Evaluation of Indigenous Pichia kudriavzevii from cocoa fermentation for a probiotic candidate
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Abstract. Wulan R, Astuti RI, Rukayadi Y, Meryandini A. 2021. Evaluation of Indigenous Pichia kudriavzevii from cocoa fermentation for a probiotic candidate. Biodiversitas 22: 1317-1325. Currently, probiotics are becoming a concern along with a healthy lifestyle awareness. Besides bacteria, yeast can be used as a probiotic candidate with specific functional properties. Research on yeast as a probiotic is still limited (except for Saccharomyces boulardii). Previous research has isolated yeasts from the cocoa fermentation process. This study aimed to evaluate the probiotics properties and antioxidant activity of yeast strains isolated from spontaneous cocoa fermentation in Sukabumi, Indonesia. Previous research has isolated 23 yeast strains from spontaneous cocoa (Theobroma cacao L.) fermentation. Of the 23 yeast strains isolated from cocoa fermentation, 22 strains showed negative hemolysis as an indicator of non-pathogenic properties. Ten yeast strains were able to grow at 37 °C and 41 °C, pH 3, 0.5% bile salts, had autoaggregation ability (63.99-95.33%), and co-aggregation with S. typhimurium ATCC14028 (>80%), as character requirement for probiotic candidates. The genetic identification of the ten yeast strains showed that they were 99% identical to Pichia kudriavzevii. Based on its antioxidant activity, the P. kudriavzevii 2P10 metabolites had the highest percentage of inhibition (68.51%) against DPPH free radicals and resistance to H2O2 oxidative stress up to 3 mM. It can be concluded that P. kudriavzevii 2P10 is a promising probiotic candidate for functional foods and health purposes.
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References
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Martins D, English AM. 2014. Catalase activity is stimulated by H2O2 in rich culture medium and is required for H2O2 resistance and adaptation in yeast. Redox Biol. 2(1):308–313.
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Moon SH, Chang M, Kim HY, Chang HC. 2014. Pichia kudriavzevii is the major yeast involved in film-formation, off-odor production, and texture-softening in over-ripened Kimchi. Food Sci Biotechnol. 23(2):489–497.
Nash AK, Auchtung TA, Wong MC, Smith DP, Gesell JR, Ross MC, Stewart CJ, Metcalf GA, Muzny DM, Gibbs RA, et al. 2017. The gut mycobiome of the Human Microbiome Project healthy cohort. Microbiome. 5(153):1–13.
Nayak AP, Green BJ, Beezhold DH. 2013. Fungal hemolysins. Med Mycol. 51(1):1–16.
Oja M, Maran U. 2015. The Permeability of an Artificial Membrane for Wide Range of pH in Human Gastrointestinal Tract: Experimental Measurements and Quantitative Structure-Activity Relationship. Mol Inform. 34(6–7):493–506.
Pereira GVM, Alvarez JP, Neto DP de C, Soccol VT, Tanobe VOA, Rogez H, Góes-Neto A, Soccol CR. 2017. Great intraspecies diversity of Pichia kudriavzevii in cocoa fermentation highlights the importance of yeast strain selection for flavor modulation of cocoa beans. LWT. 84:290–297.
Samagaci L, Ouattara HG, Goualié BG, Niamke SL. 2014. Growth capacity of yeasts potential starter strains under cocoa fermentation stress conditions in Ivory Coast. Emirates J Food Agric. 26(10):861–870.
Sanders ME, Merenstein D, Merrifield CA, Hutkins R. 2018. Probiotics for human use. Nutr Bull. 43(3):212–225.
Shahat AS. 2018. Antioxidant and Anticancer activities of yeast grown on commercial media. Int J Biol Chem Sci. 11(5):2442–2455.
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 30(12):2725–2729.
Urdaneta V, Casadesús J. 2017. Interactions between Bacteria and Bile Salts in the Gastrointestinal and Hepatobiliary Tracts. 4(163):1–13.
Yusuf SM. 2020. Aktivitas Ekstrak Xylocarpus granatum dan Senyawa Xyloccensins sebagai Agen Antiaging: Studi pada Schizosaccharomyces pombe [Thesis]. IPB University, Bogor. [Indonesian].
