The role of the gut microbiota of eusocial bees: a literature review

Authors

DOI:

https://doi.org/10.33448/rsd-v10i14.21623

Keywords:

bee microbiota; symbionts; bacterial microbiota; Eusocial bees.

Abstract

Bees have complex symbiotic interactions with microorganisms, which, in exchange for shelter and food, provide their hosts with several benefits, such as food metabolism, detoxification, supply of essential nutrients, protection against invasive species and pathogens, modulation of development and immunity. Thus, these symbiotic relationships are often essential for the bees' survival. The aim of this study is to present the role of the bacterial intestinal microbiota of eusocial bees and the importance it plays in its host. We also highlight what these bacteria are and how they are acquired. The databases of PubMed, CAPES Journals and Academic Research Tool (Scholar Google) were used, in a period of time from 2009 to 2020, related to the role of the intestinal microbiota of eusocial bees. Altogether 28 articles were found, the data obtained were tabulated exposing the host species and the benefits that the bacterial microbiota exerts. In addition, the main activities performed by these intestinal symbionts were selected and each one was discussed, explaining, based on related studies, how they work.

Author Biographies

Suziane Pinto Rodrigues, Universidade Federal do Amazonas

Graduated in Biomedicine from the Uninorte Laureate International Universities School of Health Sciences (2018). She has a PAIC Scientific Initiation at Alfredo da Matta Foundation, working in research involving topics such as Genetics, Polymorphisms and Molecular Biology of microorganisms (2018). Currently, she has a master's degree in progress at the Multi-Institutional Program in Biotechnology at the Federal University of Amazonas.

José Carlos Ipuchima da Silva, Universidade do Estado do Amazonas

Bachelor's Degree in Biomedicine from Centro Universitário do Norte (2018), Degree in Biological Sciences from Centro Universitário Leonardo da Vinci (2020), Specialist in Clinical Analysis and Microbiology from Faculdade do Vale Elvira Dayrel (2020) and Master in Biotechnology from Graduate Program in Biotechnology and Natural Resources of the Amazon by the University of the State of Amazonas (PPGMBT).

Thaissa Cunha de Oliveira, Universidade Federal do Amazonas

Pharmacist, graduated from Universidade Paulista (UNIP - Manaus). She was a scientific initiation student at the National Institute for Research in the Amazon-INPA, from 2016 to 2018, working in the area of microbiology. She is currently a master's student at the Multi-Institutional Graduate Program in Biotechnology-UFAM.

Larissa Ipuchima da Silva, Universidade do Estado do Amazonas

Graduated in Chemical Engineering from the State University of Amazonas (2017). Has experience in Chemistry, common phase in Analytical Chemistry.

Nadionara Costa Menezes, Universidade do Estado do Amazonas

Doctoral student at the Graduate Program in Biodiversity and Biotechnology (UEA). She holds a Master's Degree in Agriculture in the Humid Tropic, from the National Institute for Research in the Amazon (2015). Graduated in Oil and Gas Technology from Centro Universitário do Norte (2011). She has experience in the area of Microbiology, with an emphasis on Soil Microbiology, working mainly in bioremediation, degradation, rhizobia and oil, plant-microorganism associations, microbial enzymes, hormone production.

References

Asenjo, F., Olmos, A., Henríquez-Piskulich, P., Polanco, V., Aldea, P., Ugalde, J. A., & Trombert, A. N. (2016). Genome sequencing and analysis of the first complete genome of Lactobacillus kunkeei strain MP2, an Apis mellifera gut isolate. PeerJ, 4, e1950. https://doi.org/10.7717/peerj.1950.

Barker R. J. (1977). Some carbohydrates found in pollen and pollen substitutes are toxic to honey bees. The Journal of nutrition, 107(10), 1859–1862. https://doi.org/10.1093/jn/107.10.1859

Barker, R. J., & Lehner, Y. (1974). Influence of diet on sugars found by thin-layer chromatography in thoraces of honey bees, Apis mellifera L. The Journal of experimental zoology, 188(2), 157–164. https://doi.org/10.1002/jez.1401880204

Bonilla-Rosso, G., & Engel, P. (2018). Functional roles and metabolic niches in the honey bee gut microbiota. Current opinion in microbiology, 43, 69–76. https://doi.org/10.1016/j.mib.2017.12.009

