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Selection of potentially probiotic Kluyveromyces lactis for the fermentation of cheese whey–based beverage

  • Daelen Resende Oliveira
  • Ana Claudia Alencar Lopes
  • Rafaela Andrade Pereira
  • Patricia Gomes Cardoso
  • Whasley Ferreira DuarteEmail author
Original Article
  • 21 Downloads

Abstract

Purpose

This work aimed to assess the probiotic potential of different Kluyveromyces lactis strains isolated from Canastra cheese and to produce a fermented cheese whey beverage added to beetroot juice using the selected strain.

Methods

Kluyveromyces lactis strains were tested for their resistance to the passage through the simulated gastrointestinal tract, adhesion properties, and functional effects such as inhibition of enteric pathogens, short-chain fatty acids (SCFA) production, and β-galactosidase activity. The selected strain was used to produce a fermented cheese whey beverage added to beetroot juice in different proportions. The produced beverages were characterized using HPLC for sugars, Folin-Ciocalteu for total phenolic content, DPPH for antioxidant activity, and GC-MS for volatiles compounds.

Results

Except B51, all strains showed viability above 75% after exposure to the simulated gastric and duodenal juices. The aggregation rates were above 84% in 24 h. Only B9 and C16 strains presented hydrophobicity above 60%. The highest B9 β-galactosidase activities were 2.17 U/g and 2.21 U/g for pH 7 and 9, respectively. The B9 SCFA profile was similar to that found for Saccharomyces bourllardi. The fermented cheese whey beverages presented phenolic content ranging from 102.75 to 291.61 μg EAG/mL and inhibition of DPPH ranging from 38.69 to 81.02% after 21 days of storage, besides being lactose free. Esters and acetates were the most abundant compounds.

Conclusions

Kluyveromyces lactis B9 presented interesting results as a potential probiotic yeast. The produced beverages allowed the delivery of K. lactis B9 through innovative product with functional properties.

Keywords

β-Galactosidase Functional beverages Antioxidant activity Volatile compounds 

Notes

Funding information

This study was financially supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001, Conselho Nacional de Desenvolvimento Científico e Tecnológico do Brasil (CNPq), and Fundação de Amparo à Pesquisa de MG (FAPEMIG).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving human participants and/or animals

This study did not involve human participants or animals.

Informed consent

The authors mutually agree with the submission of the manuscript to Annals of Microbiology.

