Gut microbial communities of social bees

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.

Abstract

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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Composition and spatial organization of bacterial communities in the honey bee gut.
Figure 2: Honey bee life history and associated changes in the gut microbiota.
Figure 3: Metabolic activities of the core bee gut microbiota.

References

  1. 1

    Engel, P. & Moran, N. A. The gut microbiota of insects — diversity in structure and function. FEMS Microbiol. Rev. 37, 699–735 (2013).

    Article  CAS  PubMed  Google Scholar 

  2. 2

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

    Article  CAS  Google Scholar 

  3. 3

    Hooper, L. V., Littman, D. R. & Macpherson, A. J. Interactions between the microbiota and the immune system. Science 336, 1268–1273 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. 4

    Arumugam, M. et al. Enterotypes of the human gut microbiome. Nature 473, 174–180 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. 5

    Schloissnig, S. et al. Genomic variation landscape of the human gut microbiome. Nature 493, 45–50 (2013).

    Article  CAS  PubMed  Google Scholar 

  6. 6

    Moeller, A. H. et al. Rapid changes in the gut microbiome during human evolution. Proc. Natl Acad. Sci. USA 111, 16431–16435 (2014).

    Article  CAS  PubMed  Google Scholar 

  7. 7

    Sankar, S. A., Lagier, J. C., Pontarotti, P., Raoult, D. & Fournier, P. E. The human gut microbiome, a taxonomic conundrum. Syst. Appl. Microbiol. 38, 276–286 (2015).

    Article  CAS  PubMed  Google Scholar 

  8. 8

    Chandler, J. A., Lang, J. M., Bhatnagar, S., Eisen, J. A. & Kopp, A. Bacterial communities of diverse Drosophila species: ecological context of a host–microbe model system. PLoS Genet. 7, e1002272 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. 9

    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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. 10

    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  Google Scholar 

  11. 11

    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  PubMed  Google Scholar 

  12. 12

    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). This metagenomic study reveals the broad set of functions that are attributable to each member of the gut microbial community in honey bees and provides the first evidence of extensive strain diversity within each species of the community; strains that are essentially identical in 16S rDNA sequences can be highly divergent at protein-coding loci.

    Article  PubMed  Google Scholar 

  13. 13

    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  Google Scholar 

  14. 14

    Powell, J. E., Martinson, V. G., Urban-Mead, K. & Moran, N. A. Routes of acquisition of the gut microbiota of Apis mellifera. Appl. Environ. Microbiol. 80, 7378–7387 (2014). In this study, the transmission routes and temporal progression of bacterial colonization in the gut of adult worker bees were determined through the use of experimental treatments and deep 16S rDNA sequencing.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. 15

    Engel, P. et al. Standard methods for research on Apis mellifera gut symbionts. J. Apic. Res. 52, 1–24 (2013).

    Article  Google Scholar 

  16. 16

    Cox-Foster, D. L. et al. A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318, 283–287 (2007). Large-scale honey bee deaths occurred in 2006–2007: this study uses early next-generation sequencing technology to identify causative agents. Although bee deaths could not be attributed to a single disease, this analysis reveals the widespread presence of the core members of the bacterial gut community across diverse populations of honey bees.

    Article  CAS  PubMed  Google Scholar 

  17. 17

    Genersch, E. Honey bee pathology: current threats to honey bees and beekeeping. Appl. Microbiol. Biotechnol. 87, 87–97 (2010).

    Article  CAS  PubMed  Google Scholar 

  18. 18

    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).

    Article  CAS  PubMed  Google Scholar 

  19. 19

    Babendreier, D., Joller, D., Romeis, J., Bigler, F. & Widmer, F. Bacterial community structures in honeybee intestines and their response to two insecticidal proteins. FEMS Microbiol. Ecol. 59, 600–610 (2007).

    Article  CAS  PubMed  Google Scholar 

  20. 20

    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 

  21. 21

    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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. 22

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. 23

    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 

  24. 24

    Scardovi, V. & Trovatelli, D. New species of bifidobacteria 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).