Bottacini, F., Milani, C., Turroni, F., Sánchez, B., Foroni, E., Duranti, S., Serafini, F., Viappiani, A., Strati, F., Ferrarini, A., Delledonne, M., Henrissat, B., Coutinho, P., Fitzgerald, G. F., Margolles, A., van Sinderen, D., & Ventura, M. (2012). Bifidobacterium asteroides PRL2011 genome analysis reveals clues for colonization of the insect gut. PloS one, 7(9), e44229. https://doi.org/10.1371/journal.pone.0044229

Bulet, P., Hetru, C., Dimarcq, J. L., & Hoffmann, D. (1999). Antimicrobial peptides in insects; structure and function. Developmental and comparative immunology, 23(4-5), 329–344. https://doi.org/10.1016/s0145-305x(99)00015-4

Cariveau, D. P., Elijah Powell, J., Koch, H., Winfree, R., & Moran, N. A. (2014). Variation in gut microbial communities and its association with pathogen infection in wild bumble bees (Bombus). The ISME journal, 8(12), 2369–2379. https://doi.org/10.1038/ismej.2014.68

Cruz-Landim, C. (2009). Abelhas morfologia e função de sistemas. UNESP.

Cullen, T. W., Schofield, W. B., Barry, N. A., Putnam, E. E., Rundell, E. A., Trent, M. S., Degnan, P. H., Booth, C. J., Yu, H., & Goodman, A. L. (2015). Gut microbiota. Antimicrobial peptide resistance mediates resilience of prominent gut commensals during inflammation. Science (New York, N.Y.), 347(6218), 170–175. https://doi.org/10.1126/science.1260580

du Rand, E. E., Pirk, C., Nicolson, S. W., & Apostolides, Z. (2017). The metabolic fate of nectar nicotine in worker honey bees. Journal of insect physiology, 98, 14–22. https://doi.org/10.1016/j.jinsphys.2016.10.017

Emery, O., Schmidt, K., & Engel, P. (2017). Immune system stimulation by the gut symbiont Frischella perrara in the honey bee (Apis mellifera). Molecular ecology, 26(9), 2576–2590. https://doi.org/10.1111/mec.14058

Engel, P., & Moran, N. A. (2013). Functional and evolutionary insights into the simple yet specific gut microbiota of the honey bee from metagenomic analysis. Gut microbes, 4(1), 60–65. https://doi.org/10.4161/gmic.22517

Engel, P., Bartlett, K. D., & Moran, N. A. (2015). The Bacterium Frischella perrara Causes Scab Formation in the Gut of its Honeybee Host. mBio, 6(3), e00193-15. https://doi.org/10.1128/mBio.00193-15

Engel, P., Kwong, W. K., McFrederick, Q., Anderson, K. E., Barribeau, S. M., Chandler, J. A., Cornman, R. S., Dainat, J., de Miranda, J. R., Doublet, V., Emery, O., Evans, J. D., Farinelli, L., Flenniken, M. L., Granberg, F., Grasis, J. A., Gauthier, L., Hayer, J., Koch, H., Kocher, S. & Dainat, B. (2016). The Bee Microbiome: Impact on Bee Health and Model for Evolution and Ecology of Host-Microbe Interactions. mBio, 7(2), e02164-15. https://doi.org/10.1128/mBio.02164-15

Engel, P., Martinson, V. G., & Moran, N. A. (2012). Functional diversity within the simple gut microbiota of the honey bee. Proceedings of the National Academy of Sciences of the United States of America, 109(27), 11002–11007. https://doi.org/10.1073/pnas.1202970109

Ercole, F. F., Melo, L. S. & Alcoforado, C. L. G. C. (2014). Revisão integrativa versus revisão sistemática. Revista Mineira de Enfermagem. 18(1), 9-12.

Fairbrother, A., Purdy, J., Anderson, T., & Fell, R. (2014). Risks of neonicotinoid insecticides to honeybees. Environmental toxicology and chemistry, 33(4), 719–731. https://doi.org/10.1002/etc.2527

Forsgren, E., Olofsson, T. C., Váasquez, A., Frias, I. (2010). Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae. Apidologie 41, 99–108. https://doi.org/10.1051/apido/2009065

Frias, B. E. D, Barbosa, C. D., Lourenço, A. P. (2016). Nutrição de pólen em abelhas ( Apis mellifera ): impacto na saúde adulta. Apidologie, 47, 15-25. https://doi.org/10.1007/s13592-015-0373-y

Gallai, N., Salles, J. M., Settele, J., Vaissière, B. E. (2009). Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics, Elsevier, 68(3), 810-821. https://doi.org/10.1016/j.ecolecon.2008.06.014

Gill, R. J., Ramos-Rodriguez, O., & Raine, N. E. (2012). Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature, 491(7422), 105–108. https://doi.org/10.1038/nature11585

Goulson, D. (2010). Bumblebees : behaviour, ecology, and conservation, 2nd ed. Oxford University Press.

