El papel de la microbiota intestinal de las abejas eusociales: una revisión de la literatura

Autores/as

DOI:

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

Palabras clave:

microbiota de abejas; simbiontes; microbiota bacteriana; Abejas eusociales.

Resumen

Las abejas tienen complejas interacciones simbióticas con los microorganismos, que a cambio de refugio y alimento, brindan a sus hospederos varios beneficios, como metabolismo de los alimentos, desintoxicación, suministro de nutrientes esenciales, protección contra especies invasoras y patógenos, modulación del desarrollo e inmunidad. Por lo tanto, estas relaciones simbióticas suelen ser esenciales para la supervivencia de las abejas. El objetivo de este estudio es presentar el papel de la microbiota intestinal bacteriana de las abejas eusociales y la importancia que juega en su hospedador. También destacamos qué son estas bacterias y cómo se adquieren. Se utilizaron las bases de datos de PubMed, CAPES Journals y Academic Research Tool (Scholar Google), en un período de tiempo de 2009 a 2020, relacionado con el papel de la microbiota intestinal de las abejas eusociales. En total se encontraron 28 artículos, los datos obtenidos se tabularon exponiendo las especies hospedadoras y los beneficios que ejerce la microbiota bacteriana. Además, se seleccionaron las principales actividades que realizan estos simbiontes intestinales y se discutió cada una, explicando, en base a estudios relacionados, cómo funcionan.

Biografía del autor/a

Suziane Pinto Rodrigues, Universidade Federal do Amazonas

Licenciada en Biomedicina por la Facultad de Ciencias de la Salud de las Universidades Internacionales Laureate Uninorte (2018). Tiene Iniciación Científica PAIC en la Fundación Alfredo da Matta, trabajando en investigaciones que involucran temas como Genética, Polimorfismos y Biología Molecular de Microorganismos (2018). Actualmente, con maestría en progreso en el Programa Multinstitucional en Biotecnología de la Universidad Federal de Amazonas.

José Carlos Ipuchima da Silva, Universidade do Estado do Amazonas

Licenciada en Biomedicina por el Centro Universitário do Norte (2018), Licenciada en Ciencias Biológicas por el Centro Universitário Leonardo da Vinci (2020), Especialista en Análisis Clínicos y Microbiología por la Faculdade do Vale Elvira Dayrel (2020) y Máster en Biotecnología por el Programa de Posgrado en Biotecnología y Recursos Naturales de la Amazonía por la Universidad del Estado de Amazonas (PPGMBT).

Thaissa Cunha de Oliveira, Universidade Federal do Amazonas

Farmacéutico, egresado de la Universidade Paulista (UNIP - Manaus). Fue estudiante de iniciación científica en el Instituto Nacional de Investigaciones de la Amazonía - INPA, de 2016 a 2018, trabajando en el área de microbiología. Actualmente es estudiante de maestría en el Programa de Posgrado Multiinstitucional en Biotecnología - UFAM.

Larissa Ipuchima da Silva, Universidade do Estado do Amazonas

Licenciada en Ingeniería Química por la Universidad Estatal de Amazonas (2017). Tiene experiencia en Química, fase común en Química Analítica.

Nadionara Costa Menezes, Universidade do Estado do Amazonas

Estudiante de doctorado en el Programa de Postgrado en Biodiversidad y Biotecnología (UEA). Tiene una Maestría en Agricultura en el Trópico Húmedo, del Instituto Nacional de Investigaciones en la Amazonía (2015). Licenciada en Tecnología de Petróleo y Gas por el Centro Universitário do Norte (2011). Tiene experiencia en el campo de la Microbiología, con énfasis en Microbiología de Suelos, trabajando principalmente en biorremediación, degradación, rizobios y aceite, asociaciones planta-microorganismo, enzimas microbianas, producción de hormonas.

Citas

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

Publicado

24/10/2021

Cómo citar

RODRIGUES, S. P. .; SILVA, J. C. I. da .; OLIVEIRA, T. C. de .; SILVA, L. I. da .; MENEZES, N. C. . El papel de la microbiota intestinal de las abejas eusociales: una revisión de la literatura. 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: 17 jul. 2024.

Número

Sección

Ciencias Agrarias y Biológicas