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The honeybee microbiota and its impact on health and disease

Nature Reviews Microbiology volume 22, pages 122–137 (2024)Cite this article

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Abstract

Honeybees (Apis mellifera) are key pollinators that support global agriculture and are long-established models for developmental and behavioural research. Recently, they have emerged as models for studying gut microbial communities. Earlier research established that hindguts of adult worker bees harbour a conserved set of host-restricted bacterial species, each showing extensive strain variation. These bacteria can be cultured axenically and introduced to gnotobiotic hosts, and some have basic genetic tools available. In this Review, we explore the most recent research showing how the microbiota establishes itself in the gut and impacts bee biology and health. Microbiota members occupy specific niches within the gut where they interact with each other and the host. They engage in cross-feeding and antagonistic interactions, which likely contribute to the stability of the community and prevent pathogen invasion. An intact gut microbiota provides protection against diverse pathogens and parasites and contributes to the processing of refractory components of the pollen coat and dietary toxins. Absence or disruption of the microbiota results in altered expression of genes that underlie immunity, metabolism, behaviour and development. In the field, such disruption by agrochemicals may negatively impact bees. These findings demonstrate a key developmental and protective role of the microbiota, with broad implications for bee health.

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Fig. 1: Microbial dynamics and spatial organization in the honeybee gut.
Fig. 2: The roles of the honeybee gut microbiota in pathogen protection.
Fig. 3: The roles of the honeybee gut microbiota in development and behaviour.
Fig. 4: The roles of the honeybee gut microbiota in digestion and detoxification.
Fig. 5: Beekeeping and agricultural practices that affect honeybee gut communities.

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References

  1. Robinson, G. E., Page, R. E. Jr, Strambi, C. & Strambi, A. Hormonal and genetic control of behavioral integration in honey bee colonies. Science 246, 109–112 (1989).

    Article  CAS  PubMed  ADS  Google Scholar 

  2. Menzel, R. The honeybee as a model for understanding the basis of cognition. Nat. Rev. Neurosci. 13, 758–768 (2012).

    Article  CAS  PubMed  Google Scholar 

  3. Zayed, A. & Robinson, G. E. Understanding the relationship between brain gene expression and social behavior: lessons from the honey bee. Annu. Rev. Genet. 46, 591–615 (2012).

    Article  CAS  PubMed  Google Scholar 

  4. Kwong, W. K. & Moran, N. A. Gut microbial communities of social bees. Nat. Rev. Microbiol. 14, 374–384 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Romero, S., Nastasa, A., Chapman, A., Kwong, W. K. & Foster, L. J. The honey bee gut microbiota: strategies for study and characterization. Insect Mol. Biol. 28, 455–472 (2019).

    Article  CAS  PubMed  Google Scholar 

  6. Cox-Foster, D. L. et al. A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318, 283–287 (2007).

    Article  CAS  PubMed  ADS  Google Scholar 

  7. Martinson, V. G. et al. A simple and distinctive microbiota associated with honey bees and bumble bees. Mol. Ecol. 20, 619–628 (2011).

    Article  PubMed  Google Scholar 

  8. Moran, N. A., Hansen, A. K., Powell, J. E. & Sabree, Z. L. Distinctive gut microbiota of honey bees assessed using deep sampling from individual worker bees. PLoS ONE 7, e36393 (2012).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  9. Martinson, V. G., Moy, J. & Moran, N. A. Establishment of characteristic gut bacteria during development of the honeybee worker. Appl. Environ. Microbiol. 78, 2830–2840 (2012).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  10. Powell, J. E., Martinson, V. G., Urban-Mead, K. & Moran, N. A. Routes of acquisition of the gut microbiota of the honey bee Apis mellifera. Appl. Environ. Microbiol. 80, 7378–7387 (2014).

    Article  PubMed  PubMed Central  ADS  Google Scholar 

  11. Zheng, J. et al. A taxonomic note on the genus Lactobacillus: description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae. Int. J. Syst. Evol. Microbiol. 70, 2782–2858 (2020).

    Article  CAS  PubMed  Google Scholar 

  12. D’Alvise, P. et al. The impact of winter feed type on intestinal microbiota and parasites in honey bees. Apidologie 49, 252–264 (2018).

    Article  Google Scholar 

  13. Corby-Harris, V., Maes, P. & Anderson, K. E. The bacterial communities associated with honey bee (Apis mellifera) foragers. PLoS ONE 9, e95056 (2014).

    Article  PubMed  PubMed Central  ADS  Google Scholar 

  14. Rothman, J. A., Carroll, M. J., Meikle, W. G., Anderson, K. E. & McFrederick, Q. S. Longitudinal effects of supplemental forage on the honey bee (Apis mellifera) microbiota and inter- and intra-colony variability. Microb. Ecol. 76, 814–824 (2018).

    Article  CAS  PubMed  ADS  Google Scholar 

  15. Kapheim, K. M. et al. Caste-specific differences in hindgut microbial communities of honey bees (Apis mellifera). PLoS ONE 10, e0123911 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  16. Wu, J. et al. Honey bee genetics shape the strain-level structure of gut microbiota in social transmission. Microbiome 9, 225 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Kešnerová, L. et al. Gut microbiota structure differs between honeybees in winter and summer. ISME J. 14, 801–814 (2020).

    Article  PubMed  Google Scholar 

  18. Jones, J. C. et al. Gut microbiota composition is associated with environmental landscape in honey bees. Ecol. Evol. 8, 441–451 (2018).

