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Selection of yeasts from bee products for alcoholic beverage production

  • Mayara Salgado Silva
  • Luciana Marina Arruda
  • Pedro Lanna Xavier
  • Maria Ximena Díaz Ramírez
  • Fernando Augusto da Silveira
  • Weyder Cristiano Santana
  • Paulo Henrique Alves da Silva
  • Luciano Gomes Fietto
  • Monique Renon EllerEmail author
Food Microbiology - Research Paper
  • 17 Downloads

Abstract

The use of appropriate yeast strains allows to better control the fermentation during beverage production. Bee products, especially of stingless bees, are poorly explored as sources of fermenting microorganisms. In this work, yeasts were isolated from honey and pollen from Tetragonisca angustula (Jataí), Nannotrigona testaceicornis (Iraí), Frieseomelitta varia (Marmelada), and honey of Apis mellifera bees and screened according to morphology, growth, and alcohol production. Bee products showed to be potential sources of fermenting microorganisms. From 55 isolates, one was identified as Papiliotrema flavescens, two Rhodotorula mucilaginosa, five Saccharomyces cerevisiae, and nine Starmerella meliponinorum. The S. cerevisiae strains were able to produce ethanol and glycerol at pH 4.0–8.0 and temperature of 10–30 °C, with low or none production of undesirable compounds, such as acetic acid and methanol. These strains are suitable for the production of bioethanol and alcoholic beverages due to their high ethanol production, similar or superior to the commercial strain, and in a broad range of conditions like as 50% (m/v) glucose, 10% (v/v) ethanol, or 500 mg L−1 of sodium metabisulfite.

Keywords

Ethanol production Yeast selection Stingless bees Honey 

Notes

Funding information

This work was supported by Fundação Arthur Bernardes (FUNARBE), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).

Compliance with ethical standards

Disclaimer

The funders had no role in the study design, data collection, analysis, publishing decisions, or preparation of this manuscript.