    CAS  PubMed  Google Scholar 

  25. 25

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. 26

    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 

  27. 27

    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  CAS  PubMed  Google Scholar 

  28. 28

    Corby-Harris, V. et al. Origin and effect of Alpha 2.2 Acetobacteraceae in honey bee larvae and description of Parasaccharibacter apium gen. nov., sp. nov. Appl. Environ. Microbiol. 80, 7460–7472 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. 29

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

    Article  CAS  PubMed  Google Scholar 

  30. 30

    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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. 31

    Anderson, K. E. et al. Hive-stored pollen of honey bees: many lines of evidence are consistent with pollen preservation, not nutrient conversion. Mol. Ecol. 23, 5904–5917 (2014). It has long been suspected that hive-stored pollen was gradually degraded into a more nutritious food source by microbial action. However, this study finds few bacteria in stored pollen, which implies that digestion occurs in the worker gut.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. 32

    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  CAS  PubMed  PubMed Central  Google Scholar 

  33. 33

    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). The sequencing of S. alvi and G. apicola isolates from honey bees and bumble bees indicates that they occupy distinct metabolic niches and have diverse gene sets. In vivo experiments demonstrate barriers to host-switching for S. alvi strains, which suggests specialization to hosts.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. 34

    McFrederick, Q. S. et al. Environment or kin: whence do bees obtain acidophilic bacteria? Mol. Ecol. 21, 1754–1768 (2012).

    Article  PubMed  Google Scholar 

  35. 35

    McFrederick, Q. S. et al. Specificity between lactobacilli and hymenopteran hosts is the exception rather than the rule. Appl. Environ. Microbiol. 79, 1803–1812 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. 36

    McFrederick, Q. S., Wcislo, W. T., Hout, M. C. & Mueller, U. G. Host species and developmental stage, but not host social structure, affects bacterial community structure in socially polymorphic bees. FEMS Microbiol. Ecol. 88, 398–406 (2014). Although sociality seems to be key to the transmission of microbiota in corbiculate bees, the same is not found to be true for halictid bees in this study, as their gut microbial communities are dominated by environmentally acquired bacteria.

    Article  CAS  PubMed  Google Scholar 

  37. 37

    Ahn, J. H. et al. Pyrosequencing analysis of the bacterial communities in the guts of honey bees Apis Cerana and Apis Mellifera in Korea. J. Microbiol. 50, 735–745 (2012).

    Article  PubMed  Google Scholar 

  38. 38

    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).

    Article  CAS  PubMed  Google Scholar 

  39. 39

    Koch, H. & Schmid-Hempel, P. Bacterial communities in central European bumblebees: low diversity and high specificity. Microb. Ecol. 62, 121–213 (2011).

    Article  PubMed  Google Scholar 

  40. 40

    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).

    Article  CAS  PubMed  Google Scholar 

  41. 41

    Yoshiyama, M. & Kimura, K. Bacteria in the gut of Japanese honeybee, Apis cerana japonica, and their antagonistic effect against Paenibacillus larvae, the causal agent of American foulbrood. J. Invertebr. Pathol. 102, 91–96 (2009).

    Article  PubMed  Google Scholar 

  42. 42

    Lim, H. C., Chu, C.C., Seufferheld, M. J. & Cameron, S. A. Deep sequencing and ecological characterization of gut microbial communities of diverse bumble bee species. PLoS ONE 10, e0118566 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. 43

    Li, J. et al. Two gut community enterotypes recur in diverse bumblebee species. Curr. Biol. 25, R652–R653 (2015).

    Article  CAS  PubMed  Google Scholar 

  44. 44

    Saraithong, P., Li, Y., Saenphet, K., Chen, Z. & Chantawannakul, P. Bacterial community structure in Apis florea larvae analyzed by denaturing gradient gel electrophoresis and 16S rRNA gene sequencing. Insect Sci. 22, 606–618 (2015).

