Skip to main content

Advertisement

SpringerLink
Log in

Probiotic Potential, Antioxidant Activity, and Phytase Production of Indigenous Yeasts Isolated from Indigenous Fermented Foods

  • Published:
Probiotics and Antimicrobial Proteins Aims and scope Submit manuscript

Abstract

While many bacteria have been used as probiotics by industries, only two yeasts, Saccharomyces cerevisiae var. boulardii and Kluyveromyces fragilis (B0399), have been used for this purpose. In the present work, a total of 116 yeasts isolated from Brazilian indigenous fermented food, cocoa fermentation, and kefir were in vitro characterized for probiotic attributes. From 116 isolates, 36 were tolerant to gastrointestinal conditions evaluated by tolerance to pH 2.0, bile salts (0.3% w/v), and 37 °C temperature. From those, 15 isolates showed a similar or higher percentage (P < 0.05) of hydrophobicity, autoaggregation, and coaggregation with E. coli than the reference strain S. boulardii. All these strains showed a high percentage of adhesion to Caco-2 cells (> 63%) and antioxidant activity (ranging from 18 to 62%). Phytate hydrolysis was evaluated for these yeasts and 13 strains showed positive results, which is important for nutrient availability in plant-based foods. These results are important insights for characterization of novel probiotic yeast strains as well as to aggregate functional value to these food products.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Rivera-Espinoza Y, Gallardo-Navarro Y (2010) Non-dairy probiotic products. Food Microbiol 27:1–11. https://doi.org/10.1016/j.fm.2008.06.008

    Article  PubMed  Google Scholar 

  2. Food and Agriculture Organization of the United Nations - FAO; World Health Organization - WHO (2002) Guidelines for the evaluation of probiotics in food. Report of a Joint FAO/WHO Working Group on Drafting Guidelines for the Evaluation of Probiotics in Food

  3. Andrabi ST, Bhat B, Gupta M, Bajaj BK (2016) Phytase-producing potential and other functional attributes of lactic acid Bacteria isolates for prospective probiotic applications. Probiotics Antimicrob Proteins 8:121–129. https://doi.org/10.1007/s12602-016-9220-3

    Article  CAS  PubMed  Google Scholar 

  4. Chen P, Zhang Q, Dang H, Liu X, Tian F, Zhao J, Chen Y, Zhang H, Chen W (2014) Screening for potential new probiotic based on probiotic properties and a -glucosidase inhibitory activity. Food Control 35:65–72. https://doi.org/10.1016/j.foodcont.2013.06.027

    Article  CAS  Google Scholar 

  5. Czerucka D, Piche T, Rampal P (2007) Review article : yeast as probiotics – Saccharomyces boulardii. Aliment Pharmacol Ther 26(6):767–778. https://doi.org/10.1111/j.1365-2036.2007.03442.x

  6. Generoso SV, Viana M, Santos R, Martins FS, Machado JAN, Arantes RME, Nicoli JR, Correia MITD, Cardoso VN (2010) Saccharomyces cerevisiae strain UFMG 905 protects against bacterial translocation, preserves gut barrier integrity and stimulates the immune system in a murine intestinal obstruction model. Arch Microbiol 192:477–484. https://doi.org/10.1007/s00203-010-0574-8

    Article  CAS  PubMed  Google Scholar 

  7. Klingberg TD, Lesnik U, Arneborg N, Raspor P, Jespersen L (2008) Comparison of Saccharomyces cerevisiae strains of clinical and nonclinical origin by molecular typing and determination of putative virulence traits. FEMS Yeast Res 8:631–640. https://doi.org/10.1111/j.1567-1364.2008.00365.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Silva T, Reto M, Sol M, Peito A, Peres CM, Peres C, Malcata FX (2011) Characterization of yeasts from Portuguese brined olives, with a focus on their potentially probiotic behavior. LWT - Food Sci Technol 44:1349–1354. https://doi.org/10.1016/j.lwt.2011.01.029

    Article  CAS  Google Scholar 

  9. Ramos CL, Thorsen L, Schwan RF, Jespersen L (2013) Strain-specific probiotics properties of Lactobacillus fermentum, Lactobacillus plantarum and Lactobacillus brevis isolates from Brazilian food products. Food Microbiol 36:22–29. https://doi.org/10.1016/j.fm.2013.03.010

    Article  CAS  PubMed  Google Scholar 

  10. Saito VST, Dos Santos TF, Vinderola CG et al (2014) Viability and resistance of lactobacilli isolated from cocoa fermentation to simulated gastrointestinal digestive steps in soy yogurt. J Food Sci 79:M208–M213. https://doi.org/10.1111/1750-3841.12326

    Article  CAS  PubMed  Google Scholar 

  11. Leite a MO, Miguel M a L, Peixoto RS et al (2015) Probiotic potential of selected lactic acid bacteria strains isolated from Brazilian kefir grains. J Dairy Sci 98:3622–3632. https://doi.org/10.3168/jds.2014-9265

