Skip to main content
Log in

Fermentative capabilities of native yeast strains grown on juices from different Agave species used for tequila and mezcal production

  • Biotechnology and Industrial Microbiology - Research Paper
  • Published:
Brazilian Journal of Microbiology Aims and scope Submit manuscript

Abstract

The Asparagaceae family is endemic from America, being the Agave genus the most important. The Agave species possess economic relevance and are use as raw material to produce several distilled alcoholic beverages, as bacanora, tequila, and mezcal. The fermentation process has been carry out either spontaneously or by adding a selected yeast strain. The latter is generally responsible for the production of ethanol and volatile compounds. This study comprised five Agave species (A. angustifolia, A. cupreata, A. durangensis, A. salmiana, and A. tequilana) and eight endogenous yeast strains: five of them were non-Saccharomyces (Torulaspora delbrueckii, Zygosaccharomyces bisporus, Candida ethanolica, and two Kluyveromyces marxianus) and three Saccharomyces cerevisiae strains. The results showed that the S. cerevisiae strains were not able to grow on A. durangensis and A. salmiana juices. The Kluyveromyces marxianus strains grew and fermented all the agave juices and displayed high ethanol production (48–52 g L−1) and volatile compounds. The ethanol production was higher on A. angustifolia juice (1.1–2.8-fold), whereas the volatile compound was dependent on both yeast strain and the Agave species. The use of endogenous non-Saccharomyces yeast strains is feasible, as they may outperform S. cerevisiae regarding the production of fermented beverages from agave plants with a high content of ethanol and aromatic compounds.

Graphical abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Good-Avila SV, Souza V, Gaut BS, Eguiarte LE (2006) Timing and rate of speciation in Agave (Agavaceae). Proc Natl Acad Sci 103(24):9124–9129. https://doi.org/10.1073/pnas.0603312103

    Article  CAS  PubMed  Google Scholar 

  2. Orozco-Cortes A, Alvarez-Manilla G, Sanchez-Gutierrez G, Rutiaga-Quinones O, Miranda-Lopez J, Soto-Cruz N (2015) Characterization of fructans from Agave durangensis. African J Plant Sci 9(9):360–367. https://doi.org/10.5897/AJPS2013.1007

    Article  CAS  Google Scholar 

  3. Colunga-GarcíaMarín P, Zizumbo-Villarreal D (2007) Tequila and other Agave spirits from west-central Mexico: current germplasm diversity, conservation and origin. Biodivers Conserv 16(6):1653–1667. https://doi.org/10.1007/s10531-006-9031-z

    Article  Google Scholar 

  4. Ávila-Fernández Á, Galicia-Lagunas N, Rodríguez-Alegría ME, Olvera C, López-Munguía A (2011) Production of functional oligosaccharides through limited acid hydrolysis of agave fructans. Food Chem 129(2):380–386. https://doi.org/10.1016/j.foodchem.2011.04.088

    Article  CAS  PubMed  Google Scholar 

  5. Lopez MG, Mancilla-Margalli NA, Mendoza-Diaz G (2003) Molecular structures of fructans from Agave tequilana Weber var. azul. J Agric Food Chem 51(27):7835–7840. https://doi.org/10.1021/jf030383v

    Article  CAS  PubMed  Google Scholar 

  6. Mart́inez-Aguilar JF, Peña-Álvarez A (2009) Characterization of five typical Agave plants used to produce mezcal through their simple lipid composition analysis by gas chromatography. J Agric Food Chem 57(5):1933–1939. https://doi.org/10.1021/jf802141d

    Article  CAS  PubMed  Google Scholar 

  7. Narvaez-Zapata J, Sanchez-Teyer L (2009) Agaves as a raw material: recent technologies and applications. Recent Patents Biotechnol 3:185–191. https://doi.org/10.2174/187220809789389144

    Article  CAS  Google Scholar 

  8. Consejo Regulador del Tequila. (2015) Información Estadística. Consum agave para Tequila y Tequila 100% agave. www.crt.mx. Accessed June 2016

  9. Consejo Regulador del Mezcal (2018). http://www.crm.org.mx/. Accessed November 7, 2018

  10. Kirchmayr MR, Segura-García LE, Lappe-Oliveras P, Moreno-Terrazas R, de la Rosa M, Gschaedler Mathis A (2017) Impact of environmental conditions and process modifications on microbial diversity, fermentation efficiency and chemical profile during the fermentation of Mezcal in Oaxaca. LWT Food Sci Technol 79:160–169. https://doi.org/10.1016/j.lwt.2016.12.052

    Article  CAS  Google Scholar 

  11. Arrizon J, Fiore C, Acosta G, Romano P, Gschaedler A (2006) Fermentation behaviour and volatile compound production by agave and grape must yeasts in high sugar Agave tequilana and grape must fermentations. Antonie van Leeuwenhoek, Int J Gen Mol Microbiol 89(1):181–189. https://doi.org/10.1007/s10482-005-9022-1

