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Species traits and environmental conditions are among the many factors that shape bee communities. Their effective conservation is currently challenged due to global changes. The gut microbiome likely contributes to bee plasticity and resilience but is largely understudied in solitary bees. A stable core microbiome in social bees has been identified to be important for health and survival in changing environmental conditions, but knowledge on a host-specific core microbiome in solitary bees is very scarce. In the present study, we analyzed the gut bacterial and fungal communities of eight solitary bee species commonly found in apple orchards along a latitudinal gradient throughout Europe. We aimed to understand the intra- and interspecific variations in the gut microbial communities and the extent to which host species and local environment shape the solitary bee gut microbiota. The bacterial community showed strong host effects, with each bee species having a distinct core bacterial community that was mostly stable across locations. The fungal community was most strongly influenced by the local environment, while different environmental variables were responsible for the variation in bacterial and fungal communities. Our study demonstrated that the examined solitary bee species harbor a distinct microbial diversity and composition, which undergoes host- and location-specific filtering.

Key Points A distinctive microbial community of approximately nine bacterial species clusters inhabits the bee gut. These bacteria are host-adapted, and each species cluster occupies particular niches and spatial locations in the bee. The gut microbial community of the bee is transmitted through social contact, similar to the mode of transmission in mammals. The characteristic microbial community of the bee gut can be perturbed and invaded by opportunistic microorganisms, which resembles disease states in humans. There is substantial strain-level diversity in the bee gut microbiota, with individual strains harbouring unique sets of genes with distinct functional capabilities. How this diversity arises and is maintained is not well understood. Metabolically, most members of the microbial community in the bee gut are fermentative, breaking down the carbohydrate-rich diet of bees into products, such as lactic acid and acetate. Although not yet well-established, these fermentative microorganisms may have a role in contributing to the nutrition of hosts. The normal bee gut microbiota has been associated with lower levels of infection with pathogens, which may indicate a beneficial role of the microbiota for the host bee. The bee gut microbiota can be cultured in vitro , and gnotobiotic bees can be easily produced, which makes bees a tractable model for the study of the symbiosis of gut microorganisms. The gut of honey bees is inhabited by a small group of highly host-adapted bacteria. In this Review, Kwong and Moran detail the composition and functions of the microbiota of honey bees and highlight similarities and differences to the human microbiota. The gut microbiota can have profound effects on hosts, but the study of these relationships in humans is challenging. The specialized gut microbial community of honey bees is similar to the mammalian microbiota, as both are mostly composed of host-adapted, facultatively anaerobic and microaerophilic bacteria. However, the microbial community of the bee gut is far simpler than the mammalian microbiota, being dominated by only nine bacterial species clusters that are specific to bees and that are transmitted through social interactions between individuals. Recent developments, which include the discovery of extensive strain-level variation, evidence of protective and nutritional functions, and reports of eco-physiological or disease-associated perturbations to the microbial community, have drawn attention to the role of the microbiota in bee health and its potential as a model for studying the ecology and evolution of gut symbionts.

Bees acquire carbohydrates from nectar and lipids; and amino acids from pollen, which also contains polysaccharides including cellulose, hemicellulose, and pectin. These potential energy sources could be degraded and fermented through microbial enzymatic activity, resulting in short chain fatty acids available to hosts. However, the contributions of individual microbiota members to polysaccharide digestion have remained unclear. Through analysis of bacterial isolate genomes and a metagenome of the honey bee gut microbiota, we identify that Bifidobacterium and Gilliamella are the principal degraders of hemicellulose and pectin. Both Bifidobacterium and Gilliamella show extensive strain-level diversity in gene repertoires linked to polysaccharide digestion. Strains from honey bees possess more such genes than strains from bumble bees. In Bifidobacterium, genes encoding carbohydrate-active enzymes are colocated within loci devoted to polysaccharide utilization, as in Bacteroides from the human gut. Carbohydrate-active enzyme-encoding gene expressions are up-regulated in response to particular hemicelluloses both in vitro and in vivo. Metabolomic analyses document that bees experimentally colonized by different strains generate distinctive gut metabolomic profiles, with enrichment for specific monosaccharides, corresponding to predictions from genomic data. The other 3 core gut species clusters (Snodgrassella and 2 Lactobacillus clusters) possess few or no genes for polysaccharide digestion. Together, these findings indicate that strain composition within individual hosts determines the metabolic capabilities and potentially affects host nutrition. Furthermore, the niche specialization revealed by our study may promote overall community stability in the gut microbiomes of bees.