    Article  CAS  PubMed  Google Scholar 

  45. 45

    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).

    Article  CAS  PubMed  Google Scholar 

  46. 46

    Cariveau, D. P., Powell, J. E., Koch, H., Winfree, R. & Moran, N. A. Variation in gut microbial communities and its association with pathogen infection in wild bumble bees (Bombus) ISME J. 12, 2369–2379 (2014).

    Article  CAS  Google Scholar 

  47. 47

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. 48

    Martinson, V. G., Magoc, T., Koch, H., Salzberg, S. L. & Moran, N. A. Genomic features of a bumble bee symbiont reflect its host environment. Appl. Environ. Microbiol. 80, 3793–3803 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. 49

    Killer, J. et al. Bombiscardovia coagulans gen. nov., sp. nov., a new member of the family Bifidobacteriaceae isolated from the digestive tract of bumblebees. Syst. Appl. Microbiol. 33, 359–366 (2010).

    Article  CAS  PubMed  Google Scholar 

  50. 50

    Killer, J. et al. Bifidobacterium actinocoloniiforme sp. nov. and Bifidobacterium bohemicum sp. nov., from the bumblebee digestive tract. Int. J. Syst. Evol. Microbiol. 61, 1315–1321 (2011).

    Article  CAS  PubMed  Google Scholar 

  51. 51

    Wu, M. et al. Characterization of bifidobacteria in the digestive tract of the Japanese honeybee, Apis cerana japonica. J. Invertebr. Pathol. 112, 88–93 (2013).

    Article  CAS  PubMed  Google Scholar 

  52. 52

    Lugli, G. A. et al. Investigation of the evolutionary development of the genus Bifidobacterium by comparative genomics. Appl. Environ. Microbiol. 80, 6383–6394 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. 53

    Praet, J. et al. Bifidobacterium commune sp. nov. isolated from the bumble bee gut. Antonie Van Leeuwenhoek 107, 1307–1313 (2015).

    Article  CAS  PubMed  Google Scholar 

  54. 54

    Praet, J. et al. Novel lactic acid bacteria isolated from the bumble bee gut: Convivina intestini gen. nov., sp. nov. Lactobacillus bombicola sp. nov., and Weissella bombi sp. nov. Antonie Van Leeuwenhoek 107, 1337–1349 (2015).

    Article  CAS  PubMed  Google Scholar 

  55. 55

    Ellegaard, K. M., Tamarit, D. & Javelind, E. Extensive intra-phylotype diversity in lactobacilli and bifidobacteria from the honeybee gut. BMC Genomics 16, 284 (2015). This study conducts genomic analysis of Lactobacillus strains and Bifidobacterium spp. from honey bees and finds extensive variation in gene content between different isolates, particularly for genes that affect carbohydrate use and the biosynthesis of exopolysaccharides.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. 56

    Kwong, W. K. & Moran, N. A. Evolution of host specialization in gut microbes: the bee gut as a model. Gut Microbes 6, 214–220 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  57. 57

    Tamarit, D. et al. Functionally structured genomes in Lactobacillus kunkeei colonizing the honey crop and food products of honeybees and stingless bees. Genome Biol. Evol. 7, 1455–1473 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. 58

    Mohr, K. I. & Tebbe, C. C. Field study results on the probability and risk of a horizontal gene transfer from transgenic herbicide-resistant oilseed rape pollen to gut bacteria of bees. Appl. Microbiol. Biotechnol. 75, 573–582 (2007).

    Article  CAS  PubMed  Google Scholar 

  59. 59

    Li, L. et al. Bombella intestini gen. nov., sp. nov., an acetic acid bacterium isolated from bumble bee crop. Int. J. Syst. Evol. Microbiol. 65, 267–273 (2015).

    Article  CAS  PubMed  Google Scholar 

  60. 60

    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).

