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Yeast and Bacterial Composition in Pot-Pollen Recovered from Meliponini in Colombia: Prospects for a Promising Biological Resource

  • Marcela Villegas-Plazas
  • Judith Figueroa-Ramírez
  • Carla Portillo
  • Paola Monserrate
  • Víctor Tibatá
  • Oswaldo Andrés Sánchez
  • Howard Junca
Chapter

Abstract

Animals have an intimate association with diverse communities of microorganisms, commonly referred to as the microbiome, and bees are no exception. While several studies to date have explored the symbiotic microbial community within the gut of honeybees, little is known of the microbial communities associated with hive-stored pollen and ‘beebread’ of Meliponini. This holds particular interest, as it is believed that the processes of producing honey within beehives is largely dependent on metabolic transformations performed by microbial communities. Since such knowledge pertaining to the microbial role within natural fermentation of pollen has valuable and potential biotechnological applications, the aim of this study is to explore bioactivities and inter-domain microbial communities of the so-called ripe pollen by cataloguing the yeast component using culture-dependent methods and the bacterial components using culture-independent methods. We are reviewing and reporting original results, all from specimens collected in Colombia, about the cumulative antimicrobial activities detected in A. mellifera pollen and T. angustula pot-pollen extracts; the taxonomic composition and comparisons of the microbiomes associated with hive-stored pollen from colonies of A. mellifera, T. angustula and Melipona; and the biochemical and molecular identification of yeasts isolated from beebread of A. mellifera and from pot-pollen of four genera of stingless bees (Meliponini: Scaptotrigona, Plebeia, Paratrigona and T. angustula). This work demonstrates the importance of diversity within the inter-domain microbial communities of Meliponini species and their potential as an untapped resource for biological and/or biotechnological application and biodiversity exploration.

Notes

Acknowledgements

We would like to thank Universidad Nacional de Colombia, Departamento Administrativo de Ciencia y Tecnología COLCIENCIAS for the financial support, Bee Research Lab (Laboratorio de abejas) Universidad Nacional LABUN for kindly providing the beebread samples from Apis mellifera, the Asociación Apícola Comunera for kindly providing samples of stingless bees and Compañía Campo Colombia SAS for kindly providing us the samples of stingless bees used in this report. We also thank the members of Research Group AYNI ‘Microbiología Veterinaria, Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional de Colombia Sede Bogotá’ for the continuous support and excellent technical help. We thank Erika García at Microbiomas Foundation, Colombia, and Nadim Ajami at Baylor College of Medicine, USA, for the excellent support on material preparation and technologies used for culture-independent analyses. We would like to thank the editors, Prof. Dr. Patricia Vit and Dr. David Roubik for their helpful and constructive remarks and the outstanding editorial work, and to Dr. Melissa L. Wos-Oxley for carefully proofreading the text and for her valuable suggestions and corrections which improved the manuscript.