References

  1. 1.
    Pando Bedriñana R, Querol Simón A, Suárez VB (2010) Genetic and phenotypic diversity of autochthonous cider yeasts in a cellar from Asturias. Food Microbiol 27(4):503–508.  https://doi.org/10.1016/j.fm.2009.11.018 CrossRefPubMedGoogle Scholar
  2. 2.
    Pereira AP, Dias T, Andrade J, Ramalhosa E, Estevinho LM (2009) Mead production: selection and characterization assays of Saccharomyces cerevisiae strains. Food Chem Toxicol 47(8):2057–2063.  https://doi.org/10.1016/j.fct.2009.05.028 CrossRefPubMedGoogle Scholar
  3. 3.
    Tapsoba F, Legras J-L, Savadogo A, Dequin S, Traore AS (2015) Diversity of Saccharomyces cerevisiae strains isolated from Borassus akeassii palm wines from Burkina Faso in comparison to other African beverages. Int J Food Microbiol 211:128–133.  https://doi.org/10.1016/j.ijfoodmicro.2015.07.010 CrossRefPubMedGoogle Scholar
  4. 4.
    van der Aa KA, Jesperen L, Glover RL, Diawara B, Jakobsen M (2001) Identification and characterization of Saccharomyces cerevisiae strains isolated from West African sorghum beer. Yeast 18(11):1069–1079.  https://doi.org/10.1002/yea.756 CrossRefGoogle Scholar
  5. 5.
    Mašková Z, Čanigová M, Ivanišová E et al (2018) Pollen CAN - Testing of bee pollen fermentation in model conditions. J Microbiol Biotechnol Food Sci 8(2):805–811.  https://doi.org/10.15414/jmbfs.2018.8.2.805-811 CrossRefGoogle Scholar
  6. 6.
    Silva MS, Rabadzhiev Y, Eller MR, Iliev I, Ivanova I, Santana WC (2017) Microrganisms in honey. In: Honey Analyses, 1st edn. InTech, pp 233–258.  https://doi.org/10.5772/52807 Google Scholar
  7. 7.
    Snowdon JA, Cliverb D (1996) Microorganisms in honey. Int J Food Microbiol 31:1–6CrossRefGoogle Scholar
  8. 8.
    Souza BD, Marchini LC, Dias CTD, Oda-Souza M, de Carvalho CAL, Alves RMD (2009) Microbiological evaluation of Trigonine bee (Apidae: Trigonini) honey samples from the State of Bahia - Brazil. Cienc E Tecnol Aliment 29(4):798–802CrossRefGoogle Scholar
  9. 9.
    Dias T, Rodrigues S, Estevinho LM, Feás X, da Silva JP (2011) Botanical, nutritional and microbiological characterisation of honeybee-collected pollen from Portugal. Food Chem Toxicol.  https://doi.org/10.1016/j.fct.2011.11.005
  10. 10.
    Gomes S, Dias LG, Moreira LL, Rodrigues P, Estevinho L (2010) Physicochemical, microbiological and antimicrobial properties of commercial honeys from Portugal. Food Chem Toxicol 48(2):544–548.  https://doi.org/10.1016/j.fct.2009.11.029 CrossRefPubMedGoogle Scholar
  11. 11.
    Bogdanov S. First World Conference on Organic Beekeeping Program and Abstracts Apimondia. In: Apimondia. Vol 1. ; 2010:50.Google Scholar
  12. 12.
    dos Santos CF, Francisco F (2016) de O, Imperatriz-Fonseca VL, Arias MC. Eusocial bee male aggregations: spatially and temporally separated but genetically homogenous. Entomol Exp Appl 158(3):320–326.  https://doi.org/10.1111/eea.12407 CrossRefGoogle Scholar
  13. 13.
    Roubik DW, Moreno JE, Vergara C, Wittmann D (1986) Sporadic food competition with the African honey bee: projected impact on neotropical social bees. J Trop Ecol 2(2):97–111.  https://doi.org/10.1017/S0266467400000699 CrossRefGoogle Scholar
  14. 14.
    van Tomé HV, Martins GF, Lima MAP, Campos LAO, Guedes RNC (2012) Imidacloprid-induced impairment of mushroom bodies and behavior of the native stingless bee Melipona quadrifasciata anthidioides. PLoS One 7(6).  https://doi.org/10.1371/journal.pone.0038406 CrossRefGoogle Scholar
  15. 15.