References

  1. Aloglu HS, Ozer ED, Oner Z (2016) Assimilation of cholesterol and probiotic characterization of yeast strains isolated from raw milk and fermented foods. Int J Dairy Technol 69:63–70CrossRefGoogle Scholar
  2. Alves Z, Melo A, Figueiredo AR, Coimbra MA, Gomes AC, Rocha SM (2015) Exploring the Saccharomyces cerevisiae volatile metabolome: indigenous versus commercial strains. PLoS ONE 10(11):e0143641CrossRefPubMedPubMedCentralGoogle Scholar
  3. Amorim JC, Piccoli RH, Duarte WF (2018) Probiotic potential of yeasts isolated from pineapple and their use in the elaboration of potentially functional fermented beverages. Food Res Int 107:518–527CrossRefPubMedGoogle Scholar
  4. Andrade RP, Melo CN, Genisheva Z, Schwan RF, Duarte WF (2017) Yeasts from Canastra cheese production process: isolation and evaluation of their potential for cheese whey fermentation. Food Res Int 91:72–79CrossRefPubMedGoogle Scholar
  5. Beards E, Tuohy K, Gibson G (2010) Bacterial, SCFA and gas profiles of a range of food ingredients following in vitro fermentation by human colonic microbiota. Anaerobe 16:420–425CrossRefPubMedPubMedCentralGoogle Scholar
  6. Cardoso VM, Borelli BM, Lara CA, Soares MA, Pataro C, Bodevan EC, Rosa CA (2015) The influence of seasons and ripening time on yeast communities of a traditional Brazilian cheese. Food Res Int 69:331–340CrossRefGoogle Scholar
  7. Ceugniez A, Drider D, Jacques P, Coucheney F (2015) Yeast diversity in a traditional French cheese “Tommed’orchies” reveals infrequent and frequent species with associated benefits. Food Microbiol 52:177–184CrossRefPubMedGoogle Scholar
  8. Ceugniez A, Coucheney F, Jacques P, Daube G, Delcenserie V, Drider D (2017) Anti-Salmonella activity and probiotic trends of Kluyveromyces marxianus S-2-05 and Kluyveromyces lactis S-3-05 isolated from a French cheese, Tommed’Orchies. Res Microbiol 168:575–582CrossRefPubMedGoogle Scholar
  9. Chen LS, Ma Y, Maubois JL, Chen LJ, Liu QH, Guo JP (2010a) Identification of yeasts from raw milk and selection for some specific antioxidant properties. Int J Dairy Technol 63:47–54CrossRefGoogle Scholar
  10. Chen LS, Ma Y, Maubois JL, He SH, Chen LJ, Li HM (2010b) Screening for the potential probiotic yeast strains from raw milk to assimilate cholesterol. Dairy Sci Technol 90:537–548CrossRefGoogle Scholar
  11. Chen G, Xie M, Wan P, Chen D, Ye H, Chen L, Liu Z (2018) Digestion under saliva, simulated gastric and small intestinal conditions and fermentation in vitro by human intestinal microbiota of polysaccharides from Fuzhuan brick tea. Food Chem 244:331–339CrossRefPubMedGoogle Scholar
  12. Costa MGM, Fonteles TV, De Jesus ALT, Rodrigues S (2013) Sonicated pineapple juice as substrate for L. casei cultivation for probiotic beverage development: process optimization and product stability. Food Chem 139:261–266CrossRefPubMedGoogle Scholar
  13. Costa GP, Nicolli KP, Welke JE, Manfroi V, Zini CA (2018) Volatile profile of sparkling wines produced with the addition of mannoproteins or lees before second fermentation performed with free and immobilized yeasts. J Braz Chem Soc 29:1866–1875Google Scholar
  14. Cummings JH, Macfarlane GT (2002) Gastrointestinal effects of prebiotics. Br J Nutr 87:145–151CrossRefGoogle Scholar
  15. Cummings J, Pomare EW, Branch WJ, Naylor CP, Macfarlane GT (1987) Short-chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut 28:1221–1227CrossRefPubMedPubMedCentralGoogle Scholar
  16. Czerny M, Christbauer M, Christbauer M, Fischer A, Granvogl M, Hammer M, Hartl C, Hernandez NM, Schieberle P (2008) Re-investigation on odour thresholds of key food aroma compounds and development of an aroma language based on odour qualities of defined aqueous odorant solutions. Eur Food Res Technol 228:265–273CrossRefGoogle Scholar
  17. Di T, Chen G, Sun Y, Ou S, Zeng X, Ye H (2018) In vitro digestion by saliva, simulated gastric and small intestinal juices and fermentation by human fecal microbiota of sulfated polysaccharides from Gracilaria rubra. J Funct Foods 40:18–27CrossRefGoogle Scholar
  18. Diosma G, Romanin DE, Rey-Burusco M, Londero A, Garrote GL (2014) Yeasts from kefir grains: isolation, identification, and probiotic characterization. World J Microbiol Biotechnol 30:43–53CrossRefPubMedGoogle Scholar
  19. Duarte WF, Dias DR, Oliveira JM, Teixeira JA, de Almeida JBS, Schwan RF (2010) Raspberry (Rubus idaeus L.) wine: yeast selection, sensory evaluation and instrumental analysis of volatile and other compounds. Food Res Int 43:2303–2314CrossRefGoogle Scholar
  20. Escudero-López B, Cerrillo I, Gil-Izquierdo Á, Hornero-Méndez D, Herrero-Martín G, Berná G, Fernández-Pachón MS (2016) Effect of thermal processing on the profile of bioactive compounds and antioxidant capacity of fermented orange juice. Int J Food Sci Nutr 67:779–788CrossRefPubMedGoogle Scholar
  21. 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 75:100–106CrossRefGoogle Scholar
  22. FAO and WHO (2002) Guidelines for the evaluation of probiotics in food. [internet document] URL http://www.fao.org/es/ESN/Probio/probio.htm/. Accessed 10/11/2013.
  23. Gänzle MG, Haase G, Jelen P (2008) Lactose: crystallization, hydrolysis and value-added derivatives. Int Dairy J 18:685–694CrossRefGoogle Scholar
  24. Gibson GR, Probert HM, Van Loo J, Rastall RA, Roberfroid MB (2004) Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutr Res Rev 17:259–275CrossRefPubMedGoogle Scholar