Adult honeybees harbor a specialized gut microbiota of relatively low complexity. While seasonal differences in community composition have been reported, previous studies have focused on compositional changes rather than differences in absolute bacterial loads. Moreover, little is known about the gut microbiota of winter bees, which live much longer than bees during the foraging season, and which are critical for colony survival. We quantified seven core members of the bee gut microbiota in a single colony over 2 years and characterized the community composition in 14 colonies during summer and winter. Our data show that total bacterial loads substantially differ between foragers, nurses, and winter bees. Long-lived winter bees had the highest bacterial loads and the lowest community α-diversity, with a characteristic shift toward high levels of Bartonella and Commensalibacter , and a reduction of opportunistic colonizers. Using gnotobiotic bee experiments, we show that diet is a major contributor to the observed differences in bacterial loads. Overall, our study reveals that the gut microbiota of winter bees is remarkably different from foragers and nurses. Considering the importance of winter bees for colony survival, future work should focus on the role of the gut microbiota in winter bee health and disease.

Microbial symbionts living within animal guts are largely composed of resident bacterial species, forming communities that often provide benefits to the host. Gut microbiomes of adult honey bees (Apis mellifera) include core residents such as the betaproteobacterium Snodgrassella alvi, alongside transient parasites such as the protozoan Lotmaria passim. To test how these species affect microbiome composition and host physiology, we administered S. alvi and/or L. passim inocula to newly emerged worker bees from four genetic backgrounds (GH ) and reared them in normal (within hives) or stressed (protein-deficient, asocial) conditions. Microbiota acquired by normal bees were abundant but quantitatively differed across treatments, indicating treatment-associated dysbiosis. Pretreatment with S. alvi made normal bees more susceptible to L. passim and altered developmental and detoxification gene expression. Stressed bees were more susceptible to L. passim and were depauperate in core microbiota, yet supplementation with S. alvi did not alter this susceptibility. Microbiomes were generally more variable by GH in stressed bees, which also showed opposing and comparatively reduced modulation of gene expression responses to treatments compared with normal bees. These data provide experimental support for a link between altered gut microbiota and increased parasite and pathogen prevalence, as observed from honey bee colony collapse disorder.

Social bees harbor a simple and specialized microbiota that is spatially organized into different gut compartments. Recent results on the potential involvement of bee gut communities in pathogen protection and nutritional function have drawn attention to the impact of the microbiota on bee health. However, the contributions of gut microbiota to host physiology have yet to be investigated. Here we show that the gut microbiota promotes weight gain of both whole body and the gut in individual honey bees. This effect is likely mediated by changes in host vitellogenin, insulin signaling, and gustatory response. We found that microbial metabolism markedly reduces gut pH and redox potential through the production of shortchain fatty acids and that the bacteria adjacent to the gut wall form an oxygen gradient within the intestine. The short-chain fatty acid profile contributed by dominant gut species was confirmed in vitro. Furthermore, metabolomic analyses revealed that the gut community has striking impacts on the metabolic profiles of the gut compartments and the hemolymph, suggesting that gut bacteria degrade plant polymers from pollen and that the resulting metabolites contribute to host nutrition. Our results demonstrate how microbial metabolism affects bee growth, hormonal signaling, behavior, and gut physicochemical conditions. These findings indicate that the bee gut microbiota has basic roles similar to those found in some other animals and thus provides a model in studies of host–microbe interactions.

Honey bees are essential pollinators threatened by colony losses linked to the spread of parasites and pathogens. Here, we report a new approach for manipulating bee gene expression and protecting bee health. We engineered a symbiotic bee gut bacterium, Snodgrassella alvi, to induce eukaryotic RNA interference (RNAi) immune responses. We show that engineered S. alvi can stably recolonize bees and produce double-stranded RNA to activate RNAi and repress host gene expression, thereby altering bee physiology, behavior, and growth. We used this approach to improve bee survival after a viral challenge, and we show that engineered S. alvi can kill parasitic Varroa mites by triggering the mite RNAi response. This symbiont-mediated RNAi approach is a tool for studying bee functional genomics and potentially for safeguarding bee health.