    Article  PubMed  Google Scholar 

  19. Olofsson, T. C., Alsterfjord, M., Nilson, B., Butler, È. & Vásquez, A. Lactobacillus apinorum sp. nov., Lactobacillus mellifer sp. nov., Lactobacillus mellis sp. nov., Lactobacillus melliventris sp. nov., Lactobacillus kimbladii sp. nov., Lactobacillus helsingborgensis sp. nov. and Lactobacillus kullabergensis sp. nov., isolated from the honey stomach of the honeybee Apis mellifera. Int. J. Syst. Evol. Microbiol. 64, 3109–3119 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  20. Engel, P., Kwong, W. K. & Moran, N. A. Frischella perrara gen. nov., sp. nov., a Gammaproteobacterium isolated from the gut of the honeybee, Apis mellifera. Int. J. Syst. Evol. Microbiol. 63, 3646–3651 (2013).

    Article  CAS  PubMed  Google Scholar 

  21. Kešnerová, L., Moritz, R. & Engel, P. Bartonella apis sp. nov., a honey bee gut symbiont of the class Alphaproteobacteria. Int. J. Syst. Evol. Microbiol. 66, 414–421 (2016).

    Article  PubMed  Google Scholar 

  22. Ludvigsen, J., Porcellato, D., Amdam, G. V. & Rudi, K. Addressing the diversity of the honeybee gut symbiont Gilliamella: description of Gilliamella apis sp. nov., isolated from the gut of honeybees (Apis mellifera). Int. J. Syst. Evol. Microbiol. 68, 1762–1770 (2018).

    Article  CAS  PubMed  Google Scholar 

  23. Milani, C. et al. Genomic encyclopedia of type strains of the genus Bifidobacterium. Appl. Environ. Microbiol. 80, 6290–6302 (2014).

    Article  PubMed  PubMed Central  ADS  Google Scholar 

  24. Kwong, W. K. & Moran, N. A. Cultivation and characterization of the gut symbionts of honey bees and bumble bees: description of Snodgrassella alvi gen. nov., sp. nov., a member of the family Neisseriaceae of the Betaproteobacteria, and Gilliamella apicola gen. nov., sp. nov., a member of Orbaceae fam. nov., Orbales ord. nov., a sister taxon to the order ‘Enterobacteriales’ of the Gammaproteobacteria. Int. J. Syst. Evol. Microbiol. 63, 2008–2018 (2013).

    Article  CAS  PubMed  Google Scholar 

  25. Ellegaard, K. M. & Engel, P. Genomic diversity landscape of the honey bee gut microbiota. Nat. Commun. 10, 446 (2019). Shotgun metagenomics allows the assessment of honeybee gut microbiota diversity, showing that previously described phylotypes contain sequence-discrete populations or species, which tend to co-exist in individual bees and show age-specific abundance profiles.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  26. Parish, A. J., Rice, D. W., Tanquary, V. M., Tennessen, J. M. & Newton, I. L. G. Honey bee symbiont buffers larvae against nutritional stress and supplements lysine. ISME J. 16, 2160–2168 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Powell, J. E., Eiri, D., Moran, N. A. & Rangel, J. Modulation of the honey bee queen microbiota: effects of early social contact. PLoS ONE 13, e0200527 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  28. Callegari, M. et al. Compartmentalization of bacterial and fungal microbiomes in the gut of adult honeybees. NPJ Biofilms Microbiomes 7, 42 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  29. Gómez-Moracho, T. et al. Experimental evidence of harmful effects of Crithidia mellificae and Lotmaria passim on honey bees. Int. J. Parasitol. 50, 1117–1124 (2020).

    Article  PubMed  Google Scholar 

  30. Tokarev, Y. S. et al. A formal redefinition of the genera Nosema and Vairimorpha (Microsporidia: Nosematidae) and reassignment of species based on molecular phylogenetics. J. Invertebr. Pathol. 169, 107279 (2020).

    Article  CAS  PubMed  Google Scholar 

  31. Grupe, A. C. II & Quandt, C. A. A growing pandemic: a review of Nosema parasites in globally distributed domesticated and native bees. PLoS Pathog. 16, e1008580 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  32. Decker, L. E. et al. Higher variability in fungi compared to bacteria in the foraging honey bee gut. Microb. Ecol. 85, 330–334 (2023).

    Article  PubMed  ADS  Google Scholar 

  33. Kwong, W. K. et al. Dynamic microbiome evolution in social bees. Sci. Adv. 3, e1600513 (2017). The distribution and phylogenies of the core bacterial lineages in the microbiota of social bees suggest that these lineages have co-evolved with bee hosts since the origin of the Corbiculata clade, about 80 million years ago.

    Article  PubMed  PubMed Central  ADS  Google Scholar 

  34. Ellegaard, K. M., Suenami, S., Miyazaki, R. & Engel, P. Vast differences in strain-level diversity in the gut microbiota of two closely related honey bee species. Curr. Biol. 30, 2520–2531.e7 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Hammer, T. J., Le, E., Martin, A. N. & Moran, N. A. The gut microbiota of bumblebees. Insectes Soc. 68, 287–301 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  36. Sarton-Lohéac, G. et al. Deep divergence and genomic diversification of gut symbionts of neotropical stingless bees. MBio 14, e0353822 (2023).

