Honey bees as models for gut microbiota research

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The gut microbiota of the honey bee (Apis mellifera) offers several advantages as an experimental system for addressing how gut communities affect their hosts and for exploring the processes that determine gut community composition and dynamics. A small number of bacterial species dominate the honey bee gut community. These species are restricted to bee guts and can be grown axenically and genetically manipulated. Large numbers of microbiota-free hosts can be economically reared and then inoculated with single isolates or defined communities to examine colonization patterns and effects on host phenotypes. Honey bees have been studied extensively, due to their importance as agricultural pollinators and as models for sociality. Because of this history of bee research, the physiology, development, and behavior of honey bees is relatively well understood, and established behavioral and phenotypic assays are available. To date, studies on the honey bee gut microbiota show that it affects host nutrition, weight gain, endocrine signaling, immune function, and pathogen resistance, while perturbation of the microbiota can lead to reduced host fitness. As in humans, the microbiota is concentrated in the distal part of the gut, where it contributes to digestion and fermentation of plant cell wall components. Much like the human gut microbiota, many bee gut bacteria are specific to the bee gut and can be directly transmitted between individuals through social interaction. Although simpler than the human gut microbiota, the bee gut community presents opportunities to understand the processes that govern the assembly of specialized gut communities as well as the routes through which gut communities impact host biology.

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Fig. 1: Similarities (center) and differences (right and left sides) between the gut microbiota of humans and the gut microbiota of honey bees.
Fig. 2: Design of gnotobiotic honey bee studies.
Fig. 3: Summary of the effects of the honey bee gut microbiota on host and the gut microbial metabolism.


  1. 1.

    Ghannoum, M. A. et al. Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. PLoS Pathog. 6, e1000713 (2010).

  2. 2.

    Findley, K. et al. Topographic diversity of fungal and bacterial communities in human skin. Nature 498, 367–370 (2013).

  3. 3.

    Drell, T. et al. Characterization of the vaginal micro- and mycobiome in asymptomatic reproductive-age Estonian women. PLoS One 8, e54379 (2013).

  4. 4.

    Donaldson, G. P., Lee, S. M. & Mazmanian, S. K. Gut biogeography of the bacterial microbiota. Nat. Rev. Microbiol. 14, 20–32 (2016).

  5. 5.

    Trompette, A. et al. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat. Med. 20, 159–166 (2014).

  6. 6.

    Rooks, M. G. & Garrett, W. S. Gut microbiota, metabolites and host immunity. Nat. Rev. Immunol. 16, 341–352 (2016).

  7. 7.

    Kamada, N., Chen, G. Y., Inohara, N. & Núñez, G. Control of pathogens and pathobionts by the gut microbiota. Nat. Immunol. 14, 685–690 (2013).

  8. 8.

    Qin, N. et al. Alterations of the human gut microbiome in liver cirrhosis. Nature 513, 59–64 (2014).

  9. 9.

    Zitvogel, L. et al. Cancer and the gut microbiota: an unexpected link. Sci. Transl. Med. 7, 271ps1 (2015).

  10. 10.

    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).

  11. 11.

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

  12. 12.

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

  13. 13.

    Lee, F. J., Rusch, D. B., Stewart, F. J., Mattila, H. R. & Newton, I. L. Saccharide breakdown and fermentation by the honey bee gut microbiome. Environ. Microbiol. 17, 796–815 (2015).

  14. 14.

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

  15. 15.

    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).

  16. 16.

    Sabree, Z. L., Hansen, A. K. & Moran, N. A. Independent studies using deep sequencing resolve the same set of core bacterial species dominating gut communities of honey bees. PLoS One 7, e41250 (2012).

  17. 17.

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

  18. 18.

    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).

  19. 19.

    Bonilla-Rosso, G. & Engel, P. Functional roles and metabolic niches in the honey bee gut microbiota. Curr. Opin. Microbiol. 43, 69–76 (2018).

  20. 20.

    Anderson, K. E. & Ricigliano, V. A. Honey bee gut dysbiosis: a novel context of disease ecology. Curr. Opin. Insect Sci. 22, 125–132 (2017).

  21. 21.

    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).

  22. 22.

    von Frisch, K. The Dance Language and Orientation of Bees (Harvard University Press, Cambridge, MA, USA, 1967).

  23. 23.

    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).

  24. 24.

    Page, R. E. Jr. & Peng, C. Y. Aging and development in social insects with emphasis on the honey bee, Apis mellifera L. Exp. Gerontol. 36, 695–711 (2001).