    Article  CAS  PubMed  Google Scholar 

  12. Perricone M, Bevilacqua A, Corbo MR, Sinigaglia M (2014) Technological characterization and probiotic traits of yeasts isolated from Altamura sourdough to select promising microorganisms as functional starter cultures for cereal-based products. Food Microbiol 38:26–35. https://doi.org/10.1016/j.fm.2013.08.006

    Article  CAS  PubMed  Google Scholar 

  13. Pedersen LL, Owusu-Kwarteng J, Thorsen L, Jespersen L (2012) Biodiversity and probiotic potential of yeasts isolated from Fura, a west African spontaneously fermented cereal. Int J Food Microbiol 159:144–151. https://doi.org/10.1016/j.ijfoodmicro.2012.08.016

    Article  CAS  PubMed  Google Scholar 

  14. Miguel MGDCP, Cardoso PG, Lago LDA, Schwan RF (2010) Diversity of bacteria present in milk kefir grains using culture-dependent and culture-independent methods. Food Res Int 43:1523–1528. https://doi.org/10.1016/j.foodres.2010.04.031

    Article  Google Scholar 

  15. Ramos CL, De AEG, Freire AL, Schwan RF (2011) Diversity of bacteria and yeast in the naturally fermented cotton seed and rice beverage produced by Brazilian Amerindians. Food Microbiol 28:1380–1386. https://doi.org/10.1016/j.fm.2011.06.012

    Article  CAS  PubMed  Google Scholar 

  16. Santos CCADA, De Almeida EG, De Melo GVP, Schwan RF (2012) Microbiological and physicochemical characterisation of caxiri, an alcoholic beverage produced by the indigenous Juruna people of Brazil. Int J Food Microbiol 156:112–121. https://doi.org/10.1016/j.ijfoodmicro.2012.03.010

    Article  CAS  PubMed  Google Scholar 

  17. Moreira IMDV, Miguel MGDCP, Duarte WF et al (2013) Microbial succession and the dynamics of metabolites and sugars during the fermentation of three different cocoa (Theobroma cacao L.) hybrids. Food Res Int 54:9–17. https://doi.org/10.1016/j.foodres.2013.06.001

    Article  CAS  Google Scholar 

  18. Ramos CL, de Sousa ESO, Ribeiro J et al (2015) Microbiological and chemical characteristics of tarubá, an indigenous beverage produced from solid cassava fermentation. Food Microbiol 49:182–188. https://doi.org/10.1016/j.fm.2015.02.005

    Article  CAS  PubMed  Google Scholar 

  19. Bevilacqua A, Perricone M, Cannarsi M, Corbo MR, Sinigaglia M (2009) Technological and spoiling characteristics of the yeast microflora isolated from Bella di Cerignola table olives. Int J Food Sci Technol 44:2198–2207. https://doi.org/10.1111/j.1365-2621.2009.02060.x

    Article  CAS  Google Scholar 

  20. Binetti a, Carrasco M, Reinheimer J, Suárez V (2013) Yeasts from autochthonal cheese starters: technological and functional properties. J Appl Microbiol 115:434–444. https://doi.org/10.1111/jam.12228

    Article  CAS  PubMed  Google Scholar 

  21. Kos B, Šušković J, Vuković S, Šimpraga M, Frece J, Matošić S (2003) Adhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M92. J Appl Microbiol 94:981–987. https://doi.org/10.1046/j.1365-2672.2003.01915.x

    Article  CAS  PubMed  Google Scholar 

  22. Pieniz S, Andreazza R, Anghinoni T, Camargo F, Brandelli A (2014) Probiotic potential, antimicrobial and antioxidant activities of Enterococcus durans strain LAB18s. Food Control 37:251–256. https://doi.org/10.1016/j.foodcont.2013.09.055

    Article  CAS  Google Scholar 

  23. Chen L-S, Ma Y, Maubois J-L et al (2010) Identifcation of yeasts from raw milk and selection for some specific antioxidant properties. Int J Dairy Technol 63:47–54. https://doi.org/10.1111/j.1471-0307.2009.00548.x

    Article  CAS  Google Scholar 

  24. Ries EF, Macedo GA (2009) Progressive screening of thermostable yeasts for phytase production. Food Sci Biotechnol 18:655–660

    CAS  Google Scholar 

  25. Fadda ME, Mossa V, Deplano M, Pisano MB, Cosentino S (2017) In vitro screening of Kluyveromyces strains isolated from Fiore Sardo cheese for potential use as probiotics. LWT - Food Sci Technol 75:100–106. https://doi.org/10.1016/j.lwt.2016.08.020

    Article  CAS  Google Scholar 

  26. Almeida EG, Rachid CCTC, Schwan RF (2007) Microbial population present in fermented beverage “cauim” produced by Brazilian Amerindians. Int J Food Microbiol 120:146–151. https://doi.org/10.1016/j.ijfoodmicro.2007.06.020