    Article  PubMed  Google Scholar 

  37. Cerqueira, A. E. S. et al. Extinction of anciently associated gut bacterial symbionts in a clade of stingless bees. ISME J. 15, 2813–2816 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  38. Figueroa, L. L., Maccaro, J. J., Krichilsky, E., Yanega, D. & McFrederick, Q. S. Why did the bee eat the chicken? Symbiont gain, loss, and retention in the vulture bee microbiome. MBio 12, e0231721 (2021).

    Article  PubMed  Google Scholar 

  39. Kueneman, J. G., Bonadies, E., Thomas, D., Roubik, D. W. & Wcislo, W. T. Neotropical bee microbiomes point to a fragmented social core and strong species-level effects. Microbiome 11, 150 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  40. Holley, J.-A. C., Jackson, M. N., Pham, A. T., Hatcher, S. C. & Moran, N. A. Carpenter bees (Xylocopa) harbor a distinctive gut microbiome related to that of honey bees and bumble bees. Appl. Environ. Microbiol. 88, e0020322 (2022).

    Article  PubMed  Google Scholar 

  41. Engel, P., Martinson, V. G. & Moran, N. A. Functional diversity within the simple gut microbiota of the honey bee. Proc. Natl Acad. Sci. USA 109, 11002–11007 (2012).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  42. Zheng, H. et al. Division of labor in honey bee gut microbiota for plant polysaccharide digestion. Proc. Natl Acad. Sci. USA 116, 25909–25916 (2019). Honeybee gut symbionts, including Bifidobacterium, Gilliamella and Lactobacillus strains, encode specific pectate lyases and glycoside hydrolases that are highly variable between strains and are involved in the degradation of recalcitrant components within pollen husks.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  43. Zheng, H. et al. Metabolism of toxic sugars by strains of the bee gut symbiont Gilliamella apicola. MBio 7, e01326-16 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  44. Lee, F. J., Miller, K. I., McKinlay, J. B. & Newton, I. L. G. Differential carbohydrate utilization and organic acid production by honey bee symbionts. FEMS Microbiol. Ecol. 94, fiy113 (2018).

    Article  CAS  Google Scholar 

  45. Kwong, W. K., Mancenido, A. L. & Moran, N. A. Immune system stimulation by the native gut microbiota of honey bees. R. Soc. Open Sci. 4, 170003 (2017).

    Article  PubMed  PubMed Central  ADS  Google Scholar 

  46. Horak, R. D., Leonard, S. P. & Moran, N. A. Symbionts shape host innate immunity in honeybees. Proc. Biol. Sci. 287, 20201184 (2020). The honeybee symbiont S. alvi activates the expression of host AMPs, such as apidaecin, defensin and hymenoptaecin, but live S. alvi cells appear to suppress some parts of innate immune signalling.

    PubMed  PubMed Central  Google Scholar 

  47. Raymann, K. & Moran, N. A. The role of the gut microbiome in health and disease of adult honey bee workers. Curr. Opin. Insect Sci. 26, 97–104 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  48. Steele, M. I., Motta, E. V. S., Gattu, T., Martinez, D. & Moran, N. A. The gut microbiota protects bees from invasion by a bacterial pathogen. Microbiol. Spectr. 9, e0039421 (2021).

    Article  PubMed  Google Scholar 

  49. Palmer-Young, E. C., Markowitz, L. M., Huang, W.-F. & Evans, J. D. High temperatures augment inhibition of parasites by a honey bee gut symbiont. Appl. Environ. Microbiol. 89, e01023 (2023).

    Article  PubMed  PubMed Central  ADS  Google Scholar 

  50. Zheng, H., Powell, J. E., Steele, M. I., Dietrich, C. & Moran, N. A. Honeybee gut microbiota promotes host weight gain via bacterial metabolism and hormonal signaling. Proc. Natl Acad. Sci. USA 114, 4775–4780 (2017).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  51. Motta, E. V. S., Powell, J. E., Leonard, S. P. & Moran, N. A. Prospects for probiotics in social bees. Philos. Trans. R. Soc. Lond. B Biol. Sci. 377, 20210156 (2022). This paper summarizes recent research on probiotics for bees and presents new evidence that the use of defined native gut bacteria is a promising way to restore perturbed microbial communities in bees exposed to agrochemicals.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Wang, X. et al. High-fat diets with differential fatty acids induce obesity and perturb gut microbiota in honey bee. Int. J. Mol. Sci. 22, 834 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Zhang, Z. et al. Honeybee gut Lactobacillus modulates host learning and memory behaviors via regulating tryptophan metabolism. Nat. Commun. 13, 2037 (2022).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  54. Engel, P. et al. The bee microbiome: impact on bee health and model for evolution and ecology of host–microbe interactions. MBio 7, e02164-15 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  55. Emery, O., Schmidt, K. & Engel, P. Immune system stimulation by the gut symbiont Frischella perrara in the honey bee (Apis mellifera). Mol. Ecol. 26, 2576–2590 (2017).

    Article  CAS  PubMed  Google Scholar 

  56. Engel, P., Bartlett, K. D. & Moran, N. A. The bacterium Frischella perrara causes scab formation in the gut of its honeybee host. MBio 6, e00193-15 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  57. Li, Y., Leonard, S. P., Powell, J. E. & Moran, N. A. Species divergence in gut-restricted bacteria of social bees. Proc. Natl Acad. Sci. USA 119, e2115013119 (2022). This study describes the use of genome sequences from isolates of S. alvi and Gilliamella spp. to identify ‘populations’ defined by evidence for homologous exchange and therefore representing biological species.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Bobay, L.-M., Wissel, E. F. & Raymann, K. Strain structure and dynamics revealed by targeted deep sequencing of the honey bee gut microbiome. mSphere 5, e11694-20 (2020).