Goulson, D., Nicholls, E., Botías, C., & Rotheray, E. L. (2015). Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science (New York, N.Y.), 347(6229), 1255957. https://doi.org/10.1126/science.1255957

Henry, M., Béguin, M., Requier, F., Rollin, O., Odoux, J. F., Aupinel, P., Aptel, J., Tchamitchian, S., & Decourtye, A. (2012). A common pesticide decreases foraging success and survival in honey bees. Science (New York, N.Y.), 336(6079), 348–350. https://doi.org/10.1126/science.1215039

Kakumanu, M. L., Reeves, A. M., Anderson, T. D., Rodrigues, R. R., & Williams, M. A. (2016). Honey Bee Gut Microbiome Is Altered by In-Hive Pesticide Exposures. Frontiers in microbiology, 7, 1255. https://doi.org/10.3389/fmicb.2016.01255

Kešnerová, L., Mars, R., Ellegaard, K. M., Troilo, M., Sauer, U., & Engel, P. (2017). Disentangling metabolic functions of bacteria in the honey bee gut. PLoS biology, 15(12), e2003467. https://doi.org/10.1371/journal.pbio.2003467

Kešnerová, L., Moritz, R., & Engel, P. (2016). Bartonella apis sp. nov., a honey bee gut symbiont of the class Alphaproteobacteria. International journal of systematic and evolutionary microbiology, 66(1), 414–421. https://doi.org/10.1099/ijsem.0.000736

Khan, K. A., Al-Ghamdi, A. A., Ghramh, H. A., Ansari, M. J., Ali, H., Alamri, S. A., Al-Kahtani, S. N., Adgaba, N., Qasim, M., & Hafeez, M. (2020). Structural diversity and functional variability of gut microbial communities associated with honey bees. Microbial pathogenesis, 138, 103793. https://doi.org/10.1016/j.micpath.2019.103793

Killer, J., Dubná, S., Sedláček, I., & Švec, P. (2014). 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. International journal of systematic and evolutionary microbiology, 64(Pt 1), 152–157. https://doi.org/10.1099/ijs.0.053033-0

Koch, H., & Schmid-Hempel, P. (2011). Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proceedings of the National Academy of Sciences of the United States of America, 108(48), 19288–19292. https://doi.org/10.1073/pnas.1110474108

Kwong, W. K., & Moran, N. A. (2013). 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. International journal of systematic and evolutionary microbiology, 63(Pt 6), 2008–2018. https://doi.org/10.1099/ijs.0.044875-0

Kwong, W. K., & Moran, N. A. (2016). Gut microbial communities of social bees. Nature reviews. Microbiology, 14(6), 374–384. https://doi.org/10.1038/nrmicro.2016.43

Kwong, W. K., Engel, P., Koch, H., & Moran, N. A. (2014). Genomics and host specialization of honey bee and bumble bee gut symbionts. Proceedings of the National Academy of Sciences of the United States of America, 111(31), 11509–11514. https://doi.org/10.1073/pnas.1405838111

Kwong, W. K., Mancenido, A. L., & Moran, N. A. (2017). Immune system stimulation by the native gut microbiota of honey bees. Royal Society open science, 4(2), 170003. https://doi.org/10.1098/rsos.170003

Kwong, W. K., Medina, L. A., Koch, H., Sing, K. W., Soh, E., Ascher, J. S., Jaffé, R., & Moran, N. A. (2017). Dynamic microbiome evolution in social bees. Science advances, 3(3), e1600513. https://doi.org/10.1126/sciadv.1600513

Lee, F. J., Miller, K. I., McKinlay, J. B., & Newton, I. (2018). Differential carbohydrate utilization and organic acid production by honey bee symbionts. FEMS microbiology ecology, 94(8), 10.1093/femsec/fiy113. https://doi.org/10.1093/femsec/fiy113

Lee, F. J., Rusch, D. B., Stewart, F. J., Mattila, H. R., & Newton, I. L. (2015). Saccharide breakdown and fermentation by the honey bee gut microbiome. Environmental microbiology, 17(3), 796–815. https://doi.org/10.1111/1462-2920.12526

