O papel da microbiota bacteriana intestinal de abelhas eussociais: uma revisão de literatura
DOI:
https://doi.org/10.33448/rsd-v10i14.21623Palavras-chave:
microbiota de abelhas; Simbiontes; microbiota bacteriana; Abelhas eussociais.Resumo
As abelhas apresentam complexas interações simbióticas com microrganismos, os quais em troca de abrigo e alimento, fornecem a seus hospedeiros diversos benefícios, como metabolização de alimentos, desintoxicação, fornecimento de nutrientes essenciais, proteção contra espécies invasoras e patógenos, modulação do desenvolvimento e imunidade. Assim, essas relações simbióticas muitas vezes são essenciais para a sobrevivência das abelhas. Objetivo deste estudo, é apresentar o papel da microbiota intestinal bacteriana de abelhas eussociais e a importância que ela exerce em seu hospedeiro. Destacamos também, quais são estas bactérias e como elas são adquiridas. Foram usadas as bases de dados do PubMed, Periódicos da CAPES e Ferramenta de Pesquisa Acadêmica (Scholar Google), em um período de tempo compreendido de 2009 a 2020, relacionados ao papel da microbiota intestinal de abelhas eussociais. Ao todo foram encontrados 28 artigos, os dados obtidos foram tabelados expondo as espécies hospedeira e os benefícios que a microbiota bacteriana exerce. Além disso, foram selecionadas as principais atividade exercidas por esses simbiontes intestinais e decorrido sobre cada uma, explicando, com base em estudos relacionados, como funcionam.
Referências
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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