    Ferreira Junior NT, Blochtein B, de Moraes JF (2011) Seasonal flight and resource collection patterns of colonies of the stingless bee Melipona bicolor schencki Gribodo (Apidae, Meliponini) in an Araucaria forest area in southern Brazil. Rev Bras Entomol 54(4):630–636.  https://doi.org/10.1590/s0085-56262010000400015 CrossRefGoogle Scholar
  16. 16.
    Araujo ED, Oliveira RG, Calazans HCM et al (2016) Risk of local extinction and genetic diversity of Melipona quadrifasciata (Apidae: Meliponini) in a possible northeastern limit of its distribution in Brazil. Sociobiology 63(2):804–812.  https://doi.org/10.13102/sociobiology.v63i2.946 CrossRefGoogle Scholar
  17. 17.
    Ribéreau-Gayon P, Dubourdieu D, Donèche B, Lonvaud A (2006) Handbook of Enology. The chemistry of wine stabilization and treatments, vol 2. John Wiley.  https://doi.org/10.1002/0470010398 CrossRefGoogle Scholar
  18. 18.
    Ribereau-Gayon P, Dubourdieu D, Doneche B, Lonvaud A (2006) Handbook of Enology: The microbiology of wine and vinifications: Second Edition, vol 1, 2nd edn. John Wiley & Sons, LTDA, England.  https://doi.org/10.1002/0470010363 CrossRefGoogle Scholar
  19. 19.
    Carreto L, Eiriz MF, Gomes AC, Pereira PM, Schuller D, Santos MS (2008) Comparative genomics of wild type yeast strains unveils important genome diversity. BMC Genomics 9:524.  https://doi.org/10.1186/1471-2164-9-524 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Kurtzman CP, Fell JW, Boekhout T, Robert V (2011) In: Elsevier B (ed) The yeasts, a taxonomic study, vol 1, 3rd edn. Elsevier, B.V, Amsterdam.  https://doi.org/10.1016/B978-0-444-52149-1.00007-0 CrossRefGoogle Scholar
  21. 21.
    Lachance M-A (1990) Ribosomal DNA spacer variation in the cactophilic yeast Clavispora opuntiae. Mol Biol Evol 7(2):178–193Google Scholar
  22. 22.
    Meyer T, Rosa CA, Lachance M-A. The yeast genus Starmerek gen . nov . and Starmerella bombicola sp . nov ., the teleomorph of Candida bombicola (Spencer, Gorin & Tullock) Meyer & Yarrow. lnt J Syst Bacteriol. 1998;(48):1413-1417.Google Scholar
  23. 23.
    Scmidell W, Lima UA, Aquarone E, Borzani W (2001) Biotecnologia Industrial: Engenharia Bioquímica. Edgard Blücher, São PauloGoogle Scholar
  24. 24.
    Minitab Inc. Minitab, 2010.; 2010. doi: https://doi.org/10.1201/b15846.CrossRefGoogle Scholar
  25. 25.
    SILVA FAS. ASSISTAT 7.7 PT. 1996. http://www.assistat.com/indexp.html.
  26. 26.
    OriginLab Corporation. OriginPro. 2007. https://www.originlab.com/index.aspx?go = Products/Origin.
  27. 27.
    Morais P, Calaça PS, Rosa C (2013) Microorganisms associated with Stingless Bees. In: Vit P, Silvia RM, Roubik PD (eds) Pot-Honey: A Legacy of Stingless Bees, 1st edn. Springer, Australia, pp 173–186.  https://doi.org/10.1007/978-1-4614-4960-7_11 CrossRefGoogle Scholar
  28. 28.
    Ayala R, Gonzalez VH, Engel MS (2013) Mexican stingless bees (Himenoptera: Apidae): Diversity, distribution and indigenus knowledge. In: Pot-Honey: A Legacy of Stingless Bees, 1st edn. Springer, New York, pp 135–152.  https://doi.org/10.1007/978-1-4614-4960-7 CrossRefGoogle Scholar
  29. 29.
    Chuttong B, Chanbang Y, Sringarm K, Burgett M (2015) Physicochemical profiles of Stingless Bees (Apidae: Meliponini) Honey from South East Asia (Thailand). Food Chem 192:149–155.  https://doi.org/10.1016/j.foodchem.2015.06.089 CrossRefPubMedGoogle Scholar
  30. 30.