    Article  CAS  Google Scholar 

  12. López-Alvarez A, Díaz-Pérez AL, Sosa-Aguirre C, Macías-Rodríguez L, Campos-García J (2012) Ethanol yield and volatile compound content in fermentation of agave must by Kluyveromyces marxianus UMPe-1 comparing with Saccharomyces cerevisiae baker’s yeast used in tequila production. J Biosci Bioeng 113(5):614–618. https://doi.org/10.1016/j.jbiosc.2011.12.015

    Article  CAS  PubMed  Google Scholar 

  13. Segura-García LE, Taillandier P, Brandam C, Gschaedler A (2015) Fermentative capacity of Saccharomyces and non-Saccharomyces in agave juice and semi-synthetic medium. LWT Food Sci Technol 60(1):284–291. https://doi.org/10.1016/j.lwt.2014.08.005

    Article  CAS  Google Scholar 

  14. Fleet GH (2003) Yeast interactions and wine flavour. Int J Food Microbiol 86(1–2):11–22. https://doi.org/10.1016/S0168-1605(03)00245-9

    Article  CAS  PubMed  Google Scholar 

  15. Romano P, Fiore C, Paraggio M, Caruso M, Capece A (2003) Function of yeast species and strains in wine flavour. Int J Food Microbiol 86(1–2):169–180. https://doi.org/10.1016/S0168-1605(03)00290-3

    Article  CAS  PubMed  Google Scholar 

  16. Alcázar M, Kind T, Gschaedler A, Silveria M, Arrizon J, Fiehn O, Vallejo A, Higuera I, Lugo E (2017) Effect of steroidal saponins from Agave on the polysaccharide cell wall composition of Saccharomyces cerevisiae and Kluyveromyces marxianus. LWT Food Sci Technol 77:e1–e439. https://doi.org/10.1016/j.lwt.2016.11.048

  17. Arroyo-López FN, Querol A, Barrio E (2009) Application of a substrate inhibition model to estimate the effect of fructose concentration on the growth of diverse Saccharomyces cerevisiae strains. J Ind Microbiol Biotechnol 36(5):663–669. https://doi.org/10.1007/s10295-009-0535-x

    Article  CAS  PubMed  Google Scholar 

  18. Arellano M, Pelayo C, Ramírez J, Rodriguez I (2008) Characterization of kinetic parameters and the formation of volatile compounds during the tequila fermentation by wild yeasts isolated from agave juice. J Ind Microbiol Biotechnol 35(8):835–841. https://doi.org/10.1007/s10295-008-0355-4

    Article  CAS  PubMed  Google Scholar 

  19. Baccou JC, Lambert F, Sauvaire Y (1977) Spectrophotometric method for the determination of total steroidal sapogenin. Analyst. 102(1215):458–465. https://doi.org/10.1039/an9770200458

    Article  CAS  PubMed  Google Scholar 

  20. Chaney AL, Marbach EP (1962) Modified reagents for determination of urea and ammonia. Clin Chem 8:130–132. https://doi.org/10.1021/AC60252A045

    Article  CAS  PubMed  Google Scholar 

  21. Díaz-Montaño DM, Délia ML, Estarrón-Espinosa M, Strehaiano P (2008) Fermentative capability and aroma compound production by yeast strains isolated from Agave tequilana Weber juice. Enzym Microb Technol 42(7):608–616. https://doi.org/10.1016/j.enzmictec.2007.12.007

    Article  CAS  Google Scholar 

  22. Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31(3):426–428. https://doi.org/10.1021/ac60147a030

    Article  CAS  Google Scholar 

  23. Gutierrez-Pulido H, de la Vara R (2012) Analisis y Diseno de Experimentos. Mc Graw Hill Interamericana, Mexico

    Google Scholar 

  24. Little RJA, Rubin DB. (2002) Missing data in experiments. In: Statistical analysis with missing data 24–40. https://doi.org/10.1002/9781119013563.ch2

  25. Cira LA, Gonzáez GA, Torres JC, Pelayo C, Gutiérrez M, Ramírez J (2008) Heterologous expression of Fusarium oxysporum tomatinase in Saccharomyces cerevisiae increases its resistance to saponins and improves ethanol production during the fermentation of Agave tequilana Weber var. azul and Agave salmiana must. Antonie van Leeuwenhoek, Int J Gen Mol Microbiol 93(3):259–266. https://doi.org/10.1007/s10482-007-9200-4

    Article  CAS  Google Scholar 

  26. Escalante-Minakata P, Blaschek HP, Barba De La Rosa AP, Santos L, De León-Rodríguez A (2008) Identification of yeast and bacteria involved in the mezcal fermentation of Agave salmiana. Lett Appl Microbiol 46(6):626–630. https://doi.org/10.1111/j.1472-765X.2008.02359.x

    Article  CAS  PubMed  Google Scholar 

  27. Verdugo Valdez A, Segura Garcia L, Kirchmayr M, Ramírez Rodríguez P, González Esquinca A, Coria R, Gschaedler Mathis A (2011) Yeast communities associated with artisanal mezcal fermentations from Agave salmiana. Antonie van Leeuwenhoek, Int J Gen Mol Microbiol 100(4):497–506. https://doi.org/10.1007/s10482-011-9605-y