  25. 25.

    Shpigler, H. Y. et al. Deep evolutionary conservation of autism-related genes. Proc. Natl. Acad. Sci. USA 114, 9653–9658 (2017).

  26. 26.

    Gallai, N., Salles, J. M., Settele, J. & Vaissiere, B. E. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol. Econ. 68, 810–821 (2009).

  27. 27.

    Stokstad, E. The case of the empty hives. Science 316, 970–972 (2007).

  28. 28.

    Honeybee Genome Sequencing Consortium. Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443, 931–949 (2006).

  29. 29.

    Wallberg, A. et al. A worldwide survey of genome sequence variation provides insight into the evolutionary history of the honeybee Apis mellifera. Nat. Genet. 46, 1081–1088 (2014).

  30. 30.

    Nelson, R. M., Wallberg, A., Simões, Z. L. P., Lawson, D. J. & Webster, M. T. Genomewide analysis of admixture and adaptation in the Africanized honeybee. Mol. Ecol. 26, 3603–3617 (2017).

  31. 31.

    Goodman, A. L. et al. Extensive personal human gut microbiota culture collections characterized and manipulated in gnotobiotic mice. Proc. Natl. Acad. Sci. USA 108, 6252–6257 (2011).

  32. 32.

    Ridaura, V. K. et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 341, 1241214 (2013).

  33. 33.

    Hamilton, D. R. & Bradley, R. E. Sr. An integrated system for the production of gnotobiotic Anopheles quadrimaculatus. J. Invertebr. Pathol. 30, 318–324 (1977).

  34. 34.

    Dillon, R. & Charnley, K. Mutualism between the desert locust Schistocerca gregaria and its gut microbiota. Res. Microbiol. 153, 503–509 (2002).

  35. 35.

    Oertel, E. Metamorphosis in the honeybee. J. Morphol. 50, 295–339 (1930).

  36. 36.

    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).

  37. 37.

    Bodenheimer, F. S. Studies in animal populations. II. Seasonal population-trends of the honey-bee. Q. Rev. Biol. 12, 406–425 (1937).

  38. 38.

    Winston, M. L. The Biology of the Honey Bee (Harvard University Press, Cambridge, MA, USA, 1987).

  39. 39.

    Hroncova, Z. et al. Variation in honey bee gut microbial diversity affected by ontogenetic stage, age and geographic location. PLoS One 10, e0118707 (2015).

  40. 40.

    Vojvodic, S., Rehan, S. M. & Anderson, K. E. Microbial gut diversity of Africanized and European honey bee larval instars. PLoS One 8, e72106 (2013).

  41. 41.

    Nelson, J. A., Lineburg, B. & Sturtevant, A. P. Growth and Feeding of Honeybee Larvae (US Department of Agriculture, Washington, DC, USA, 1924).

  42. 42.

    Jay, S. C. The development of honeybees in their cells. J. Apic. Res. 2, 117–134 (2015).

  43. 43.

    White, P. B. The normal bacterial flora of the bee. J. Pathol. Bacteriol. 24, 64–78 (1921).

  44. 44.

    Gilliam, M. Microbial sterility of the intestinal content of the immature honey bee, Apis mellifera. Ann. Entomol. Soc. Am. 64, 315–316 (1971).

  45. 45.

    Schwarz, R. S., Moran, N. A. & Evans, J. D. Early gut colonizers shape parasite susceptibility and microbiota composition in honey bee workers. Proc. Natl. Acad. Sci. USA 113, 9345–9350 (2016).

  46. 46.

    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).

  47. 47.

    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).

  48. 48.

    Schmehl, D. R., Tomé, H. V. V., Mortensen, A. N., Martins, G. F. & Ellis, J. D. Protocol for the in vitro rearing of honey bee (Apis mellifera L.) workers. J. Apic. Res. 55, 113–129 (2016).

  49. 49.

    Crane, E. Bees and Beekeeping: Science, Practice, and World Resources (Comstock Pub. Associates, Ithaca, NY, USA, 1990).

  50. 50.

    Kasiotis, K. M., Anagnostopoulos, C., Anastasiadou, P. & Machera, K. Pesticide residues in honeybees, honey and bee pollen by LC–MS/MS screening: reported death incidents in honeybees. Sci. Total Environ. 485–486, 633–642 (2014).

  51. 51.