  25. Guyton AC, Hall JE (2011) Tratado de Fisiologia Médica. Elsevier, Rio de JaneiroGoogle Scholar
  26. Haraguchi FK, Abreu WC, Paula HD (2006) Proteínas do soro do leite: composição, propriedades nutricionais, aplicações no esporte e benefícios para a saúde humana. Rev Nutr 19:479–488CrossRefGoogle Scholar
  27. Hatoum R, Labrie S, Fliss I (2012) Antimicrobial and probiotic properties of yeasts: from fundamental to novel applications. Front Microbiol 3:1–12CrossRefGoogle Scholar
  28. Kiefer I, Prock P, Lawrence C, Wise J, Bieger W, Bayer P, Rieder A (2004) Supplementation with mixed fruit and vegetable juice concentrates increased serum antioxidants and folate in healthy adults. J Am Coll Nutr 23:205–211CrossRefPubMedGoogle Scholar
  29. Kos B, Susković J, Vuković S, Simpraga M, Frece J, Matosi S (2003) Adhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M92. J Appl Microbiol 94:981–987CrossRefPubMedGoogle Scholar
  30. Kumura H, Tanoue Y, Tsukahara M, Tanaka T, Shimazaki K (2004) Screening of dairy yeast strains for probiotic applications. J Dairy Sci 87:4050–4056CrossRefPubMedGoogle Scholar
  31. Ledauphin J, Guichard H, Saint-Clair JF, Picoche B, Barillier D (2003) Chemical and sensorial aroma characterization of freshly distilled calvados. 2. Identification of volatile compounds and key odorants. J Agric Food Chem 51:433–442CrossRefPubMedGoogle Scholar
  32. Maccaferri S, Klinder A, Brigidi P, Cavina P, Costabile A (2012) Potential probiotic Kluyveromyces marxianus B0399 modulates the immune response in Caco-2 cells and peripheral blood mononuclear cells and impacts the human gut microbiota in an in vitro colonic model system. Appl Environ Microbiol 78:956–964CrossRefPubMedPubMedCentralGoogle Scholar
  33. Mäkeläinen HS, Mäkivuokko HA, Salminen SJ, Rautonen NE, Ouwehand AC (2007) The effects of polydextrose and xylitol on microbial community and activity in a 4-stage colon simulator. J Food Sci 72:M153–M159CrossRefPubMedGoogle Scholar
  34. Meilgaard MC (1975) Flavor chemistry of beer: Part II: flavor and threshold of 239 aroma volatiles. MBAA Techn Q 12:151–168Google Scholar
  35. Park SC, Hwang MH, Kim YH, Kim JC, Song JC, Lee KW, Kim TW (2006) Comparison of pH and bile resistance of Lactobacillus acidophilus strains isolated from rat, pig, chicken, and human sources. World J Microbiol Biotechnol 22:35–37CrossRefGoogle Scholar
  36. Patel S (2015) Functional food relevance of whey protein: a review of recent findings and scopes ahead. J Funct Foods 19:308–319CrossRefGoogle Scholar
  37. Pitalua E, Jimenez M, Vernon-Carter EJ, Beristain CI (2010) Antioxidative activity of microcapsules with beetroot juice using gum Arabic as wall material. Food Bioprod Process 88:253–258CrossRefGoogle Scholar
  38. Rajkowska K, Kunicka-Styczynsk A (2010) Probiotic properties of yeasts isolated from chicken feces and kefirs. Pol J Microbiol 59:257–263PubMedGoogle Scholar
  39. Ravichandran K, Ahmed AR, Knorr D, Smetanska I (2012) The effect of different processing methods on phenolic acid content and antioxidant activity of red beet. Food Res Int 48:16–20CrossRefGoogle Scholar
  40. Richards LB, Li M, Van Esch BCAM, Garssen J, Folkerts G (2016) The effects of short-chain fatty acids on the cardiovascular system. Pharma Nutr 49:68–111Google Scholar
  41. Saber A, Alipour B, Faghfoori Z, Khosroushahi AY (2017) Secretion metabolites of dairy Kluyveromyces marxianus AS41 isolated as probiotic, induces apoptosis in different human cancer cell lines and exhibit anti-pathogenic effects. J Funct Foods 34:408–421CrossRefGoogle Scholar
  42. Siebert TE, Smyth HE, Capone DL, Neuwöhoner C, Pardon KH, Skouroumounis GK, Herderich MJ, Sefton MA, Pollnitz AP (2005) Stable isotope dilution analysis of wine fermentation products by HS-SPME-GC-MS. Anal Bioanal Chem 381:937–947CrossRefPubMedGoogle Scholar
  43. Soares RD, Welke JE, Nicolli, KP, Zanus M (2015) Monitoring the evolution of volatile compounds using gas chromatography during the stages of production of Moscatel sparkling wine. Food Chem 183: 291–304Google Scholar
  44. Song C, Liu GL, Xu JL, Chi ZM (2010) Purification and characterization of extracellular β-galactosidase from the psychrotolerant yeast Guehomyces pullulans 17-1 isolated from sea sediment in Antarctica. Process Biochem 45:954–960CrossRefGoogle Scholar
  45. Spohner SC, Schaum V, Quitmann H, Czermak P (2016) Kluyveromyces lactis: an emerging tool in biotechnology. J Biotechnol 222:104–116CrossRefPubMedGoogle Scholar
  46. Syal P, Vohra A (2013) Probiotic potential of yeasts isolated from traditional Indian fermented foods. Int J Microbiol Res 5:390–398CrossRefGoogle Scholar
  47. Wootton-Beard PC, Ryan L (2011) A beetroot juice shot is a significant and convenient source of bioaccessible antioxidants. J Funct Foods 3:329–334CrossRefGoogle Scholar
  48. Wruss J, Waldenberger G, Huemer S, Uygun P, Lanzerstorfer P, Müller U, Weghuber J (2015) Compositional characteristics of commercial beetroot products and beetroot juice prepared from seven beetroot varieties grown in Upper Austria. J Food Compos Anal 42:46–55CrossRefGoogle Scholar
  49. Zheng X, Li K, Shi X, Ni Y, Li B, Zhuge B (2018) Potential characterization of yeasts isolated from Kazak artisanal cheese to produce flavoring compounds. Microbiologyopen 7:e00533CrossRefGoogle Scholar

Copyright information

© Università degli studi di Milano 2019

Authors and Affiliations

  1. 1.Department of BiologyUniversity of Lavras (UFLA)LavrasBrazil

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