References

  1. Abouda Z, Zerdani I, Kalalou I, Faid MA. 2011. The antibacterial activity of Moroccan Beebread and bee-pollen (dresh and Dried) against Pathogenic Bacteria. Research Journal of Microbiology 64: 376-384.Google Scholar
  2. Ahn JH, Hong IP, Bok JI, Kim BY, Song J, Weon HY. 2012. Pyrosequencing analysis of the bacterial communities in the guts of honey bees Apis cerana and Apis mellifera in Korea. Journal of Microbiology 50:735–745. doi:  10.1007/s12275-012-2188-0.CrossRefGoogle Scholar
  3. Ambika Manirajan B, Ratering S, Rusch V, Schwiertz A, Geissler-Plaum R, Cardinale M, Schnell S. 2016. Bacterial microbiota associated with flower pollen is influenced by pollination type, and shows a high degree of diversity and species-specificity. Environmental Microbiology Sep 9. Epub ahead of print. doi:  10.1111/1462-2920.13524.CrossRefPubMedGoogle Scholar
  4. Anderson KE, Carroll MJ, Sheehan TI, Mott BM, Maes P, Corby, Harris V. 2014. Hive-stored pollen of honey bees: Many lines of evidence are consistent with pollen preservation, not nutrient conversion. Molecular Ecology 23:5904–5917. doi:  10.1111/mec.12966.CrossRefPubMedPubMedCentralGoogle Scholar
  5. Association of Official Analytical Chemists (AOAC). 2007. Official Methods of Analysis. 18th. Edition. AOAC; Arlington (TX), USA. 1383 pp.Google Scholar
  6. Basim E, Basim H, Özcan M. 2006. Antibacterial activities of Turkish pollen and propolis extracts against plant bacterial pathogens. Journal of Food Engineering 77:992–996. doi:  10.1016/j.jfoodeng.2005.08.027.CrossRefGoogle Scholar
  7. Bogdanov S. 2004. Quality standards of bee pollen and beeswax. Apiacta 39:334–341.Google Scholar
  8. Bottacini F, Milani C, Turroni F, Sánchez B, Foroni E, Duranti S, Serafini F, Viappiani A, Strati F, Ferrarini A, Delledonne M. 2012. Bifidobacterium asteroides PRL2011 Genome Analysis Reveals Clues for Colonization of the Insect Gut. PLoS One 7:1–14. doi:  10.1371/journal.pone.0044229.CrossRefGoogle Scholar
  9. Brodschneider R, Crailsheim K. 2010. Nutrition and health in honey bees - Review article. Apidologie 41: 278–294. doi:  10.1051/apido/2010012.CrossRefGoogle Scholar
  10. Brysch-Herzberg M. 2004. Ecology of yeasts in plant-bumblebee mutualism in Central Europe. FEMS Microbiology Ecology 50: 87–100. doi:  10.1016/j.femsec.2004.06.003.CrossRefPubMedPubMedCentralGoogle Scholar
  11. Camargo J, García M, Júnior AC. 1992. Notas previas sobre a bionomia de Ptilotrigona lurida (Hymenoptera, Apidae, Meliponinae). Boletim do Museu Paraense Emilio Goeldi, 8: 391-394.Google Scholar
  12. Carpes ST. 2008. Estudo Das Caracteristicas Fisico-Quimicas e Biologicas do Polen Apicola de Apis mellifera L. da regiao sul do Brasil. PhD Thesis, Universidade Federal Do Parana; Curitiba, Brasil. 255 pp.Google Scholar
  13. Corby-Harris V, Maes P, Anderson KE. 2014. The bacterial communities associated with honey bee (Apis mellifera) foragers. PLoS One. doi:  10.1371/journal.pone.0095056 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Daniel HM, Rosa CA, São Thiago-Calaça PS, Antonini Y, Bastos EM, Evrard P, Huret S, Fidalgo-Jiménez A, Lachance MA. 2013. Starmerella neotropicalis f. a., sp. nov., a yeast species found in bees and pollen. International Journal of Systematic and Evolutionary Microbiology 63:3896–3903. doi:  10.1099/ijs.0.055897-0 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Donaldson-Matasci MC, DeGrandi-Hoffman G, Dornhaus A. 2013. Bigger is better: Honeybee colonies as distributed information-gathering systems. Animal Behavior 85:585–592. doi:  10.1016/j.anbehav.2012.12.020 CrossRefGoogle Scholar
  16. Douglas G, Sigler L. 2015. Trichosporonoides megachiliensis, a new hyphomycete associated with alfalfa leafcutter bees, with notes on Trichosporonoides and Moniliellag. JSTOR 84: 555–570.Google Scholar
  17. Engel P, Kwong WK, McFrederick Q, Anderson KE, Barribeau SM, Chandler JA, Cornman RS, Dainat J, de Miranda JR, Doublet V, Emery O. 2016. The bee microbiome: Impact on bee health and model for evolution and ecology of host-microbe interactions. MBio 7: e02164-15. doi:  10.1128/mBio.02164-15.CrossRefPubMedPubMedCentralGoogle Scholar
  18. Engel P, Martinson VG, Moran N. 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: 11002–11007. doi:  10.1073/pnas.1202970109.CrossRefGoogle Scholar