Aponte M, Murru N, Shoukat M. 2020. Therapeutic, prophylactic, and functional use of probiotics: a current perspective. Front Microbiol. 11(562048):1–16.
Ardhana MM, Fleet GH. 2003. The microbial ecology of cocoa bean fermentations in Indonesia. Int J Food Microbiol. 86(1–2):87–99.
Banwo K, Alonge Z, Sanni AI. 2020 Mei 20. Binding capacities and antioxidant activities of Lactobacillus plantarum and Pichia kudriavzevii against cadmium and lead toxicities. Biol Trace Elem Res.:1–13. doi:10.1007/s12011-020-02164-1.
Berutu CAM, Fahrurrozi F, Meryandini A. 2017. Pectinase production and clarification treatments of apple (Malus domestica) juice. Ann Bogor. 21(2):63–68.
Buxton R. 2005. Blood Agar Plates and Hemolysis Protocols.
Carstensen JW, Chehri M, Schønning K, Rasmussen SC, Anhøj J, Godtfredsen NS, Andersen CØ, Petersen AM. 2018. Use of prophylactic Saccharomyces boulardii to prevent Clostridium difficile infection in hospitalized patients: a controlled prospective intervention study. Eur J Clin Microbiol Infect Dis. 37(8):1431–1439.
Chamnipa N, Thanonkeo S, Klanrit P, Thanonkeo P. 2018. The potential of the newly isolated thermotolerant yeast Pichia kudriavzevii RZ8-1 for high-temperature ethanol production. Brazilian J Microbiol. 49(2):378–391.
Chelliah R, Ramakrishnan SR, Prabhu PR, Antony U. 2016. Evaluation of antimicrobial activity and probiotic properties of wild-strain Pichia kudriavzevii isolated from frozen idli batter. Yeast. 33(8):385–401.
Czerucka D, Piche T, Rampal P. 2007. Review article: Yeast as probiotics - Saccharomyces boulardii. Aliment Pharmacol Ther. 26(6):767–778.
Datta S, Timson DJ, Annapure US. 2017. Antioxidant properties and global metabolite screening of the probiotic yeast Saccharomyces cerevisiae var. boulardii. J Sci Food Agric. 97(9):3039–3049.
Delgado-Ospina J, Triboletti S, Alessandria V, Serio A, Sergi M, Paparella A, Rantsiou K, Chaves-López C. 2020. Functional biodiversity of yeasts isolated from Colombian fermented and dry cocoa beans. Microorganisms. 8(7):1–17.
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.
Fernandez-Pacheco Rodríguez P, Arévalo-Villena M, Zaparoli Rosa I, Briones Pérez A. 2018. Selection of potential non-Saccharomyces probiotic yeasts from food origin by a step-by-step approach. Food Res Int. 112:143–151.
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.
Greppi A, Saubade F, Botta C, Humblot C, Guyot JP, Cocolin L. 2017. Potential probiotic Pichia kudriavzevii strains and their ability to enhance folate content of traditional cereal-based African fermented food. Food Microbiol. 62:169–177.
Gut AM, Vasiljevic T, Yeager T, Donkor ON. 2019. Characterization of yeasts isolated from traditional kefir grains for potential probiotic properties. J Funct Foods. 58:56–66.
Helmy EA, Soliman SA, Abdel-Ghany TM, Ganash M. 2019. Evaluation of potentially probiotic attributes of certain dairy yeast isolated from buffalo sweetened Karish cheese. Heliyon. 5(5):1–9.
Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S, et al. 2014. Expert consensus document: The international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol. 11(8):506–514.
Hong SM, Kwon HJ, Park SJ, Seong WJ, Kim I, Kim JH. 2018. Genomic and probiotic characterization of SJP-SNU strain of Pichia kudriavzevii. AMB Express. 8(80):1–9.
Hsiung RT, Fang WT, LePage BA, Hsu SA, Hsu CH, Chou JY. 2020. In Vitro Properties of Potential Probiotic Indigenous Yeasts Originating from Fermented Food and Beverages in Taiwan. Probiotics Antimicrob Proteins..