    Article  Google Scholar 

  59. Raymann, K., Bobay, L.-M. & Moran, N. A. Antibiotics reduce genetic diversity of core species in the honeybee gut microbiome. Mol. Ecol. 27, 2057–2066 (2018).

    Article  CAS  PubMed  Google Scholar 

  60. Steele, M. I., Kwong, W. K., Whiteley, M. & Moran, N. A. Diversification of type VI secretion system toxins reveals ancient antagonism among bee gut microbes. MBio 8, e01630-17 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  61. Brochet, S. et al. Niche partitioning facilitates coexistence of closely related honey bee gut bacteria. eLife 10, e68583 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Ellegaard, K. M. et al. Genomic changes underlying host specialization in the bee gut symbiont Lactobacillus Firm5. Mol. Ecol. 28, 2224–2237 (2019).

    Article  PubMed  Google Scholar 

  63. Motta, E. V. S. et al. Host-microbiome metabolism of a plant toxin in bees. eLife 11, e82595 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Kešnerová, L. et al. Disentangling metabolic functions of bacteria in the honey bee gut. PLoS Biol. 15, e2003467 (2017). This study combines metabolomics and gnotobiotic bees to investigate the metabolic contributions of individual members of the bee gut microbiota.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Koch, H. et al. Host and gut microbiome modulate the antiparasitic activity of nectar metabolites in a bumblebee pollinator. Philos. Trans. R. Soc. Lond. B Biol. Sci. 377, 20210162 (2022). This study disentangles the contributions of host and gut microbial enzymes to the metabolism of some plant secondary metabolites.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Tauber, J. P. et al. Colony-level effects of amygdalin on honeybees and their microbes. Insects 11, 783 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  67. Kwong, W. K., Engel, P., Koch, H. & Moran, N. A. Genomics and host specialization of honey bee and bumble bee gut symbionts. Proc. Natl Acad. Sci. USA 111, 11509–11514 (2014).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  68. Quinn, A. et al. Foraging on host synthesized metabolites enables the bacterial symbiont Snodgrassella alvi to colonize the honey bee gut. Preprint at bioRxiv https://doi.org/10.1101/2023.01.23.524906 (2023).

  69. Powell, J. E., Leonard, S. P., Kwong, W. K., Engel, P. & Moran, N. A. Genome-wide screen identifies host colonization determinants in a bacterial gut symbiont. Proc. Natl Acad. Sci. USA 113, 13887–13892 (2016).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  70. Cabirol, A. et al. A defined community of core gut microbiota members promotes cognitive performance in honey bees. Preprint at bioRxiv https://doi.org/10.1101/2023.01.03.522593 (2023).

  71. Steele, M. I. & Moran, N. A. Evolution of interbacterial antagonism in bee gut microbiota reflects host and symbiont diversification. mSystems 6, e00063-21 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  72. Chen, C., Yang, X. & Shen, X. Confirmed and potential roles of bacterial T6SSs in the intestinal ecosystem. Front. Microbiol. 10, 1484 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  73. Schmidt, K. et al. Integration host factor regulates colonization factors in the bee gut symbiont Frischella perrara. eLife 12, e76182 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  74. Le, N.-H., Pinedo, V., Lopez, J., Cava, F. & Feldman, M. F. Killing of Gram-negative and Gram-positive bacteria by a bifunctional cell wall-targeting T6SS effector. Proc. Natl Acad. Sci. USA 118, e2106555118 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Coyte, K. Z., Schluter, J. & Foster, K. R. The ecology of the microbiome: networks, competition, and stability. Science 350, 663–666 (2015).

    Article  CAS  PubMed  ADS  Google Scholar 

  76. Heilbronner, S., Krismer, B., Brötz-Oesterhelt, H. & Peschel, A. The microbiome-shaping roles of bacteriocins. Nat. Rev. Microbiol. 19, 726–739 (2021).

    Article  CAS  PubMed  Google Scholar 

  77. Zendo, T. et al. Kunkecin A, a new nisin variant bacteriocin produced by the fructophilic lactic acid bacterium, Apilactobacillus kunkeei FF30-6 isolated from honey bees. Front. Microbiol. 11, 571903 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  78. Shkoporov, A. N., Turkington, C. J. & Hill, C. Mutualistic interplay between bacteriophages and bacteria in the human gut. Nat. Rev. Microbiol. 20, 737–749 (2022).

    Article  CAS  PubMed  Google Scholar 

  79. Bonilla-Rosso, G., Steiner, T., Wichmann, F., Bexkens, E. & Engel, P. Honey bees harbor a diverse gut virome engaging in nested strain-level interactions with the microbiota. Proc. Natl Acad. Sci. USA 117, 7355–7362 (2020). This study shows that honeybee guts harbour bacteriophage communities that have co-evolved with core bacterial symbionts and may fulfil crucial roles in mediating antagonistic and beneficial interactions within the bee gut microbiota.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  80. Busby, T. J., Miller, C. R., Moran, N. A. & Van Leuven, J. T. Global composition of the bacteriophage community in honey bees. mSystems 7, e0119521 (2022).