    Article  CAS  PubMed  Google Scholar 

  61. 61

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. 62

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. 63

    Tarpy, D. R., Mattila, H. R. & Newton, I. L. Development of the honey bee gut microbiome throughout the queen-rearing process. Appl. Environ. Microbiol. 81, 3182–3191 (2015). In this study, honey bee queens are sampled throughout their development, showing that queens have a different gut microbiome composition from that of workers.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. 64

    Yun, J. H. et al. Insect gut bacterial diversity determined by environmental habitat, diet, developmental stage, and phylogeny of host. Appl. Environ. Microbiol. 80, 5254–5264 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. 65

    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).

    Article  PubMed  PubMed Central  Google Scholar 

  66. 66

    Tozkar, C. Ö., Kence, M., Kence, A., Huang, Q. & Evans, J. D. Metatranscriptomic analyses of honey bee colonies. Front. Genet. 6, 100 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. 67

    Cho, I. & Blaser, M. J. The human microbiome: at the interface of health and disease. Nat. Rev. Genet. 13, 260–270 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. 68

    Koch, H., Cisarovsky, G. & Schmid-Hempel, P. Ecological effects on gut bacterial communities in wild bumblebee colonies. J. Anim. Ecol. 81, 1202–1210 (2012).

    Article  PubMed  Google Scholar 

  69. 69

    Meeus, I. et al. 16S rRNA amplicon sequencing demonstrates that indoor-reared bumblebees (Bombus terrestris) harbor a core subset of bacteria normally associated with the wild host. PLoS ONE 10, e0125152 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. 70

    Parmentier, L., Meeus, I., Mosallanejad, H., de Graaf, D. C. & Smagghe, G. Plasticity in the gut microbial community and uptake of Enterobacteriaceae (Gammaproteobacteria) in Bombus terrestris bumblebees' nests when reared indoors and moved to an outdoor environment. Apidologie 47, 237–250 (2015).

    Article  Google Scholar 

  71. 71

    Jefferson, J. M., Dolstad, H. A., Sivalingam, M. D. & Snow, J. W. Barrier immune effectors are maintained during transition from nurse to forager in the honey bee. PLoS ONE 8, e54097 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. 72

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

    Article  CAS  PubMed  Google Scholar 

  73. 73

    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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. 74

    Alippi, A. M., León, I. E. & López, A. C. Tetracycline-resistance encoding plasmids from Paenibacillus larvae, the causal agent of American foulbrood disease, isolated from commercial honeys. Int. Microbiol. 17, 49–61 (2014).

    CAS  PubMed  Google Scholar 

  75. 75

    Blaser, M. J. Missing Microbes: How the Overuse of Antibiotics Is Fueling Our Modern Plagues (Henry Holt, 2014).

    Google Scholar 

  76. 76

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. 77

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

  78. 78

    Killer, J., Dubná, S., Sedlác˘ek, I. & S˘vec, 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).

    Article  CAS  PubMed  Google Scholar 

  79. 79

    Killer, J. et al. Lactobacillus bombi sp. nov., from the digestive tract of laboratory-reared bumblebee queens (Bombus terrestris). Int. J. Syst. Evol. Microbiol. 64, 2611–2617 (2014).

    Article  CAS  PubMed  Google Scholar 

  80. 80

    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). This study shows that the infection of bumble bees by different strains of a trypanosomatid parasite is more dependent on the source of the gut microbiota than on host genotype, which suggests that bacteria in the guts of bees are undergoing a co-evolutionary 'arms race' with the parasites.

    Article  PubMed  Google Scholar 

  81. 81

    Butler, È. et al. Proteins of novel lactic acid bacteria from Apis mellifera mellifera: an insight into the production of known extra-cellular proteins during microbial stress. BMC Microbiol. 13, 235 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. 82

    Forsgren, E., Olofsson, T. C., Vásquez, A. & Fries, I. Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae. Apidologie 41, 99–108 (2009).