    Begum SB, Roobia RR, Karthikeyan M, Murugappan RM (2015) Validation of nutraceutical properties of honey and probiotic potential of its innate microflora. LWT - Food Sci Technol 60(2):743–750.  https://doi.org/10.1016/j.lwt.2014.10.024 CrossRefGoogle Scholar
  31. 31.
    Teixeira ACP, Marini MM, Nicoli JR et al (2003) Starmerella meliponinorum sp. nov., a novel ascomycetous yeast species associated with Stingless Bees. Int J Syst Evol Microbiol 53(1):339–343.  https://doi.org/10.1099/ijs.0.02262-0 CrossRefPubMedGoogle Scholar
  32. 32.
    Yurkov A, Guerreiro MA, Sharma L, Carvalho C, Fonseca Á. Multigene assessment of the species boundaries and sexual status of the Basidiomycetous yeasts Cryptococcus flavescens and C. terrestris (Tremellales). PLoS One. 2015;10(3).CrossRefGoogle Scholar
  33. 33.
    Surussawadee J, Khunnamwong P, Srisuk N, Limtong S (2014) Papiliotrema siamense f.a., sp. nov., a yeast species isolated from plant leaves. Int J Syst Evol Microbiol 64(2014):3058–3062.  https://doi.org/10.1099/ijs.0.065607-0 CrossRefPubMedGoogle Scholar
  34. 34.
    Jaiboon K, Lertwattanasakul N, Limtong P, Limtong S (2016) Yeasts from peat in a tropical peat swamp forest in Thailand and their ability to produce ethanol, indole-3-acetic acid and extracellular enzymes. Mycol Prog 15(7):755–770.  https://doi.org/10.1007/s11557-016-1205-9 CrossRefGoogle Scholar
  35. 35.
    Castanha RF, de Morais LAS, Pinto A, Mariano AP, Monteiro TR. Produção de lipídeos em culturas de leveduras utilizando resíduo de laticínios. In: 26 oCongresso Brasileiro de Microbiologia. Foz do Iguaçu - PR; 2011:722-2.Google Scholar
  36. 36.
    Aksu Z, Tuǧba EA (2005) Carotenoids production by the yeast Rhodotorula mucilaginosa: use of agricultural wastes as a carbon source. Process Biochem 40(9):2985–2991.  https://doi.org/10.1016/j.procbio.2005.01.011 CrossRefGoogle Scholar
  37. 37.
    Li M, Liu GL, Chi Z, Chi ZM (2010) Single cell oil production from hydrolysate of cassava starch by marine-derived yeast Rhodotorula mucilaginosa TJY15a. Biomass Bioenergy 34(1):101–107.  https://doi.org/10.1016/j.biombioe.2009.10.005 CrossRefGoogle Scholar
  38. 38.
    Li R, Zhang H, Liu W, Zheng X (2011) Biocontrol of postharvest gray and blue mold decay of apples with Rhodotorula mucilaginosa and possible mechanisms of action. Int J Food Microbiol 146(2):151–156.  https://doi.org/10.1016/j.ijfoodmicro.2011.02.015 CrossRefPubMedGoogle Scholar
  39. 39.
    Carvalho CM, Rocha A, Estevinho MLF, Choupina A (2005) Identification of honey yeast species based on rflp analysis of the its region. Cienc Tecnol Aliment 5(1):11–17.  https://doi.org/10.1080/11358120509487665 CrossRefGoogle Scholar
  40. 40.
    Reid VJ, Theron LW, Du Toit M, Divol B (2012) Identification and partial characterization of extracellular aspartic protease genes from Metschnikowia pulcherrima IWBT Y1123 and Candida apicola IWBT Y1384. Appl Environ Microbiol 78(19):6838–6849.  https://doi.org/10.1128/AEM.00505-12 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    la Torre-Gonzáleza FJD, Narváez-Zapataa JA, López-y-Lópezb VE, Larralde-Coronaa CP (2016) Ethanol tolerance is decreased by fructose in Saccharomyces and non-Saccharomyces yeasts. LWT - Food Sci Technol 67(April 2016):1–7CrossRefGoogle Scholar
  42. 42.
    Lewis JA, Elkon IM, McGee MA, Higbee AJ, Gasch AP (2010) Exploiting natural variation in Saccharomyces cerevisiae to identify genes for increased ethanol resistance. Genetics 186(4):1197–1205.  https://doi.org/10.1534/genetics.110.121871 CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Arroyo-López F, Salvadó Z, Tronchoni J, Guillamón JM, Barrio E, Querol A (2010) Susceptibility and resistance to ethanol in Saccharomyces strains isolated from wild and fermentative environments. Yeast 27(12):1005–1015.  https://doi.org/10.1002/yea CrossRefPubMedGoogle Scholar