    Article  PubMed  Google Scholar 

  81. Deboutte, W. et al. Honey-bee–associated prokaryotic viral communities reveal wide viral diversity and a profound metabolic coding potential. Proc. Natl Acad. Sci. USA 117, 10511–10519 (2020).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  82. Wang, J. et al. Stably transmitted defined microbial community in honeybees preserves Hafnia alvei inhibition by regulating the immune system. Front. Microbiol. 13, 1074153 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  83. Miller, D. L., Smith, E. A. & Newton, I. L. G. A bacterial symbiont protects honey bees from fungal disease. MBio 12, e0050321 (2021). This study shows that the symbiont B. apis protects honeybee larvae against the fungal pathogen A. flavus by producing specific antifungal molecules.

    Article  PubMed  Google Scholar 

  84. Lang, H. et al. Engineered symbiotic bacteria interfering Nosema redox system inhibit microsporidia parasitism in honeybees. Nat. Commun. 14, 2778 (2023).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  85. Huang, Q., Lariviere, P. J., Powell, J. E. & Moran, N. A. Engineered gut symbiont inhibits microsporidian parasite and improves honey bee survival. Proc. Natl Acad. Sci. USA 120, e2220922120 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Li, J. H. et al. New evidence showing that the destruction of gut bacteria by antibiotic treatment could increase the honey bee’s vulnerability to Nosema infection. PLoS ONE 12, e0187505 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  87. Dosch, C. et al. The gut microbiota can provide viral tolerance in the honey bee. Microorganisms 9, 871 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Lang, H. et al. Specific strains of honeybee gut Lactobacillus stimulate host immune system to protect against pathogenic Hafnia alvei. Microbiol. Spectr. 10, e0189621 (2022).

    Article  PubMed  Google Scholar 

  89. Evans, J. D. et al. Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol. Biol. 15, 645–656 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Nappi, A. J. & Christensen, B. M. Melanogenesis and associated cytotoxic reactions: applications to insect innate immunity. Insect Biochem. Mol. Biol. 35, 443–459 (2005).

    Article  CAS  PubMed  Google Scholar 

  91. Raymann, K., Coon, K. L., Shaffer, Z., Salisbury, S. & Moran, N. A. Pathogenicity of Serratia marcescens strains in honey bees. MBio 9, e01649-18 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  92. Burritt, N. L. et al. Sepsis and hemocyte loss in honey bees (Apis mellifera) infected with Serratia marcescens strain Sicaria. PLoS ONE 11, e0167752 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  93. El Sanousi, S. M., El Sarag, M. S. A. & Mohamed, S. E. Properties of Serratia marcescens isolated from diseased honeybee (Apis mellifera) larvae. Microbiology 133, 215–219 (1987).

    Article  Google Scholar 

  94. Evans, J. D. & Spivak, M. Socialized medicine: individual and communal disease barriers in honey bees. J. Invertebr. Pathol. 103, S62–S72 (2010).

    Article  PubMed  Google Scholar 

  95. Baracchi, D., Fadda, A. & Turillazzi, S. Evidence for antiseptic behaviour towards sick adult bees in honey bee colonies. J. Insect Physiol. 58, 1589–1596 (2012).

    Article  CAS  PubMed  Google Scholar 

  96. Raymann, K., Shaffer, Z. & Moran, N. A. Antibiotic exposure perturbs the gut microbiota and elevates mortality in honeybees. PLoS Biol. 15, e2001861 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  97. Forsgren, E. European foulbrood in honey bees. J. Invertebr. Pathol. 103, S5–S9 (2010).

    Article  PubMed  Google Scholar 

  98. Genersch, E. American foulbrood in honeybees and its causative agent, Paenibacillus larvae. J. Invertebr. Pathol. 103, S10–S19 (2010).

    Article  PubMed  Google Scholar 

  99. Kačániová, M., Gasper, J. & Terentjeva, M. Antagonistic effect of gut microbiota of honeybee (Apis mellifera) against causative agent of American foulbrood Paenibacillus larvae. J. Microbiol. Biotechnol. Food Sci. 9, 478–481 (2019).

    Article  Google Scholar 

  100. Al-Ghamdi, A. et al. In vitro antagonistic potential of gut bacteria isolated from indigenous honey bee race of Saudi Arabia against Paenibacillus larvae. J. Apic. Res. 59, 825–833 (2020).

    Article  Google Scholar 

  101. Koch, H. & Schmid-Hempel, P. Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proc. Natl Acad. Sci. USA 108, 19288–19292 (2011).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  102. Koch, H. & Schmid-Hempel, P. Gut microbiota instead of host genotype drive the specificity in the interaction of a natural host–parasite system. Ecol. Lett. 15, 1095–1103 (2012).

    Article  PubMed  Google Scholar 

  103. Mockler, B. K., Kwong, W. K., Moran, N. A. & Koch, H. Microbiome structure influences infection by the parasite Crithidia bombi in bumble bees. Appl. Environ. Microbiol. 84, e02335-17 (2018).

    Article  PubMed  PubMed Central  ADS  Google Scholar 

  104. Koch, H., Woodward, J., Langat, M. K., Brown, M. J. F. & Stevenson, P. C. Flagellum removal by a nectar metabolite inhibits infectivity of a bumblebee parasite. Curr. Biol. 29, 3494–3500.e5 (2019).