Jamili, Yanti NA, Susilowati PE. 2016. Diversity and the role of yeast in spontaneous cocoa bean fermentation from Southeast Sulawesi, Indonesia. Biodiversitas. 17(1):90–95.
Johansen PG, Owusu-Kwarteng J, Parkouda C, Padonou SW, Jespersen L. 2019. Occurrence and importance of yeasts in indigenous fermented food and beverages produced in Sub-Saharan Africa. Front Microbiol. 10(1789):1–22.
Kurtzman CP. 2011. Pichia E.C: Hansen (1904). Di dalam: The Yeasts. Vol. 2. Elsevier. hlm. 685–707.
Ladha G, Jeevaratnam K. 2018. Probiotic potential of Pediococcus pentosaceus LJR1, a bacteriocinogenic strain isolated from rumen liquor of goat (Capra aegagrus hircus). Food Biotechnol. 32(1):60–77.
Martins D, English AM. 2014. Catalase activity is stimulated by H2O2 in rich culture medium and is required for H2O2 resistance and adaptation in yeast. Redox Biol. 2(1):308–313.
Menezes AGT, Ramos CL, Cenzi G, Melo DS, Dias DR, Schwan RF. 2019. Probiotic potential, antioxidant activity, and phytase production of indigenous yeasts isolated from indigenous fermented foods. Probiotics Antimicrob Proteins. 12:280–288.
Merchán A V., Benito MJ, Galván AI, Ruiz-Moyano Seco de Herrera S. 2020. Identification and selection of yeast with functional properties for future application in soft paste cheese. LWT. 124(109173).
Mogrovejo DC, Perini L, Gostin?ar C, Sep?i? K, Turk M, Ambroži?-Avguštin J, Brill FHH, Gunde-Cimerman N. 2020. Prevalence of Antimicrobial Resistance and Hemolytic Phenotypes in Culturable Arctic Bacteria. Front Microbiol. 11(570):1–13.
Moon SH, Chang M, Kim HY, Chang HC. 2014. Pichia kudriavzevii is the major yeast involved in film-formation, off-odor production, and texture-softening in over-ripened Kimchi. Food Sci Biotechnol. 23(2):489–497.
Nash AK, Auchtung TA, Wong MC, Smith DP, Gesell JR, Ross MC, Stewart CJ, Metcalf GA, Muzny DM, Gibbs RA, et al. 2017. The gut mycobiome of the Human Microbiome Project healthy cohort. Microbiome. 5(153):1–13.
Nayak AP, Green BJ, Beezhold DH. 2013. Fungal hemolysins. Med Mycol. 51(1):1–16.
Oja M, Maran U. 2015. The Permeability of an Artificial Membrane for Wide Range of pH in Human Gastrointestinal Tract: Experimental Measurements and Quantitative Structure-Activity Relationship. Mol Inform. 34(6–7):493–506.
Pereira GVM, Alvarez JP, Neto DP de C, Soccol VT, Tanobe VOA, Rogez H, Góes-Neto A, Soccol CR. 2017. Great intraspecies diversity of Pichia kudriavzevii in cocoa fermentation highlights the importance of yeast strain selection for flavor modulation of cocoa beans. LWT. 84:290–297.
Samagaci L, Ouattara HG, Goualié BG, Niamke SL. 2014. Growth capacity of yeasts potential starter strains under cocoa fermentation stress conditions in Ivory Coast. Emirates J Food Agric. 26(10):861–870.
Sanders ME, Merenstein D, Merrifield CA, Hutkins R. 2018. Probiotics for human use. Nutr Bull. 43(3):212–225.
Shahat AS. 2018. Antioxidant and Anticancer activities of yeast grown on commercial media. Int J Biol Chem Sci. 11(5):2442–2455.
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 30(12):2725–2729.
Urdaneta V, Casadesús J. 2017. Interactions between Bacteria and Bile Salts in the Gastrointestinal and Hepatobiliary Tracts. 4(163):1–13.
Yusuf SM. 2020. Aktivitas Ekstrak Xylocarpus granatum dan Senyawa Xyloccensins sebagai Agen Antiaging: Studi pada Schizosaccharomyces pombe [Thesis]. IPB University, Bogor. [Indonesian].
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