    Article  CAS  PubMed  Google Scholar 

  27. Magalhães KT, Pereira GV de M, Campos CR et al (2011) Brazilian kefir: structure, microbial communities and chemical composition. Braz J Microbiol 42:693–702. https://doi.org/10.1590/S1517-83822011000200034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Kechagia M, Basoulis D, Konstantopoulou S, Dimitriadi D, Gyftopoulou K, Skarmoutsou N, Fakiri EM (2013) Health benefits of probiotics: a review. ISRN Nutr 2013:481651–481657. https://doi.org/10.5402/2013/481651

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Collado MC, Meriluoto J, Salminen S (2008) Adhesion and aggregation properties of probiotic and pathogen strains. Eur Food Res Technol 226:1065–1073. https://doi.org/10.1007/s00217-007-0632-x

    Article  CAS  Google Scholar 

  30. García-Cayuela T, Korany AM, Bustos I, P. Gómez de Cadiñanos L, Requena T, Peláez C, Martínez-Cuesta MC (2014) Adhesion abilities of dairy Lactobacillus plantarum strains showing an aggregation phenotype. Food Res Int 57:44–50. https://doi.org/10.1016/j.foodres.2014.01.010

    Article  CAS  Google Scholar 

  31. Gil-Rodríguez AM, Carrascosa AV, Requena T (2015) Yeasts in foods and beverages: in vitro characterisation of probiotic traits. LWT - Food Sci Technol 64:1156–1162. https://doi.org/10.1016/j.lwt.2015.07.042

    Article  CAS  Google Scholar 

  32. Ogunremi OR, Agrawal R, Sanni AI (2015) Development of cereal-based functional food using cereal-mix substrate fermented with probiotic strain - Pichia kudriavzevii OG32. Food Sci Nutr 3:486–494. https://doi.org/10.1002/fsn3.239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Moslehi-Jenabian S, Gori K, Jespersen L (2009) AI-2 signalling is induced by acidic shock in probiotic strains of Lactobacillus spp. Int J Food Microbiol 135:295–302. https://doi.org/10.1016/j.ijfoodmicro.2009.08.011

    Article  CAS  PubMed  Google Scholar 

  34. Fischer MM, Egli IM, Aeberli I, Hurrell RF, Meile L (2014) Phytic acid degrading lactic acid bacteria in tef-injera fermentation. Int J Food Microbiol 190:54–60. https://doi.org/10.1016/j.ijfoodmicro.2014.08.018

    Article  CAS  PubMed  Google Scholar 

  35. Nuobariene L, Hansen ÅS, Arneborg N (2012) Isolation and identification of phytase-active yeasts from sourdoughs. LWT - Food Sci Technol 48:190–196. https://doi.org/10.1016/j.lwt.2012.03.011

    Article  CAS  Google Scholar 

  36. Saikia D, Manhar AK, Deka B, Roy R, Gupta K, Namsa ND, Chattopadhyay P, Doley R, Mandal M (2016) Hypocholesterolemic activity of indigenous probiotic isolate Saccharomyces cerevisiae ARDMC1 in a rat model. J Food Drug Anal 6:4–9. https://doi.org/10.1016/j.jfda.2016.12.017

    Article  CAS  Google Scholar 

  37. Gheziel C, Russo P, Arena MP, Spano G, Ouzari HI, Kheroua O, Saidi D, Fiocco D, Kaddouri H, Capozzi V (2018) Evaluating the Probiotic Potential of Lactobacillus plantarum Strains from Algerian Infant Feces: Towards the Design of Probiotic Starter Cultures Tailored for Developing Countries. Probiotics Antimicrob Proteins. https://doi.org/10.1007/s12602-018-9396-9

Download references

Acknowledgements

The authors thank to the CCMA for providing the strains used in this work.

Funding Sources

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

Author information

Authors and Affiliations

  1. Biology Department, Federal University of Lavras, CEP, Lavras, MG, 37200-000, Brazil

    Aline Galvão Tavares Menezes, Gisele Cenzi, Dirceu Sousa Melo & Rosane Freitas Schwan

  2. Department of Basic Science, Federal University of Vales do Jequitinhonha e Mucuri, CEP, Diamantina, MG, 39100-000, Brazil

    Cíntia Lacerda Ramos

  3. Food Science Department, Federal University of Lavras, CEP, Lavras, MG, 37200-000, Brazil

    Disney Ribeiro Dias

Authors
  1. Aline Galvão Tavares Menezes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cíntia Lacerda Ramos
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gisele Cenzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dirceu Sousa Melo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Disney Ribeiro Dias
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rosane Freitas Schwan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rosane Freitas Schwan.

Ethics declarations

Conflicts of Interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

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

Electronic supplementary material

ESM 1

(DOCX 18.8 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Menezes, A.G.T., Ramos, C.L., Cenzi, G. et al. Probiotic Potential, Antioxidant Activity, and Phytase Production of Indigenous Yeasts Isolated from Indigenous Fermented Foods. Probiotics & Antimicro. Prot. 12, 280–288 (2020). https://doi.org/10.1007/s12602-019-9518-z

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-019-9518-z

Keywords

Search

Navigation