    Article  CAS  PubMed  Google Scholar 

  105. Palmer-Young, E. C., Raffel, T. R. & McFrederick, Q. S. pH-mediated inhibition of a bumble bee parasite by an intestinal symbiont. Parasitology 146, 380–388 (2019).

    Article  CAS  PubMed  Google Scholar 

  106. Floyd, A. S. et al. Microbial ecology of European foul brood disease in the honey bee (Apis mellifera): towards a microbiome understanding of disease susceptibility. Insects 11, 555 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  107. Rubanov, A., Russell, K. A., Rothman, J. A., Nieh, J. C. & McFrederick, Q. S. Intensity of Nosema ceranae infection is associated with specific honey bee gut bacteria and weakly associated with gut microbiome structure. Sci. Rep. 9, 3820 (2019).

    Article  PubMed  PubMed Central  ADS  Google Scholar 

  108. Guo, J. et al. Characterization of gut bacteria at different developmental stages of Asian honey bees, Apis cerana. J. Invertebr. Pathol. 127, 110–114 (2015).

    Article  PubMed  Google Scholar 

  109. Kim, C. et al. Analysis of the gut microbiome of susceptible and resistant honeybees (Apis cerana) against sacbrood virus disease. J. Appl. Entomol. 146, 1078–1086 (2022).

    Article  CAS  Google Scholar 

  110. Sullivan, J. P., Fahrbach, S. E. & Robinson, G. E. Juvenile hormone paces behavioral development in the adult worker honey bee. Horm. Behav. 37, 1–14 (2000).

    Article  CAS  PubMed  Google Scholar 

  111. Toth, A. L., Kantarovich, S., Meisel, A. F. & Robinson, G. E. Nutritional status influences socially regulated foraging ontogeny in honey bees. J. Exp. Biol. 208, 4641–4649 (2005).

    Article  PubMed  Google Scholar 

  112. Bajgar, A., Jindra, M. & Dolezel, D. Autonomous regulation of the insect gut by circadian genes acting downstream of juvenile hormone signaling. Proc. Natl Acad. Sci. USA 110, 4416–4421 (2013).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  113. Zhang, Z., Mu, X., Shi, Y. & Zheng, H. Distinct roles of honeybee gut bacteria on host metabolism and neurological processes. Microbiol. Spectr. 10, e0243821 (2022).

    Article  PubMed  Google Scholar 

  114. Li, L. et al. Gut microbiome drives individual memory variation in bumblebees. Nat. Commun. 12, 6588 (2021).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  115. Liberti, J. et al. The gut microbiota affects the social network of honeybees. Nat. Ecol. Evol. 6, 1471–1479 (2022). This study shows that microbiota-colonized bees, when compared with microbiota-deprived bees, exhibit increased levels of brain metabolites, such as serine and ornithine, and increased specialized head-to-head interactions between nestmates.

    Article  PubMed  PubMed Central  Google Scholar 

  116. Cabirol, A., Moriano-Gutierrez, S. & Engel, P. Neuroactive metabolites modulated by the gut microbiota in honey bees. Mol. Microbiol. https://doi.org/10.1111/mmi.15167 (2023).

    Article  PubMed  Google Scholar 

  117. Billard, J.-M. d-Amino acids in brain neurotransmission and synaptic plasticity. Amino Acids 43, 1851–1860 (2012).

    Article  CAS  PubMed  Google Scholar 

  118. Scofield, H. N. & Mattila, H. R. Honey bee workers that are pollen stressed as larvae become poor foragers and waggle dancers as adults. PLoS ONE 10, e0121731 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  119. Brodschneider, R. & Crailsheim, K. Nutrition and health in honey bees. Apidologie 41, 278–294 (2010).

    Article  Google Scholar 

  120. Wu, Y. et al. Honey bee (Apis mellifera) gut microbiota promotes host endogenous detoxification capability via regulation of P450 gene expression in the digestive tract. Microb. Biotechnol. 13, 1201–1212 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Tian, B., Fadhil, N. H., Powell, J. E., Kwong, W. K. & Moran, N. A. Long-term exposure to antibiotics has caused accumulation of resistance determinants in the gut microbiota of honeybees. MBio 3, 00377-12 (2012).

    Article  Google Scholar 

  122. Soares, K. O. et al. Tetracycline exposure alters key gut microbiota in africanized honey bees (Apis mellifera scutellata x spp.). Front. Ecol. Evol. 9, 716660 (2021).

    Article  Google Scholar 

  123. Baffoni, L. et al. Honeybee exposure to veterinary drugs: how is the gut microbiota affected? Microbiol. Spectr. 9, e0017621 (2021).

    Article  PubMed  Google Scholar 

  124. Motta, E. V. S. & Moran, N. A. Impact of glyphosate on the honey bee gut microbiota: effects of intensity, duration, and timing of exposure. mSystems 5, e00268-20 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  125. Powell, J. E., Carver, Z., Leonard, S. P. & Moran, N. A. Field-realistic tylosin exposure impacts honey bee microbiota and pathogen susceptibility, which is ameliorated by native gut probiotics. Microbiol. Spectr. 9, e0010321 (2021).