    Rumkee, J. C. O., Becher, M. A., Thorbek, P. & Osborne, J. L. Modeling effects of honeybee behaviors on the distribution of pesticide in nectar within a hive and resultant in-hive exposure. Environ. Sci. Technol. 51, 6908–6917 (2017).

  52. 52.

    Kwong, W. K. et al. Dynamic microbiome evolution in social bees. Sci. Adv. 3, e1600513 (2017).

  53. 53.

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

  54. 54.

    Disayathanoowat, T., Young, J. P., Helgason, T. & Chantawannakul, P. T-RFLP analysis of bacterial communities in the midguts of Apis mellifera and Apis cerana honey bees in Thailand. FEMS Microbiol. Ecol. 79, 273–281 (2012).

  55. 55.

    Ahn, K., Xie, X., Riddle, J., Pettis, J. & Huang, Z. Y. Effects of long distance transportation on honey bee physiology. Psyche 2012, 9 (2012).

  56. 56.

    Jeyaprakash, A., Hoy, M. A. & Allsopp, M. H. Bacterial diversity in worker adults of Apis mellifera capensis and Apis mellifera scutellata (Insecta: Hymenoptera) assessed using 16S rRNA sequences. J. Invertebr. Pathol. 84, 96–103 (2003).

  57. 57.

    Corby-Harris, V. et al. Origin and effect of α2.2 Acetobacteraceae in honey bee larvae and description of Parasaccharibacter apium gen. nov., sp. nov. Appl. Environ. Microbiol. 80, 7460–7472 (2014).

  58. 58.

    Mohr, K. I. & Tebbe, C. C. Diversity and phylotype consistency of bacteria in the guts of three bee species (Apoidea) at an oilseed rape field. Environ. Microbiol. 8, 258–272 (2006).

  59. 59.

    Anderson, K. E., Rodrigues, P. A., Mott, B. M., Maes, P. & Corby-Harris, V. Ecological succession in the honey bee gut: shift in Lactobacillus strain dominance during early adult development. Microb. Ecol. 71, 1008–1019 (2016).

  60. 60.

    Anderson, K. E. et al. Microbial ecology of the hive and pollination landscape: bacterial associates from floral nectar, the alimentary tract and stored food of honey bees (Apis mellifera). PLoS One 8, e83125 (2013).

  61. 61.

    Olofsson, T. C., Alsterfjord, M., Nilson, B., Butler, E. & 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).

  62. 62.

    Rokop, Z. P., Horton, M. A. & Newton, I. L. Interactions between cooccurring lactic acid bacteria in honey bee hives. Appl. Environ. Microbiol. 81, 7261–7270 (2015).

  63. 63.

    Milani, C. et al. Phylotype-level profiling of lactobacilli in highly complex environments by means of an ITS-based metagenomic approach. Appl. Environ. Microbiol. 84, e00706–18 (2018).

  64. 64.

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

  65. 65.

    Segers, F. H., Kešnerová, L., Kosoy, M. & Engel, P. Genomic changes associated with the evolutionary transition of an insect gut symbiont into a blood-borne pathogen. ISME J. 11, 1232–1244 (2017).

  66. 66.

    Rangberg, A., Diep, D. B., Rudi, K. & Amdam, G. V. Paratransgenesis: an approach to improve colony health and molecular insight in honey bees (Apis mellifera)? Integr. Comp. Biol. 52, 89–99 (2012).

  67. 67.

    Rangberg, A., Mathiesen, G., Amdam, G. V. & Diep, D. B. The paratransgenic potential of Lactobacillus kunkeei in the honey bee Apis mellifera. Benef. Microbes 6, 513–523 (2015).

  68. 68.

    Sonnenburg, J. L. Microbiome engineering. Nature 518, S10 (2015).

  69. 69.

    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).

  70. 70.

    Ihle, K. E., Baker, N. A. & Amdam, G. V. Insulin-like peptide response to nutritional input in honey bee workers. J. Insect Physiol. 69, 49–55 (2014).

  71. 71.

    Kannan, K. & Fridell, Y. W. C. Functional implications of Drosophila insulin-like peptides in metabolism, aging, and dietary restriction. Front. Physiol. 4, 288 (2013).

  72. 72.

    Shin, S. C. et al. Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science 334, 670–674 (2011).

  73. 73.

    Nelson, C. M., Ihle, K. E., Fondrk, M. K., Page, R. E. & Amdam, G. V. The gene vitellogenin has multiple coordinating effects on social organization. PLoS Biol. 5, e62 (2007).