Martinson, V. G., Danforth, B. N., Minckley, R. L., Rueppell, O., Tingek, S., & Moran, N. A. (2011). A simple and distinctive microbiota associated with honey bees and bumble bees. Molecular ecology, 20(3), 619–628. https://doi.org/10.1111/j.1365-294X.2010.04959.x

Martinson, V. G., Moy, J., & Moran, N. A. (2012). Establishment of characteristic gut bacteria during development of the honeybee worker. Applied and environmental microbiology, 78(8), 2830–2840. https://doi.org/10.1128/AEM.07810-11

McFrederick, Q. S., Wcislo, W. T., Taylor, D. R., Ishak, H. D., Dowd, S. E., & Mueller, U. G. (2012). Environment or kin: whence do bees obtain acidophilic bacteria?. Molecular ecology, 21(7), 1754–1768. https://doi.org/10.1111/j.1365-294X.2012.05496.x

Michener, C. D. (2000). The bees of the world. Baltimore: The Johns Hopkins University Press.

Michener, CD (2007) The Bees of the World. (2a ed.), John Hopkins University Press, Baltimore.

Michener, C. D. (2013). The Meliponini. In: Vit, P., Pedro, S. R. M., Roubik, D. H. (Orgs.). Pot-Honey: A legacy of stingless bees. New York: Springer.

Moran, N. A., Hansen, A. K., Powell, J. E., & Sabree, Z. L. (2012). Distinctive gut microbiota of honey bees assessed using deep sampling from individual worker bees. PloS one, 7(4), e36393. https://doi.org/10.1371/journal.pone.0036393

Moran, N. A., Ochman, H., & Hammer, T. J. (2019). Evolutionary and ecological consequences of gut microbial communities. Annual review of ecology, evolution, and systematics, 50(1), 451–475. https://doi.org/10.1146/annurev-ecolsys-110617-062453

Motta, E., Raymann, K., & Moran, N. A. (2018). Glyphosate perturbs the gut microbiota of honey bees. Proceedings of the National Academy of Sciences of the United States of America, 115(41), 10305–10310. https://doi.org/10.1073/pnas.1803880115

Nappi, A. J., & Christensen, B. M. (2005). Melanogenesis and associated cytotoxic reactions: applications to insect innate immunity. Insect biochemistry and molecular biology, 35(5), 443–459. https://doi.org/10.1016/j.ibmb.2005.01.014

Nogrado, K., Lee, S., Chon, K., Lee, J. H. (2019). Effect of transient exposure to carbaryl wettable powder on the gut microbial community of honey bees. Applied Biological Chemistry, 62(6), 1-8. https://doi.org/10.1186/s13765-019-0415-7

Olofsson, T. C., & Vásquez, A. (2008). Detection and identification of a novel lactic acid bacterial flora within the honey stomach of the honeybee Apis mellifera. Current microbiology, 57(4), 356–363. https://doi.org/10.1007/s00284-008-9202-0

Onchuru, T. O., Javier Martinez, A., Ingham, C. S., & Kaltenpoth, M. (2018). Transmission of mutualistic bacteria in social and gregarious insects. Current opinion in insect science, 28, 50–58. https://doi.org/10.1016/j.cois.2018.05.002

Raymann, K., & Moran, N. A. (2018). The role of the gut microbiome in health and disease of adult honey bee workers. Current opinion in insect science, 26, 97–104. https://doi.org/10.1016/j.cois.2018.02.012

Raymann, K., Bobay, L. M., & Moran, N. A. (2018). Antibiotics reduce genetic diversity of core species in the honeybee gut microbiome. Molecular ecology, 27(8), 2057–2066. https://doi.org/10.1111/mec.14434

Raymann, K., Shaffer, Z., & Moran, N. A. (2017). Antibiotic exposure perturbs the gut microbiota and elevates mortality in honeybees. PLoS biology, 15(3), e2001861. https://doi.org/10.1371/journal.pbio.2001861

Ryu, J. H., Kim, S. H., Lee, H. Y., Bai, J. Y., Nam, Y. D., Bae, J. W., Lee, D. G., Shin, S. C., Ha, E. M., & Lee, W. J. (2008). Innate immune homeostasis by the homeobox gene caudal and commensal-gut mutualism in Drosophila. Science (New York, N.Y.), 319(5864), 777–782. https://doi.org/10.1126/science.1149357

Schwarz, R. S., Moran, N. A., & Evans, J. D. (2016). Early gut colonizers shape parasite susceptibility and microbiota composition in honey bee workers. Proceedings of the National Academy of Sciences of the United States of America, 113(33), 9345–9350. https://doi.org/10.1073/pnas.1606631113

Smagghe, G., & Tirry, L. (2001). Insect midgut as a site for insecticide detoxification and resistance. In I. Ishaaya (Ed.), Biochemical sites of insecticide action and resistance (pp. 293–321). Berlin, Germany: Springer.