  19. Gilliam M. 1979. Microbiology of pollen and beebread: the genus Bacillus. Apidologie 10: 269–274. doi:  10.1051/apido:19790304 CrossRefGoogle Scholar
  20. Gilliam M, Prest DB, Lorenz BJ. 1989. Microbiology of pollen and beebread: taxonomy and enzymology of molds. Apidology 20:53–68. doi:  10.1051/apido:19890106 CrossRefGoogle Scholar
  21. Grubbs KJ, Scott JJ, Budsberg KJ, Read H, Balser TC, Currie CR. 2015. Unique honey bee (Apis mellifera) hive component-based communities as detected by a hybrid of phospholipid fatty-acid and fatty-acid methyl ester analyses. PLoS One 10:1–17. doi:  10.1371/journal.pone.0121697 CrossRefGoogle Scholar
  22. Hydak M. 1970. Honey bee nutrition. Annual Reviews of Entomology. 15: 143-156. doi:  10.1146/annurev.en.15.010170.001043.CrossRefGoogle Scholar
  23. Herrera CM. 2014. Population growth of the floricolous yeast Metschnikowia reukaufii: effects of nectar host, yeast genotype, and host genotype interaction. FEMS Microbiology Ecology 88: 250–257. doi:  10.1111/1574-6941.12284 CrossRefPubMedGoogle Scholar
  24. Herrera CM, Pozo MI, Medrano M. 2013. Yeasts in nectar of an early-blooming herb: sought by bumble bees, detrimental to plant fecundity. Ecology 94: 273–279. doi:  10.1890/12-0595.1 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Higes M, Martín-Hernández R, Garrido-Bailon E, García-Palencia P, Meana A. 2008. Detection of infective Nosema ceranae (Microsporidia) spores in corbicular pollen of forager honeybees. Journal of Invertebrate Pathology 97: 76–78. doi:  10.1016/j.jip.2007.06.002.CrossRefPubMedGoogle Scholar
  26. Hong SG, Bae KS, Herzberg M, Titze A, Lachance MA. 2003. Candida kunwiensis sp. nov., a yeast associated with flowers and bumblebees. International Journal of Systematic and Evolutionary Microbiology 53: 367–372. doi:  10.1099/ijs.0.02200-0 CrossRefPubMedGoogle Scholar
  27. Kacaniova M, Vuković N, Chlebo R, Haščík P, Rovna K, Cubon J, Dżugan M, Pasternakiewicz A. 2012. The antimicrobial activity of honey, bee pollen loads and beeswax from Slovakia. Archives of Biological Sciences 64: 927–934. doi:  10.2298/ABS1203927K CrossRefGoogle Scholar
  28. Komosinska-Vassev K, Olczyk P, Kaźmierczak J, Mencner L, Olczyk K. 2015. Bee pollen: chemical composition and therapeutic application. Evidence-Based Complementary and Alternative Medicine 2015:297425.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Kuczynski J, Stombaugh J, Walters WA, González A, Caporaso JG, Knight R. 2011. Using QIIME to analyze 16S rRNA gene sequences from microbial communities. Current Protocols in Microbiology. Bioinformatics Chapter 10: Unit 10.7. doi:  10.1002/0471250953.bi1007s36
  30. Kwong WK, Engel P, Koch H, Moran NA. 2014. Genomics and host specialization of honey bee and bumble bee gut symbionts. Proceeding of the National Academy of Sciences of the United States of America 111:11509–11514. doi:  10.1073/pnas.1405838111 CrossRefGoogle Scholar
  31. Kwong WK, Moran NA. 2016. Gut microbial communities of social bees. Nature Reviews Microbiology 14:374–384. doi:  10.1038/nrmicro.2016.43 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Lee FJ, Rusch DB, Stewart FJ, Mattila HR, Newton IL. 2015. Saccharide breakdown and fermentation by the honey bee gut microbiome. Environmental Microbiology 17:796–815. doi:  10.1111/1462-2920.12526 CrossRefPubMedGoogle Scholar
  33. Martinson VG, Danforth BN, Minckley RL, Rueppell O, Tingek S, Moran NA. 2011. A simple and distinctive microbiota associated with honey bees and bumble bees. Molecular Ecology 20:619–628. doi:  10.1111/j.1365-294X.2010.04959.x CrossRefPubMedGoogle Scholar
  34. McMurdie PJ, Holmes S. 2013. Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8: e61217. doi:  10.1371/journal.pone.0061217 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Menezes C. 2010. A produção de rainhas ea multiplicação de colônias em Scaptotrigona aff. depilis (Hymenoptera, Apidae, Meliponini). Ph.D. Thesis, University of São Paulo; Ribeirão Preto, Brazil. 97 pp.Google Scholar
  36. Mohr KI, Tebbe CC. 2006. Diversity and phylotype consistency of bacteria in the guts of three bee species (Apoidea) at an oilseed rape field. Environmental Microbiology 8: 258-272.CrossRefPubMedGoogle Scholar
