatively stable, individual variations and high strain-level diversity have been detected across honey bees. Although the bee gut microbiota structure is influenced by environmental factors, the heritability of the gut members and the contribution of the host genetics remains elusive. Considering bees within a colony are not readily genetically identical due to the polyandry of the queen, we hypothesize that the microbiota structure can be shaped by host genetics. Results We used shotgun metagenomics to simultaneously profile the microbiota and host genotypes of bees from hives of four different subspecies. Gut composition is more distant between genetically different bees at both phylotype- and “sequence-discrete population” levels. We then performed a successive passaging experiment within colonies of hybrid bees generated by artificial insemination, which revealed that the microbial composition dramatically shifts across batches of bees during the social transmission. Specifically, different strains from the phylotype of Snodgrassella alvi are preferentially selected by genetically varied hosts, and strains from different hosts show a remarkably biased distribution of single-nucleotide polymorphism in the Type IV pili loci. Genome-wide association analysis identified that the relative abundance of a cluster of Bifidobacterium strains is associated with the host glutamate receptor gene specifically expressed in the bee brain. Finally, mono-colonization of Bifidobacterium with a specific polysaccharide utilization locus impacts the alternative splicing of the gluR-B gene, which is associated with an increased GABA level in the brain. Conclusions Our results indicated that host genetics influence the bee gut composition and suggest a gut-brain connection implicated in the gut bacterial strain preference. Honey bees have been used extensively as a model organism for social behaviors, genetics, and the gut microbiome. Further identification of host genetic function as a shaping force of microbial structure will advance our understanding of the host-microbe interactions.

Background The spread of antibiotic resistance genes (ARGs) has been of global concern as one of the greatest environmental threats. The gut microbiome of animals has been found to be a large reservoir of ARGs, which is also an indicator of the environmental antibiotic spectrum. The conserved microbiota makes the honeybee a tractable and confined ecosystem for studying the maintenance and transfer of ARGs across gut bacteria. Although it has been found that honeybee gut bacteria harbor diverse sets of ARGs, the influences of environmental variables and the mechanism driving their distribution remain unclear. Results We characterized the gut resistome of two closely related honeybee species, Apis cerana and Apis mellifera, domesticated in 14 geographic locations across China. The composition of the ARGs was more associated with host species rather than with geographical distribution, and A. mellifera had a higher content of ARGs in the gut. There was a moderate geographic pattern of resistome distribution, and several core ARG groups were found to be prevalent among A. cerana samples. These shared genes were mainly carried by the honeybee-specific gut members Gilliamella and Snodgrassella. Transferrable ARGs were frequently detected in honeybee guts, and the load was much higher in A. mellifera samples. Genomic loci of the bee gut symbionts containing a streptomycin resistance gene cluster were nearly identical to those of the broad-host-range IncQ plasmid, a proficient DNA delivery system in the environment. By in vitro conjugation experiments, we confirmed that the mobilizable plasmids could be transferred between honeybee gut symbionts by conjugation. Moreover, “satellite plasmids” with fragmented genes were identified in the integrated regions of different symbionts from multiple areas. Conclusions Our study illustrates that the gut microbiota of different honeybee hosts varied in their antibiotic resistance structure, highlighting the role of the bee microbiome as a potential bioindicator and disseminator of antibiotic resistance. The difference in domestication history is highly influential in the structuring of the bee gut resistome. Notably, the evolution of plasmid-mediated antibiotic resistance is likely to promote the probability of its persistence and dissemination.

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The gut bacteria of honey bee recognized as a mutualistic partner with the insect host might have originated from a free-living or parasitic lifestyle. However, little is known about the genomic features underlying this lifestyle transition. Here we compared the genomes of bee gut bacteria Apibacter with their close relatives living in different lifestyles. We found that despite general reduction in the Apibacter genome, genes involved in amino acid synthesis and monosaccharide detoxification were retained, which is putatively beneficial to the host. Interestingly, the microaerobic Apibacter species specifically acquired genes encoding for the nitrate respiration (NAR). These together with nitrate transporter and enzymatic cofactor synthesis genes were found clustered in the genomes. The NAR system is also conserved in the cohabitating bee gut microbe Snodgrassella, although with a different structure. This convergence suggests a key role of respiratory nitrate reduction for microaerophilic microbiomes to colonize bee gut epithelium. Genes involved in lipid, histidine degradation were found partially or completely lost in Apibacter. Particularly, genes encoding for the conversion to the toxic intermediates in phenylacetate degradation, as well as other potential virulence factors, are specifically lost in Apibacter group. Antibiotic resistance genes are only sporadically distributed among Apibacter species, but are prevalent in their relatives, which may be related to the remotely living feature and less exposure to antibiotics of their bee hosts. Collectively, this study advanced our knowledge of genomic features specialized to bee gut symbionts.