    Article  PubMed  Google Scholar 

  126. Ortiz-Alvarado, Y. et al. Antibiotics in hives and their effects on honey bee physiology and behavioral development. Biol. Open 9, bio053884 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Duan, X. et al. Antibiotic treatment decrease the fitness of honeybee (Apis mellifera) larvae. Insects 12, 301 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  128. Raymann, K. in Honey Bee Medicine for the Veterinary Practitioner (eds Kane, T. R. & Faux, C. M.) 125–134 (Wiley, 2021).

  129. Ramsey, S. D. et al. Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. Proc. Natl Acad. Sci. USA 116, 1792–1801 (2019).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  130. Yu, L. et al. Honey bee Apis mellifera larvae gut microbial and immune, detoxication responses towards flumethrin stress. Environ. Pollut. 290, 118107 (2021).

    Article  CAS  PubMed  Google Scholar 

  131. Qi, S. et al. Acaricide flumethrin-induced sublethal risks in honeybees are associated with gut symbiotic bacterium Gilliamella apicola through microbe–host metabolic interactions. Chemosphere 307, 136030 (2022).

    Article  CAS  PubMed  Google Scholar 

  132. Kakumanu, M. L., Reeves, A. M., Anderson, T. D., Rodrigues, R. R. & Williams, M. A. Honey bee gut microbiome is altered by in-hive pesticide exposures. Front. Microbiol. 7, 1255 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  133. Rouzé, R., Moné, A., Delbac, F., Belzunces, L. & Blot, N. The honeybee gut microbiota is altered after chronic exposure to different families of insecticides and infection by Nosema ceranae. Microbes Environ. 34, 226–233 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  134. Diaz, T., Del-Val, E., Ayala, R. & Larsen, J. Alterations in honey bee gut microorganisms caused by Nosema spp. and pest control methods. Pest Manag. Sci. 75, 835–843 (2019).

    Article  CAS  PubMed  Google Scholar 

  135. Cuesta-Maté, A. et al. Resistance and vulnerability of honeybee (Apis mellifera) gut bacteria to commonly used pesticides. Front. Microbiol. 12, 717990 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  136. Hladik, M. L. et al. Year-round presence of neonicotinoid insecticides in tributaries to the Great Lakes, USA. Environ. Pollut. 235, 1022–1029 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Buszewski, B., Bukowska, M., Ligor, M. & Staneczko-Baranowska, I. A holistic study of neonicotinoids neuroactive insecticides—properties, applications, occurrence, and analysis. Environ. Sci. Pollut. Res. Int. 26, 34723–34740 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Liu, Y.-J. et al. Thiacloprid exposure perturbs the gut microbiota and reduces the survival status in honeybees. J. Hazard Mater. 389, 121818 (2020).

    Article  CAS  PubMed  Google Scholar 

  139. Castelli, L., Branchiccela, B., Zunino, P. & Antúnez, K. Insights into the effects of sublethal doses of pesticides glufosinate-ammonium and sulfoxaflor on honey bee health. Sci. Total Environ. 868, 161331 (2023).

    Article  CAS  PubMed  ADS  Google Scholar 

  140. Raymann, K. et al. Imidacloprid decreases honey bee survival rates but does not affect the gut microbiome. Appl. Environ. Microbiol. 84, e00545-18 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  141. Rothman, J. A., Russell, K. A., Leger, L., McFrederick, Q. S. & Graystock, P. The direct and indirect effects of environmental toxicants on the health of bumblebees and their microbiomes. Proc. Biol. Sci. 287, 20200980 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  142. Blot, N., Veillat, L., Rouzé, R. & Delatte, H. Glyphosate, but not its metabolite AMPA, alters the honeybee gut microbiota. PLoS ONE 14, e0215466 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Motta, E. V. S., Raymann, K. & Moran, N. A. Glyphosate perturbs the gut microbiota of honey bees. Proc. Natl Acad. Sci. USA 115, 10305–10310 (2018).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  144. Castelli, L. et al. Impact of chronic exposure to sublethal doses of glyphosate on honey bee immunity, gut microbiota and infection by pathogens. Microorganisms 9, 845 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Almasri, H., Liberti, J., Brunet, J.-L., Engel, P. & Belzunces, L. P. Mild chronic exposure to pesticides alters physiological markers of honey bee health without perturbing the core gut microbiota. Sci. Rep. 12, 4281 (2022).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  146. Thompson, H. M. et al. Evaluating exposure and potential effects on honeybee brood (Apis mellifera) development using glyphosate as an example. Integr. Environ. Assess. Manag. 10, 463–470 (2014).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  147. Motta, E. V. S. & Moran, N. A. The effects of glyphosate, pure or in herbicide formulation, on bumble bees and their gut microbial communities. Sci. Total Environ. 872, 162102 (2023).

    Article  CAS  PubMed  ADS  Google Scholar 

  148. Cullen, M. G., Bliss, L., Stanley, D. A. & Carolan, J. C. Investigating the effects of glyphosate on the bumblebee proteome and microbiota. Sci. Total Environ. 864, 161074 (2023).

    Article  CAS  PubMed  ADS  Google Scholar 

  149. Helander, M. et al. Glyphosate and a glyphosate-based herbicide affect bumblebee gut microbiota. FEMS Microbiol. Ecol. 99, fiad065 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  150. Motta, E. V. S., Powell, J. E. & Moran, N. A. Glyphosate induces immune dysregulation in honey bees. Anim. Microbiome 4, 16 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Motta, E. V. S. et al. Oral or topical exposure to glyphosate in herbicide formulation impacts the gut microbiota and survival rates of honey bees. Appl. Environ. Microbiol. 86, 116–126 (2020).