  74. 74.

    Kešnerová, L. et al. Disentangling metabolic functions of bacteria in the honey bee gut. PLoS Biol. 15, e2003467 (2017).

  75. 75.

    Harris, J. W. & Woodring, J. Effects of stress, age, season, and source colony on levels of octopamine, dopamine and serotonin in the honey bee (Apis mellifera L.) brain. J. Insect Physiol. 38, 29–35 (1992).

  76. 76.

    Flint, H. J., Scott, K. P., Louis, P. & Duncan, S. H. The role of the gut microbiota in nutrition and health. Nat. Rev. Gastroenterol. Hepatol. 9, 577–589 (2012).

  77. 77.

    Flint, H. J., Bayer, E. A., Rincon, M. T., Lamed, R. & White, B. A. Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat. Rev. Microbiol. 6, 121–131 (2008).

  78. 78.

    Frias, B. E. D., Barbosa, C. D. & Lourenco, A. P. Pollen nutrition in honey bees (Apis mellifera): impact on adult health. Apidologie 47, 15–25 (2016).

  79. 79.

    Mollet, J. C., Leroux, C., Dardelle, F. & Lehner, A. Cell wall composition, biosynthesis and remodeling during pollen tube growth. Plants 2, 107–147 (2013).

  80. 80.

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

  81. 81.

    Koch, H., Abrol, D. P., Li, J. & Schmid-Hempel, P. Diversity and evolutionary patterns of bacterial gut associates of corbiculate bees. Mol. Ecol. 22, 2028–2044 (2013).

  82. 82.

    Fürst, M. A., McMahon, D. P., Osborne, J. L., Paxton, R. J. & Brown, M. J. Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature 506, 364–366 (2014).

  83. 83.

    Powell, E., Ratnayeke, N. & Moran, N. A. Strain diversity and host specificity in a specialized gut symbiont of honeybees and bumblebees. Mol. Ecol. 25, 4461–4471 (2016).

  84. 84.

    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).

  85. 85.

    Goodman, A. L. et al. Identifying genetic determinants needed to establish a human gut symbiont in its habitat. Cell Host Microbe 6, 279–289 (2009).

  86. 86.

    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).

  87. 87.

    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).

  88. 88.

    Tang, H. Regulation and function of the melanization reaction in Drosophila. Fly 3, 105–111 (2009).

  89. 89.

    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).

  90. 90.

    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).

  91. 91.

    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).

  92. 92.

    Moeller, A. H. et al. Cospeciation of gut microbiota with hominids. Science 353, 380–382 (2016).

  93. 93.

    Tung, J. et al. Social networks predict gut microbiome composition in wild baboons. eLife 4, 305224 (2015).

  94. 94.

    Wong, A. C., Chaston, J. M. & Douglas, A. E. The inconstant gut microbiota of Drosophila species revealed by 16S rRNA gene analysis. ISME J. 7, 1922–1932 (2013).

  95. 95.

    Tol, van, S. & Dimopoulos, G . In: A. S, Raikhel ed. Advances in Insect Physiology 51, 243–291 (Academic Press: Cambridge, MA, USA, 2016).

  96. 96.

    Hammer, T. J., Janzen, D. H., Hallwachs, W., Jaffe, S. P. & Fierer, N. Caterpillars lack a resident gut microbiome. Proc. Natl. Acad. Sci. USA 114, 9641–9646 (2017).

  97. 97.

    McFrederick, Q. S. et al. Flowers and wild megachilid bees share microbes. Microb. Ecol. 73, 188–200 (2017).

  98. 98.

    Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature 486, 207–214 (2012).

  99. 99.

    Engel, P., Stepanauskas, R. & Moran, N. A. Hidden diversity in honey bee gut symbionts detected by single-cell genomics. PLoS Genet. 10, e1004596 (2014).

  100. 100.

    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).

  101. 101.

    Russell, A. B. et al. A type VI secretion-related pathway in Bacteroidetes mediates interbacterial antagonism. Cell Host Microbe 16, 227–236 (2014).

  102. 102.

    Kwong, W. K., Steele, M. I. & Moran, N. A. Genome sequences of Apibacter spp., gut symbionts of Asian honey bees. Genome Biol. Evol. 10, 1174–1179 (2018).

  103. 103.

    Carlucci, C., Petrof, E. O. & Allen-Vercoe, E. Fecal microbiota-based therapeutics for recurrent Clostridium difficile infection, ulcerative colitis and obesity. EBioMedicine 13, 37–45 (2016).