The gut microbiome is a crucial element that facilitates a host’s adaptation to a changing environment. Compared to the western honeybee Apis mellifera, the Asian honeybee, Apis cerana populations across its natural range remain mostly semi-feral and are less affected by bee management, which provides a good system to investigate how gut microbiota evolve under environmental heterogeneity on large geographic scales. We compared and analyzed the gut microbiomes of 99 Asian honeybees, from genetically diverged populations covering 13 provinces across China. Bacterial composition varied significantly across populations at phylotype, sequence-discrete population (SDP), and strain levels, but with extensive overlaps, indicating that the diversity of microbial community among A. cerana populations is driven by nestedness. Pollen diets were significantly correlated with both the composition and function of the gut microbiome. Core bacteria, Gilliamella and Lactobacillus Firm-5, showed antagonistic turnovers and contributed to the enrichment in carbohydrate transport and metabolism. By feeding and inoculation bioassays, we confirmed that the variations in pollen polysaccharide composition contributed to the trade-off of these core bacteria. Progressive change, i.e., nestedness, is the foundation of gut microbiome evolution among the Asian honeybee. Such a transition during the co-diversification of gut microbiomes is affected by environmental factors, diets in general, and pollen polysaccharides in particular.

Honey and bumble bees are import pollinators, playing significant roles in the agricultural industry and maintaining the bio-ecosystem balance. Recently, it was found that the bees harbor a simple, yet specific gut microbiota. The normal bee gut microbiota makes essential contributions to host growth, endocrine signaling, and pathogen resistance. With the development of high through-put sequencing technology, researchers can now quickly identify the gut community structure for a low cost. This is helpful for biodiversity, conservation and bee health studies. However, the currently-used 16S rRNA databases are not specific enough to classify the bee gut microbiota properly. Many of the specific bacteria that enrich the gut of Apis cerana are in the genus Apibacter. Here, we isolated Apibacter species from A. cerana collected in five provinces of China, and added them to the current SILVA database. We also curated the nomenclature of some existing sequences and reclassified them in the updated database. Based on the analysis of the 16S rRNA sequencing data from one A. cerana and one Apis mellifera sample, our Bee Gut Microbiota-Database (BGM-Db) offers a more accurate classification of bee gut microbiota at a higher resolution than either the

Background: The gut microbiome is a crucial element that facilitates a host adaptation to a changing environment. Host-specificity often coincides with distinctions in gut microbes, suggesting a co-evolution of the holobionts. However, it is unclear how gut microbiota shared by a common host ancestor would co-diversify with hosts and eventually become distinct among sister hosts. In this context, understanding the evolutionary pathway of gut microbiomes of the same host species could provide insight on how holobionts co-adapt along environmental gradients. Specifically, we ask which factor, nature or nurture, i.e., genetics or diets, contributes more to the shaping of gut microbiome, along with host diversification and range expansion. Results: We compared and analyzed the gut microbiomes of 99 Asian honeybees, Apis cerana, from genetically diverged populations covering 13 provinces across China. Bacterial composition varied significantly across populations at phylotype, sequence-discrete population (SDP), and strain levels, but with extensive overlaps, indicating the diversity of microbial community among A. cerana populations is driven by nestedness. Taken together, genetics exhibited tangential impacts, while pollen diets were significantly correlated with both the composition and function of gut microbiome. Core bacteria, Gilliamella and Lactobacillus Firm-5, showed antagonistic turnovers and contributed to the enrichment in carbohydrate transport and metabolism. By feeding and inoculation bioassays, we confirmed that the variations in pollen polysaccharide composition contributed to the trade-off of these core bacteria. Conclusions: Progressive change, i.e., nestedness, is the foundation of gut microbiome evolution in the Asian honeybee. Such a transition during the co-diversification of gut microbiomes is shaped primarily by environmental factors, diets in general, pollen polysaccharide in particular.