    Article  Google Scholar 

  83. 83

    Vásquez, A. et al. Symbionts as major modulators of insect health: lactic acid bacteria and honeybees. PLoS ONE 7, e33188 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. 84

    Schwarz, R. S., Huang, Q. & Evans, J. D. Hologenome theory and the honey bee pathosphere. Curr. Opin. Insect Sci. 10, 1–7 (2015).

    Article  PubMed  Google Scholar 

  85. 85

    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 

  86. 86

    Buchon, N., Broderick, N. A., Poidevin, M., Pradervand, S. & Lemaitre, B. Drosophila intestinal response to bacterial infection: activation of host defense and stem cell proliferation. Cell Host Microbe 5, 200–211 (2009).

    Article  CAS  PubMed  Google Scholar 

  87. 87

    Engel, P., Vizcaino, M. I. & Crawford, J. M. Gut symbionts from distinct hosts exhibit genotoxic activity via divergent colibactin biosynthetic pathways. Appl. Environ. Microbiol. 81, 1502–1512 (2015). This paper explores the intriguing honey bee gut bacterial species F. perrara , which synthesizes a complex peptide–polyketide that is homologous to colibactin, a tumorigenic compound that is produced by some strains of E. coli in the human gut.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. 88

    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 (2014).

    Article  CAS  PubMed  Google Scholar 

  89. 89

    Kwong, W. K., Mancenido, A. L. & Moran, N. A. Genome sequences of Lactobacillus sp. strains wkB8 and wkB10, members of the Firm-5 clade, from honey bee guts. Genome Announc. 13, e01176-14 (2014).

    Article  Google Scholar 

  90. 90

    Barker, R. J. & Lehner, Y. Acceptance and sustenance value of naturally occurring sugars fed to newly emerged adult workers of honey bees (Apis mellifera L.). J. Exp. Zool. 187, 277–285 (1974).

    Article  CAS  Google Scholar 

  91. 91

    Olofsson, T. C. & Alejandra Vásquez, A. Detection and identification of a novel lactic acid bacterial flora within the honey stomach of the honeybee Apis mellifera. Curr. Microbiol. 57, 356–363 (2008).

    Article  CAS  PubMed  Google Scholar 

  92. 92

    den Besten, G. et al. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J. Lipid Res. 54, 2325–2340 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. 93

    Brune, A. Symbiotic digestion of lignocellulose in termite guts. Nat. Rev. Microbiol. 12, 168–180 (2014).

    Article  CAS  PubMed  Google Scholar 

  94. 94

    Egert, M. et al. Structure and topology of microbial communities in the major gut compartments of Melolontha melolontha larvae (Coleoptera: Scarabaeidae). Appl. Environ. Microbiol. 71, 4556–4566 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. 95

    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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. 96

    Jojima, Y. et al. Saccharibacter floricola gen. nov., sp. nov., a novel osmophilic acetic acid bacterium isolated from pollen. Int. J. Syst. Evol. Microbiol. 54, 2263–2267 (2004).

    Article  CAS  PubMed  Google Scholar 

  97. 97

    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 

  98. 98

    Degnan, P. H. et al. Factors associated with the diversification of the gut microbial communities within chimpanzees from Gombe National Park. Proc. Natl Acad. Sci. USA 109, 13034–13039 (2012).

    Article  PubMed  Google Scholar 

  99. 99

    Song, S. J. et al. Cohabiting family members share microbiota with one another and with their dogs. eLife 2, e00458 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  100. 100

    Tung, J. et al. Social networks predict gut microbiome composition in wild baboons. eLife 4, e05224 (2015).

    Article  PubMed Central  Google Scholar 

  101. 101

    Favia, G. et al. Bacteria of the genus Asaia stably associate with Anopheles stephensi, an Asian malarial mosquito vector. Proc. Natl Acad. Sci. USA 104, 9047–9051 (2007).

    Article  CAS  PubMed  Google Scholar 

  102. 102

    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).