  104. 104.

    Mountfort, D. O., Campbell, J. & Clements, K. D. Hindgut fermentation in three species of marine herbivorous fish. Appl. Environ. Microbiol. 68, 1374–1380 (2002).

  105. 105.

    Bauer, E. et al. Physicochemical conditions, metabolites and community structure of the bacterial microbiota in the gut of wood-feeding cockroaches (Blaberidae: Panesthiinae). FEMS Microbiol. Ecol. 91, 1–14 (2015).

  106. 106.

    Buchon, N., Broderick, N. A. & Lemaitre, B. Gut homeostasis in a microbial world: insights from Drosophila melanogaster. Nat. Rev. Microbiol. 11, 615–626 (2013).

  107. 107.

    Tegtmeier, D., Thompson, C. L., Schauer, C. & Brune, A. Oxygen affects gut bacterial colonization and metabolic activities in a gnotobiotic cockroach model. Appl. Environ. Microbiol. 82, 1080–1089 (2015).

  108. 108.

    Heinken, A. & Thiele, I. Anoxic conditions promote species-specific mutualism between gut microbes in silico. Appl. Environ. Microbiol. 81, 4049–4061 (2015).

  109. 109.

    Johnson, K. S. Oxygen levels in the gut lumens of herbivorous insects. J. Insect Physiol. 46, 897–903 (2000).

  110. 110.

    Cox, C. R. & Gilmore, M. S. Native microbial colonization of Drosophila melanogaster and its use as a model of Enterococcus faecalis pathogenesis. Infect. Immun. 75, 1565–1576 (2007).

  111. 111.

    Blaser, M. J. Antibiotic use and its consequences for the normal microbiome. Science 352, 544–545 (2016).

  112. 112.

    Reybroeck, W., Daeseleire, E., De Brabander, H. F. & Herman, L. Antimicrobials in beekeeping. Vet. Microbiol. 158, 1–11 (2012).

  113. 113.

    Evans, J. D. & Armstrong, T. Inhibition of the American foulbrood bacterium, Paenibacillus larvae larvae, by bacteria isolated from honey bees. J. Apic. Res. 44, 168–171 (2015).

  114. 114.

    Evans, J. D. & Spivak, M. Socialized medicine: individual and communal disease barriers in honey bees. J. Invertebr. Pathol. 103, S62–S72 (2010). (Suppl. 1).

  115. 115.

    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, e00377–12 (2012).

  116. 116.

    Ludvigsen, J., Porcellato, D., L’Abée-Lund, T. M., Amdam, G. V. & Rudi, K. Geographically widespread honeybee-gut symbiont subgroups show locally distinct antibiotic-resistant patterns. Mol. Ecol. 26, 6590–6607 (2017).

  117. 117.

    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. https://doi.org/10.1007/s00248-018-1171-7 (2018).

  118. 118.

    Thursby, E. & Juge, N. Introduction to the human gut microbiota. Biochem. J. 474, 1823–1836 (2017).

  119. 119.

    Crailsheim, K. et al. Standard methods for artificial rearing of Apis mellifera larvae. J. Apic. Res. 52, 1–16 (2013).

  120. 120.

    Bonoan, R. E., O’Connor, L. D. & Starks, P. T. Seasonality of honey bee (Apis mellifera) micronutrient supplementation and environmental limitation. J. Insect Physiol. 107, 23–28 (2018).

  121. 121.

    Ludvigsen, J. et al. Shifts in the midgut/pyloric microbiota composition within a honey bee apiary throughout a season. Microbes Environ. 30, 235–244 (2015).

  122. 122.

    Glenny, W. et al. Honey bee (Apis mellifera) colony health and pathogen composition in migratory beekeeping operations involved in California almond pollination. PLoS One 12, e0182814 (2017).

  123. 123.

    Zanni, V., Galbraith, D. A., Annoscia, D., Grozinger, C. M. & Nazzi, F. Transcriptional signatures of parasitization and markers of colony decline in Varroa-infested honey bees (Apis mellifera). Insect Biochem. Mol. Biol. 87, 1–13 (2017).

  124. 124.

    Laidlaw, H. H. Artificial insemination of the queen bee (Apis mellifera L.): morphological basis and results. J. Morphol. 74, 429–465 (1944).

  125. 125.