  44. 44.
    Ding J, Huang X, Zhang L, Zhao N, Yang D, Zhang K (2009) Tolerance and stress response to ethanol in the yeast Saccharomyces cerevisiae. Appl Microbiol Biotechnol 85(2):253–263.  https://doi.org/10.1007/s00253-009-2223-1 CrossRefPubMedGoogle Scholar
  45. 45.
    Belloch C, Orlic S, Barrio E, Querol A (2008) Fermentative stress adaptation of hybrids within the Saccharomyces sensu stricto complex. Int J Food Microbiol 122(1-2):188–195.  https://doi.org/10.1016/j.ijfoodmicro.2007.11.083 CrossRefPubMedGoogle Scholar
  46. 46.
    Schimz K-L, Holzer H (1979) Rapid decrease of ATP content in intact cells of Saccharomyces cerevisiae after incubation with low concentrations of sulfite. Arch Microbiol 121(3):225–229.  https://doi.org/10.1007/BF00425059 CrossRefPubMedGoogle Scholar
  47. 47.
    Hinze H, Holzer H (1985) Effect of sulfite or nitrite on the ATP content and the carbohydrate metabolism in yeast. Z Lebensm Unters Forsch 181(2):87–91.  https://doi.org/10.1007/BF01042566 CrossRefPubMedGoogle Scholar
  48. 48.
    Europeia U (2009) REGULAMENTO (CE) N.o 606/2009 DA COMISSÃO de 10 de Julho de 2009. J Of da União Eur L193/1(6):1–59Google Scholar
  49. 49.
    Choudhary J, Singh S, Nain L (2016) Thermotolerant fermenting yeasts for simultaneous saccharification fermentation of lignocellulosic biomass. Electron J Biotechnol.  https://doi.org/10.1016/j.ejbt.2016.02.007 CrossRefGoogle Scholar
  50. 50.
    Walker GM, Dundee A (2009) Yeasts. Fungi Biol Appl:1174–1187Google Scholar
  51. 51.
    Malfeito-Ferreira M (2014) WINES | Wine spoilage yeasts and bacteria. In: Batt CA, Tortorello M-L (eds) Encyclopedia of food microbiology (Second Edition), 2nd edn. Elsevier Ltd, New York, pp 805–810.  https://doi.org/10.1016/B978-0-12-384730-0.00390-6 CrossRefGoogle Scholar
  52. 52.
    L’Enfant M, Domon JM, Rayon C et al (2015) Substrate specificity of plant and fungi pectin methylesterases: identification of novel inhibitors of PMEs. Int J Biol Macromol 81:681–691.  https://doi.org/10.1016/j.ijbiomac.2015.08.066 CrossRefPubMedGoogle Scholar
  53. 53.
    Scanes KT, Hohmann S, Prior B (1998) a. Glycerol production by the yeast Saccharomyces cerevisiae and its relevance to wine: a review. South African J Enol Vitic 19(1):17–24 http://www.sasev.org/journal-sajev/sajev-articles/volume-19-1/art3%5Cnglycerol%5Cnin%5Cnwine.pdf Google Scholar

Copyright information

© Sociedade Brasileira de Microbiologia 2019

Authors and Affiliations

  • Mayara Salgado Silva
    • 1
  • Luciana Marina Arruda
    • 2
  • Pedro Lanna Xavier
    • 2
  • Maria Ximena Díaz Ramírez
    • 2
  • Fernando Augusto da Silveira
    • 3
  • Weyder Cristiano Santana
    • 4
  • Paulo Henrique Alves da Silva
    • 2
  • Luciano Gomes Fietto
    • 5
  • Monique Renon Eller
    • 2
    Email author
  1. 1.Instituto Federal do CearáLimoeiro do NorteBrazil
  2. 2.Department of Food TechnologyUniversidade Federal de ViçosaViçosaBrazil
  3. 3.Department of MicrobiologyUniversidade Federal de ViçosaViçosaBrazil
  4. 4.Department of EntomologyUniversidade Federal de ViçosaViçosaBrazil
  5. 5.Department of Biochemistry and Molecular BiologyUniversidade Federal de ViçosaViçosaBrazil

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