    Article  PubMed  Google Scholar 

  103. 103

    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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. 104

    Crotti, E. et al. Microbial symbionts of honeybees: a promising tool to improve honeybee health. N. Biotechnol. 30, 716–722 (2013).

    Article  CAS  PubMed  Google Scholar 

  105. 105

    Crane, E. The World History of Beekeeping and Honey Hunting. (Routledge, 1999).

    Google Scholar 

  106. 106

    Bloch, G. et al. Industrial apiculture in the Jordan valley during biblical times with Anatolian honeybees. Proc. Natl Acad. Sci. USA 107, 11240–11244 (2010).

    Article  PubMed  Google Scholar 

  107. 107

    Calderone, N. W. Insect-pollinated crops, insect pollinators and US agriculture: trend analysis of aggregate data for the period 1992–2009. PLoS ONE 7, e37235 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. 108

    Cameron, S. A. et al. Patterns of widespread decline in North American bumble bees. Proc. Natl Acad. Sci. USA 108, 662–667 (2011).

    Article  PubMed  Google Scholar 

  109. 109

    Vanbergen, A. J. & The Insect Pollinators Initiative. Threats to an ecosystem service: pressures on pollinators. Front. Ecol. Environ. 11, 251–259 (2013).

    Article  Google Scholar 

  110. 110

    Klee, J. et al. Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. J. Invertebr. Pathol. 96, 1–10 (2007).

    Article  PubMed  Google Scholar 

  111. 111

    Billiet, A. et al. Colony contact contributes to the diversity of gut bacteria in bumblebees (Bombus terrestris). Insect Sci. http://dx.doi.org/10.1111/1744-7917.12284 (2016).

  112. 112

    Kawasaki, S., Mimura, T., Satoh, T., Takeda, K. & Niimura, Y. Response of the microaerophilic Bifidobacterium species, B. boum and B. thermophilum, to oxygen. Appl. Environ. Microbiol. 72, 6854–6858 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. 113

    Palmer, C., Bik, E. M., DiGiulio, D. B., Relman, D. A. & Brown, P. O. Development of the human infant intestinal microbiota. PLoS Biol. 5, e177 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. 114

    Anderson, K. E., Rodrigues, P. A., Mott, B. M. & 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).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the US National Institutes of Health (award R01 GM108477) and the US National Science Foundation Dimensions of Biodiversity (awards 1046153 and 1415604 to N.A.M).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Nancy A. Moran.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

PowerPoint slides

Glossary

Species clusters

Bacterial groups that contain closely related strains or species.

Core microbiota

The set of microbial species that is present in most members of a host species.

Cuticle

The outer layer of the insect integument, which is primarily composed of chitin.

Malpighian tubules

Part of the insect excretory system that moves waste from the body cavity to the digestive tract for excretion.

Corbiculate bees

A related group of bees that are characterized by the presence of corbicula (pollen baskets) on their hindlimbs, and which include the social honey bees, bumble bees and stingless bees.

Eusocial

A type of social organization that is exemplified by cooperative brood care, reproductive division of labour and the cohabitation of overlapping generations.

Royal jelly

A highly nutritious secretion that is produced by worker bees and is initially fed to all larvae; continued feeding after three days results in the development of queens.

Blind guts

Sac-like guts without an exit for the expulsion of waste.

Trophallaxis

The transfer of food, fluids or secretions between individuals through direct contact.

Foulbrood disease

A bacterial disease that is caused by the infection of the gut of honey bee larvae, which results in the death of the brood.

Pan-genome

The entire gene set of a group of related bacteria, such as that of a bacterial species.

Syntrophic

Cross-feeding, whereby metabolic interactions between two organisms enhance the growth of each other.

Gnotobiotic

An organism in which the strains of microorganisms that are present are fully known.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kwong, W., Moran, N. Gut microbial communities of social bees. Nat Rev Microbiol 14, 374–384 (2016). https://doi.org/10.1038/nrmicro.2016.43

Download citation

Further reading