    Schulte, C., Theilenberg, E., Müller-Borg, M., Gempe, T. & Beye, M. Highly efficient integration and expression of piggyBac-derived cassettes in the honeybee (Apis mellifera). Proc. Natl. Acad. Sci. USA 111, 9003–9008 (2014).

  126. 126.

    Kohno, H., Suenami, S., Takeuchi, H., Sasaki, T. & Kubo, T. Production of knockout mutants by CRISPR/Cas9 in the European honeybee, Apis mellifera L. Zool. Sci. 33, 505–512 (2016).

  127. 127.

    Marco Antonio, D. S., Guidugli-Lazzarini, K. R., do Nascimento, A. M., Simões, Z. L. & Hartfelder, K. RNAi-mediated silencing of vitellogenin gene function turns honeybee (Apis mellifera) workers into extremely precocious foragers. Naturwissenschaften 95, 953–961 (2008).

  128. 128.

    Chen, Y. P. & Evans, J. D. Managed pollinator CAP coordinated agricultural project. A national research and extension initiative to reverse pollinator decline. RNAi in treating honey bee diseases. Am. Bee J. 152, 1171–1173 (2012).

  129. 129.

    Yu, N. et al. Delivery of dsRNA for RNAi in insects: an overview and future directions. Insect Sci. 20, 4–14 (2013).

  130. 130.

    Flenniken, M. L. & Andino, R. Non-specific dsRNA-mediated antiviral response in the honey bee. PLoS One 8, e77263 (2013).

  131. 131.

    Killer, J., Dubná, S., Sedláček, I. & Švec, P. Lactobacillus apis sp. nov., from the stomach of honeybees (Apis mellifera), having an in vitro inhibitory effect on the causative agents of American and European foulbrood. Int. J. Syst. Evol. Microbiol. 64, 152–157 (2014).

  132. 132.

    Bottacini, F. et al. Bifidobacterium asteroides PRL2011 genome analysis reveals clues for colonization of the insect gut. PLoS One 7, e44229 (2012).

  133. 133.

    Ellegaard, K. M. et al. Extensive intra-phylotype diversity in lactobacilli and bifidobacteria from the honeybee gut. BMC Genomics 16, 284 (2015).

  134. 134.

    Scardovi, V. & Trovatelli, L. D. New species of bifid bacteria from Apis mellifica L. and Apis indica F. A contribution to the taxonomy and biochemistry of the genus Bifidobacterium. Zentralbl. Bakteriol. Parasitenkd. Infektionskr. Hyg. 123, 64–88 (1969).

  135. 135.

    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).

  136. 136.

    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).

  137. 137.

    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).

  138. 138.

    Roh, S. W. et al. Phylogenetic characterization of two novel commensal bacteria involved with innate immune homeostasis in Drosophila melanogaster. Appl. Environ. Microbiol. 74, 6171–6177 (2008).

  139. 139.

    Kwong, W. K. & Moran, N. A. Apibacter adventoris gen. nov., sp. nov., a member of the phylum Bacteroidetes isolated from honey bees. Int. J. Syst. Evol. Microbiol. 66, 1323–1329 (2016).

  140. 140.

    Corby-Harris, V. & Anderson, K. E. Draft genome sequences of four Parasaccharibacter apium strains isolated from honey bees. Genome Announc. 6, e00165–18 (2018).

  141. 141.

    Endo, A. et al. Characterization and emended description of Lactobacillus kunkeei as a fructophilic lactic acid bacterium. Int. J. Syst. Evol. Microbiol. 62, 500–504 (2012).

  142. 142.

    Endo, A. & Okada, S. Reclassification of the genus Leuconostoc and proposals of Fructobacillus fructosus gen. nov., comb. nov., Fructobacillus durionis comb. nov., Fructobacillus ficulneus comb. nov. and Fructobacillus pseudoficulneus comb. nov. Int. J. Syst. Evol. Microbiol. 58, 2195–2205 (2008).

  143. 143.

    Chouaia, B. et al. Acetic acid bacteria genomes reveal functional traits for adaptation to life in insect guts. Genome Biol. Evol. 6, 912–920 (2014).

  144. 144.

    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).

  145. 145.

    Tian, B. & Moran, N. A. Genome sequence of Hafnia alvei bta3_1, a bacterium with antimicrobial properties isolated from honey bee gut. Genome Announc. 4, e00439–16 (2016).

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Zheng, H., Steele, M.I., Leonard, S.P. et al. Honey bees as models for gut microbiota research. Lab Anim 47, 317–325 (2018) doi:10.1038/s41684-018-0173-x

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