    Article  CAS  Google Scholar 

  28. Yang CR, Zhang Y, Jacob MR, Khan SI, Zhang YJ, Li XC (2006) Antifungal activity of C-27 steroidal saponins. Antimicrob Agents Chemother 50(5):1710–1714. https://doi.org/10.1128/AAC.50.5.1710-1714.2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Coleman JJ, Okoli I, Tegos GP, Holson EB, Wagner FF, Hamblin MR, Mylonakis E (2010) Characterization of plant-derived saponin natural products against candida albicans. ACS Chem Biol 5(3):321–332. https://doi.org/10.1021/cb900243b

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Ito S, Ihara T, Tamura H et al (2007) α-Tomatine, the major saponin in tomato, induces programmed cell death mediated by reactive oxygen species in the fungal pathogen Fusarium oxysporum. FEBS Lett 581(17):3217–3222. https://doi.org/10.1016/j.febslet.2007.06.010

    Article  CAS  PubMed  Google Scholar 

  31. Ruiz-Rubio M, PÉrez-Espinosa A, Lairini K, RoldÁn-Arjona T, Dipietro A, Anaya N (2001) Metabolism of the tomato saponin α-tomatine by phytopathogenic fungi. Stud Nat Prod Chem 25(PART F):293–326. https://doi.org/10.1016/S1572-5995(01)80010-7

    Article  CAS  Google Scholar 

  32. Fonseca GG, Gombert AK, Heinzle E, Wittmann C (2007) Physiology of the yeast Kluyveromyces marxianus during batch and chemostat cultures with glucose as the sole carbon source. FEMS Yeast Res 7(3):422–435. https://doi.org/10.1111/j.1567-1364.2006.00192.x

    Article  CAS  PubMed  Google Scholar 

  33. Lane MM, Morrissey JP (2010) Kluyveromyces marxianus: a yeast emerging from its sister’s shadow. Fungal Biol Rev 24(1–2):17–26. https://doi.org/10.1016/j.fbr.2010.01.001

    Article  Google Scholar 

  34. Lappe-Oliveras P, Moreno-Terrazas R, Arrizón-Gaviño J, Herrera-Suárez T, García-Mendoza A, Gschaedler-Mathis A. (2008) Yeasts associated with the production of Mexican alcoholic nondistilled and distilled Agave beverages. In: FEMS Yeast Research. 8:1037–1052. https://doi.org/10.1111/j.1567-1364.2008.00430.x

  35. Nonklang S, Abdel-Banat BMA, Cha-aim K, Moonjai N, Hoshida H, Limtong S, Yamada M, Akada R (2008) High-temperature ethanol fermentation and transformation with linear DNA in the thermotolerant yeast Kluyveromyces marxianus DMKU3-1042. Appl Environ Microbiol 74(24):7514–7521. https://doi.org/10.1128/AEM.01854-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Pinal L, Cedeño M, Gutiérrez H, Alvarez-Jacobs J (1997) Fermentation parameters influencing higher alcohol production in the tequila process. Biotechnol Lett 19(1):45–47. https://doi.org/10.1023/A:1018362919846

    Article  CAS  Google Scholar 

  37. Hernandez-Orte P, Cacho JF, Ferreira V (2002) Relationship between varietal amino acid profile of grapes and wine aromatic composition. Experiments with model solutions and chemometric study. J Agric Food Chem 50(10):2891–2899. https://doi.org/10.1021/jf011395o

    Article  CAS  PubMed  Google Scholar 

  38. Medeiros ABP, Pandey A, Freitas RJS, Christen P, Soccol CR (2000) Optimization of the production of aroma compounds by Kluyveromyces marxianus in solid-state fermentation using factorial design and response surface methodology. Biochem Eng J 6(1):33–39. https://doi.org/10.1016/S1369-703X(00)00065-6

    Article  CAS  PubMed  Google Scholar 

  39. Morrissey JP, Etschmann MMW, Schrader J, de Billerbeck GM (2015) Cell factory applications of the yeast Kluyveromyces marxianus for the biotechnological production of natural flavour and fragrance molecules. Yeast. 32(1):3–16. https://doi.org/10.1002/yea.3054

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Montserrat Alcazar would like to acknowledge CONACYT for the granted fellowship.

Funding

This work was supported by the National Research Council of Science and Technology of Mexico (Project SEP-CONACYT 24556).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. Arellano-Plaza.

Additional information

Responsible Editor: Eleni Gomes.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alcazar-Valle, M., Gschaedler, A., Gutierrez-Pulido, H. et al. Fermentative capabilities of native yeast strains grown on juices from different Agave species used for tequila and mezcal production. Braz J Microbiol 50, 379–388 (2019). https://doi.org/10.1007/s42770-019-00049-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42770-019-00049-7

Keywords

Navigation