    Article  Google Scholar 

  152. Tan, S. et al. Effects of glyphosate exposure on honeybees. Environ. Toxicol. Pharmacol. 90, 103792 (2022).

    Article  CAS  PubMed  Google Scholar 

  153. Pettis, J. S. et al. Crop pollination exposes honey bees to pesticides which alters their susceptibility to the gut pathogen Nosema ceranae. PLoS ONE 8, e70182 (2013).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  154. Al Naggar, Y., Singavarapu, B., Paxton, R. J. & Wubet, T. Bees under interactive stressors: the novel insecticides flupyradifurone and sulfoxaflor along with the fungicide azoxystrobin disrupt the gut microbiota of honey bees and increase opportunistic bacterial pathogens. Sci. Total. Environ. 849, 157941 (2022).

    Article  CAS  PubMed  ADS  Google Scholar 

  155. Ludvigsen, J., Amdam, G. V., Rudi, K. & L’Abée-Lund, T. M. Detection and characterization of streptomycin resistance (strA-strB) in a honeybee gut symbiont (Snodgrassella alvi) and the associated risk of antibiotic resistance transfer. Microb. Ecol. 76, 588–591 (2018).

    Article  CAS  PubMed  ADS  Google Scholar 

  156. Huang, S. K. et al. Influence of feeding type and Nosema ceranae infection on the gut microbiota of Apis cerana workers. mSystems 3, e00177-18 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  157. Castelli, L. et al. Impact of nutritional stress on honeybee gut microbiota, immunity, and Nosema ceranae Infection. Microb. Ecol. 80, 908–919 (2020).

    Article  CAS  PubMed  ADS  Google Scholar 

  158. Powell, J. E. et al. The microbiome and gene expression of honey bee workers are affected by a diet containing pollen substitutes. PLoS ONE 18, e0286070 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Chmiel, J. A., Pitek, A. P., Burton, J. P., Thompson, G. J. & Reid, G. Meta-analysis on the effect of bacterial interventions on honey bee productivity and the treatment of infection. Apidologie 52, 960–972 (2021).

    Article  Google Scholar 

  160. Damico, M. E., Beasley, B., Greenstein, D. & Raymann, K. A need for stronger regulation: commercially sold probiotics for honey bees do not live up to their claims. Preprint at bioRxiv https://doi.org/10.1101/2023.09.13.557574 (2023).

  161. Daisley, B. A. et al. Novel probiotic approach to counter Paenibacillus larvae infection in honey bees. ISME J. 14, 476–491 (2020).

    Article  CAS  PubMed  Google Scholar 

  162. Stephan, J. G. et al. Honeybee-specific lactic acid bacterium supplements have no effect on American foulbrood-infected honeybee colonies. Appl. Environ. Microbiol. 85, e00606–e00619 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  163. Lamei, S. et al. Feeding honeybee colonies with honeybee-specific lactic acid bacteria (Hbs-LAB) does not affect colony-level Hbs-LAB composition or Paenibacillus larvae spore levels, although American foulbrood affected colonies harbor a more diverse Hbs-LAB community. Microb. Ecol. 79, 743–755 (2020).

    Article  PubMed  ADS  Google Scholar 

  164. Daisley, B. A. et al. Delivery mechanism can enhance probiotic activity against honey bee pathogens. ISME J. 17, 1382–1395 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  165. Leonard, S. P. et al. Genetic engineering of bee gut microbiome bacteria with a toolkit for modular assembly of broad-host-range plasmids. ACS Synth. Biol. 7, 1279–1290 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Lariviere, P. J., Leonard, S. P., Horak, R. D., Powell, J. E. & Barrick, J. E. Honey bee functional genomics using symbiont-mediated RNAi. Nat. Protoc. 18, 902–928 (2023).

    Article  CAS  PubMed  Google Scholar 

  167. Leonard, S. P. et al. Engineered symbionts activate honey bee immunity and limit pathogens. Science 367, 573–576 (2020).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  168. Wang, Y., Kaftanoglu, O., Brent, C. S., Page, R. E. Jr & Amdam, G. V. Starvation stress during larval development facilitates an adaptive response in adult worker honey bees (Apis mellifera L.). J. Exp. Biol. 219, 949–959 (2016).

    Article  PubMed  Google Scholar 

  169. Faita, M. R., Cardozo, M. M., Amandio, D. T. T., Orth, A. I. & Nodari, R. O. Glyphosate-based herbicides and Nosema sp. microsporidia reduce honey bee (Apis mellifera L.) survivability under laboratory conditions. J. Apic. Res. 59, 332–342 (2020).

    Article  Google Scholar 

  170. Kwong, W. K., Zheng, H. & Moran, N. A. Convergent evolution of a modified, acetate-driven TCA cycle in bacteria. Nat. Microbiol. 2, 17067 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the US NIH (award R35GM131738) and the USDA National Institute of Food and Agriculture (award 2018-67013-27540) to N.A.M.

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    Erick V. S. Motta & Nancy A. Moran

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N.A.M. is an author on a patent application (US20220152128A1) for using native bee gut bacteria as bee probiotics. E.V.S.M. declares no competing interests.

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Motta, E.V.S., Moran, N.A. The honeybee microbiota and its impact on health and disease. Nat Rev Microbiol 22, 122–137 (2024). https://doi.org/10.1038/s41579-023-00990-3

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