Honeybees are important pollinators, having an essential role in the ecology of natural and agricultural environments. Honeybee colony losses episodes reported worldwide and have been associated with different pests and pathogens, pesticide exposure, and nutritional stress. This nutritional stress is related to the increase in monoculture areas which leads to a reduction of pollen availability and diversity. In this study, we examined whether nutritional stress affects honeybee gut microbiota, bee immunity, and infection by Nosema ceranae, under laboratory conditions. Consumption of Eucalyptus grandis pollen was used as a nutritionally poor-quality diet to study nutritional stress, in contraposition to the consumption of polyfloral pollen. Honeybees feed with Eucalyptus grandis pollen showed a lower abundance of Lactobacillus mellifer and Lactobacillus apis (Firm-4 and Firm-5, respectively) and Bifidobacterium spp. and a higher abundance of Bartonella apis, than honeybees fed with polyfloral pollen. Besides the impact of nutritional stress on honeybee microbiota, it also decreased the expression levels of vitellogenin and genes associated to immunity (glucose oxidase, hymenoptaecin and lysozyme). Finally, Eucalyptus grandis pollen favored the multiplication of Nosema ceranae. These results show that nutritional stress impacts the honeybee gut microbiota, having consequences on honeybee immunity and pathogen development. Those results may be useful to understand the influence of modern agriculture on honeybee health.

Populations of important pollinators, such as bumble bees and honey bees, are declining at alarming rates worldwide. Parasites are likely contributing to this phenomenon. A distinct resident community of bacteria has recently been identified in bumble bees and honey bees that is not shared with related solitary bee species. We now show that the presence of these microbiota protects bee hosts against a widespread and highly virulent natural parasite (Crithidia bombi) in an experimental setting. We add further support to this antagonistic relationship from patterns found in field data. For the successful establishment of these microbiota and a protective effect, exposure to feces from nest mates was needed after pupal eclosion. Transmission of beneficial gut bacteria could therefore represent an important benefit of sociality. Our results stress the importance of considering the host microbiota as an \"extended immune phenotype\" in addition to the host immune system itself and provide a unique perspective to understanding bees in health and disease.

Recently, it has become apparent that multiple factors are responsible for honey bee decline, including climate change, pests and pathogens, pesticides, and loss of foraging habitat. Of the large number of pathogens known to infect honey bees, very few are bacteria. Because adult workers abandon hives when diseased, many of their pathogens may go unnoticed. Here we characterized the virulence of Serratia marcescens strains isolated from honey bee guts and hemolymph. Our results indicate that S. marcescens , an opportunistic pathogen of many plants and animals, including humans, is a virulent opportunistic pathogen of honey bees, which could contribute to bee decline. Aside from the implications for honey bee health, the discovery of pathogenic S. marcescens strains in honey bees presents an opportunity to better understand how opportunistic pathogens infect and invade hosts. Although few honey bee diseases are known to be caused by bacteria, pathogens of adult worker bees may be underrecognized due to social immunity mechanisms. Specifically, infected adult bees typically abandon the hive or are removed by guards. Serratia marcescens , an opportunistic pathogen of many plants and animals, is often present at low abundance in the guts of honey bee workers and has recently been isolated from Varroa mites and from the hemolymph of dead and dying honey bees. However, the severity and prevalence of S. marcescens pathogenicity in honey bees have not been fully investigated. Here we characterized three S. marcescens strains isolated from the guts of honey bees and one previously isolated from hemolymph. In vivo tests confirmed that S. marcescens is pathogenic in workers. All strains caused mortality when a few cells were injected into the hemocoel, and the gut-isolated strains caused mortality when administered orally. In vitro assays and comparative genomics identified possible mechanisms of virulence of gut-associated strains. Expression of antimicrobial peptide and phenoloxidase genes was not elevated following infection, suggesting that these S. marcescens strains derived from honey bees can evade the immune response in their hosts. Finally, surveys from four locations in the United States indicated the presence of S. marcescens in the guts of over 60% of the worker bees evaluated. Taken together, these results suggest that S. marcescens is a widespread opportunistic pathogen of adult honey bees and that it may be highly virulent under some conditions such as perturbation of the normal gut microbiota or the presence of Varroa mites that puncture the integument, thereby enabling entry of bacterial cells. IMPORTANCE Recently, it has become apparent that multiple factors are responsible for honey bee decline, including climate change, pests and pathogens, pesticides, and loss of foraging habitat. Of the large number of pathogens known to infect honey bees, very few are bacteria. Because adult workers abandon hives when diseased, many of their pathogens may go unnoticed. Here we characterized the virulence of Serratia marcescens strains isolated from honey bee guts and hemolymph. Our results indicate that S. marcescens , an opportunistic pathogen of many plants and animals, including humans, is a virulent opportunistic pathogen of honey bees, which could contribute to bee decline. Aside from the implications for honey bee health, the discovery of pathogenic S. marcescens strains in honey bees presents an opportunity to better understand how opportunistic pathogens infect and invade hosts.