  37. Monserrate P. 2015. Valoración in vitro del potencial antimicrobiano de extractos etanólicos de polen de Apis mellifera y de Tetragonisca angustula, en busca de posibles usos terapéuticos. Universidad Nacional de Colombia. Master’s Thesis, Universidad Nacional de Colombia; Bogotá, Colombia. 83 pp.Google Scholar
  38. Pimentel MR, Antonini Y, Martins RP, Lachance MA, Rosa CA. 2005. Candida riodocensis and Candida cellae, two new yeast species from the Starmerella clade associated with solitary bees in the Atlantic rain forest of Brazil. FEMS Yeast Research 5: 875–879. doi:  10.1016/j.femsyr.2005.03.006 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Portillo Carrascal C. 2016. Identificación de levaduras presentes en el proceso de transformación de polen corbicular a pan de abejas por métodos tradicionales y moleculares. Master’s Thesis, Universidad Nacional de Colombia; Bogotá, Colombia. 109 pp.Google Scholar
  40. Powell JE, Martinson VG, Urban-Mead K, Moran NA. 2014. Routes of acquisition of the gut microbiota of the honey bee Apis mellifera. Applied Environmental Microbiology 80: 7378–7387. doi:  10.1128/AEM.01861-14.CrossRefPubMedPubMedCentralGoogle Scholar
  41. Rodríguez G, Chamorro A, Obregón F, Montoya D, Ramírez P, Solarte N. 2011. Guía ilustrada de polen y plantas nativas visitadas por abejas. Universidad Nacional de Colombia; Bogotá, Colombia. 230 pp.Google Scholar
  42. Rosa CA, Lachance MA. 2005. Zygosaccharomyces machadoi sp. n., a yeast species isolated from a nest of the stingless bee Tetragonisca angustula. Lundiana 6: 27–29.Google Scholar
  43. Rosa CA, Lachance MA, Silva JO, Teixeira AC, Marini MM, Antonini Y, Martins RP. 2003. Yeast communities associated with stingless bees. FEMS Yeast Research 4: 271–275. doi:  10.1016/S1567-1356(03)00173-9 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Saksinchai S, Suzuki M, Chantawannakul P, Ohkuma M, Lumyong S. 2012. A novel ascosporogenous yeast species, Zygosaccharomyces siamensis, and the sugar tolerant yeasts associated with raw honey collected in Thailand. Fungal Diversity 52: 123–139. doi:  10.1007/s13225-011-0115-z CrossRefGoogle Scholar
  45. Teixeira AC, Marini MM, Nicoli JR, Antonini Y, Martins RP, Lachance MA, Rosa CA. 2003. Starmerella meliponinorum sp. nov., a novel ascomycetous yeast species associated with stingless bees. International Journal of Systematic and Evolutionary Microbiology 53: 339–343. doi:  10.1099/ijs.0.02262-0 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Thorp RW. 1979. Structural, Behavioral and Physiological Adaptations of Bees (Apoidea) for collecting pollen. JSTOR 66: 788–812.Google Scholar
  47. Vásquez A, Olofsson TC. 2009. The lactic acid bacteria involved in the production of bee pollen and beebread. Journal of Apicultural Research 48: 189–195. doi:  10.3896/IBRA.1.48.3.07 CrossRefGoogle Scholar
  48. Vit P, Pulcini P. 1996. Diastase and invertase activities in Meliponini and Trigonini honeys from Venezuela. Journal of Apicultural Research 35: 57–62. doi:  10.1080/00218839.1996.11100913 CrossRefGoogle Scholar
  49. Vit P, Santiago B, Pedro SRM, Ruíz J, Maza F, Peña-Vera M, Pérez-Pérez E. 2016. Chemical and bioactive characterization of pot-pollen produced by Melipona and Scaptotrigona stingless bees from Paria Grande, Amazonas State, Venezuela. Emirates Journal of Food and Agriculture. 28: 78-84.CrossRefGoogle Scholar
  50. White TJ, Bruns T, Lee ST. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. pp. 315-322. In: Innis M, Gelfand D, Sninsky J, White T, eds. PCR Protocols: A guide to methods and applications, Academic Press, San Diego, California, USA, 482 pp.Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Marcela Villegas-Plazas
    • 1
  • Judith Figueroa-Ramírez
    • 2
  • Carla Portillo
    • 2
  • Paola Monserrate
    • 2
  • Víctor Tibatá
    • 2
  • Oswaldo Andrés Sánchez
    • 2
  • Howard Junca
    • 1
  1. 1.RG Microbial Ecology, Division of Ecogenomics & HolobiontsMicrobiomas FoundationChiaColombia
  2. 2.Research Group AYNI, Bee Science & Technology, Veterinary Microbiology, Faculty of Veterinary Medicine and Zootechnics, Universidad Nacional de ColombiaBogotáColombia

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