Tzou, P., De Gregorio, E., & Lemaitre, B. (2002). How Drosophila combats microbial infection: a model to study innate immunity and host-pathogen interactions. Current opinion in microbiology, 5(1), 102–110. https://doi.org/10.1016/s1369-5274(02)00294-1

Vásquez, A., Forsgren, E., Fries, I., Paxton, R. J., Flaberg, E., Szekely, L., & Olofsson, T. C. (2012). Symbionts as major modulators of insect health: lactic acid bacteria and honeybees. PloS one, 7(3), e33188. https://doi.org/10.1371/journal.pone.0033188

Vaudo, A. D., Tooker, J. F., Grozinger, C. M., & Patch, H. M. (2015). Bee nutrition and floral resource restoration. Current opinion in insect science, 10, 133–141. https://doi.org/10.1016/j.cois.2015.05.008

Wu, M., Sugimura, Y., Takaya, N., Takamatsu, D., Kobayashi, M., Taylor, D., & Yoshiyama, M. (2013). Characterization of bifidobacteria in the digestive tract of the Japanese honeybee, Apis cerana japonica. Journal of invertebrate pathology, 112(1), 88–93. https://doi.org/10.1016/j.jip.2012.09.005

Wu, Y., Zheng, Y., Chen, Y., Wang, S., Chen, Y., Hu, F., & Zheng, H. (2020). Honey bee (Apis mellifera) gut microbiota promotes host endogenous detoxification capability via regulation of P450 gene expression in the digestive tract. Microbial biotechnology, 13(4), 1201–1212. https://doi.org/10.1111/1751-7915.13579

Yoshiyama, M., & Kimura, K. (2009). Bacteria in the gut of Japanese honeybee, Apis cerana japonica, and their antagonistic effect against Paenibacillus larvae, the causal agent of American foulbrood. Journal of invertebrate pathology, 102(2), 91–96. https://doi.org/10.1016/j.jip.2009.07.005

Yun, J. H., Jung, M. J., Kim, P. S., & Bae, J. W. (2018). Social status shapes the bacterial and fungal gut communities of the honey bee. Scientific reports, 8(1), 2019. https://doi.org/10.1038/s41598-018-19860-7

Zheng, H., Nishida, A., Kwong, W. K., Koch, H., Engel, P., Steele, M. I., & Moran, N. A. (2016). Metabolism of Toxic Sugars by Strains of the Bee Gut Symbiont Gilliamella apicola. mBio, 7(6), e01326-16. https://doi.org/10.1128/mBio.01326-16

Zheng, H., Perreau, J., Powell, J. E., Han, B., Zhang, Z., Kwong, W. K., Tringe, S. G., & Moran, N. A. (2019). Division of labor in honey bee gut microbiota for plant polysaccharide digestion. Proceedings of the National Academy of Sciences of the United States of America, 116(51), 25909–25916. https://doi.org/10.1073/pnas.1916224116

Zheng, H., Powell, J. E., Steele, M. I., Dietrich, C., & Moran, N. A. (2017). Honeybee gut microbiota promotes host weight gain via bacterial metabolism and hormonal signaling. Proceedings of the National Academy of Sciences of the United States of America, 114(18), 4775–4780. https://doi.org/10.1073/pnas.1701819114

Zheng, H., Steele, M. I., Leonard, S. P., Motta, E., & Moran, N. A. (2018). Honey bees as models for gut microbiota research. Lab animal, 47(11), 317–325. https://doi.org/10.1038/s41684-018-0173-x

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24/10/2021

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RODRIGUES, S. P. .; SILVA, J. C. I. da .; OLIVEIRA, T. C. de .; SILVA, L. I. da .; MENEZES, N. C. . The role of the gut microbiota of eusocial bees: a literature review . Research, Society and Development, [S. l.], v. 10, n. 14, p. e30101421623, 2021. DOI: 10.33448/rsd-v10i14.21623. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/21623. Acesso em: 23 apr. 2025.

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Vol. 10 No. 14

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Agrarian and Biological Sciences

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Copyright (c) 2021 Suziane Pinto Rodrigues; José Carlos Ipuchima da Silva; Thaissa Cunha de Oliveira; Larissa Ipuchima da Silva; Nadionara Costa Menezes

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