Evaluation of some probiotic properties of yeast Rhodotorula mucilaginosa isolated from fermented buckwheat
Subject Areas :
Food Hygiene
S. Shahryari
1
(M.Sc. student of Food Biotechnology, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran)
A. Sadeghi
2
(Associate professor, Department of Food Science and Technology, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran)
M. Ebrahimi
3
(Assistant professor, Health Research Center of Food, Drug and Natural Products, Golestan University of Medical Science, Gorgan, Iran)
A. Sadeghi Mahoonak
4
(Professor, Department of Food Science and Technology, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran)
A. Moayedi
5
(Assistant professor, Department of food science and technology, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran)
Received: 2022-01-07
Accepted : 2022-03-13
Published : 2021-10-23
Keywords:
Probiotic properties,
Yeast isolate,
fermented buckwheat,
Abstract :
The study of the yeasts isolated from the least studied fermented sources may have the potential to deal with the unique isolates. In this study, one of the predominant yeasts was isolated from fermented buckwheat. The isolate was identified by amplifying the target sequence of 650 bp of its ITS gene and sequencing PCR products. Afterward, some potential probiotic features of the isolates, including survival in simulated gastrointestinal conditions, antibacterial effect, auto-aggregation, antibiotic resistance, antimycotic and hemolysis ability, as well as antifungal activity against Aspergillus niger and Aspergillus flavus were studied. Based on sequencing results of the PCR products, Rhodotorula mucilaginosa was identified as the yeast isolate. The isolate had 85.07% viability in simulated gastrointestinal conditions. The inhibitory effect of the isolate on Escherichia coli was significantly (P<0.05) higher than the other foodborne bacteria. The yeast isolate had 84.60% auto-aggregation and 60.10% hydrophobicity capabilities. However, no hemolytic activity was observed. The yeast isolate was resistant to all of the studied antibiotics, and it was sensitive towards Ketoconazole among the common antifungal agents. In conclusion, the yeast isolate had appropriate potential to be used as a probiotic culture to produce fermented food products.
References:
AACC International. (2010). Approved methods of the American association of cereal chemists. 11th The St. Paul.
Abdulla, A.A., Abed, T.A. and Saeed, A.M. (2014). Adhesion, auto-aggregation and hydrophobicity of six LactobacillusBritish Microbiology Research Journal, 4(4): 381-391.
Andrabi, S.T., Bhat, B., Gupta, M. and Bajaj, BK. (2016). Phytase-producing potential and other functional attributes of lactic acid bacteria isolates for prospective probiotic applications. Probiotics and Antimicrobial Proteins, 8(3):121-129.
Angmo, K., Kumari, A. and Bhalla, TC. (2016). Probiotic characterization of lactic acid bacteria isolated from fermented foods and beverage of Ladakh. LWT-Food Science and Technology, 66: 428-435.
Bajaj, B.K., Claes, I.J. and Lebeer, S. (2021). Functional mechanisms of probiotics. Journal of Microbiology, Biotechnology and Food Sciences, 2021: 321-327.
Banik, A., Mondal, J., Rakshit, S., Ghosh, K., Sha, S.P., Kumar Halder, S., et al. (2019). Amelioration of cold-induced gastric injury by a yeast probiotic isolated from traditional fermented foods. Journal of Functional Foods, 59: 164-173.
Bonatsou, S., Karamouza, M., Zoumpopoulou, G., Mavrogonatou, E., Kletsas, D. and Papadimitriou, K. (2018). Evaluating the probiotic potential and technological characteristics of yeasts implicated in cv. Kalamata natural black olive fermentation. International Journal of Food Microbiology, 271: 48-59.
Cai, Y., Luo, Q., Sun, M. and Corke, H. (2004). Antioxidant activity and phenolic compounds of 112 traditional Chinese medicinal plants associated with anticancer. Life Sciences, 74(17): 2157-2184.
Cavalero, D.A. and Cooper, D.G. (2003). The effect of medium composition on the structure and physical state of sophorolipids produced by Candida bombicola Journal of Biotechnology, 103(1): 31–41.
Cernicka, J., Kozovska, Z., Hnatova, M., Valachovic, m., Hapala, I., Riedl, Z., et al. (2007). Chemosensitisation of drug-resistant and drug-sensitive yeast cells to antifungals. International Journal of Antimicrobial Agents, 29(2): 170-178.
Chen, L.S., Ma, Y., Maubois, J.L., He, S.H., Chen, L.J. and Li, H.M. (2010). Screening for the potential probiotic yeast strains from raw milk to assimilate cholesterol. Dairy Science & Technology, 90(5): 537-548.
Czerucka, D., Piche, T. and Rampal, P. (2007). Review article: Yeast as probiotics: Saccharomyces boulardii. Alimentary Pharmacology & Therapeutics, 26(6): 767-778.
Fadda, M.E., Mossa, V., Deplano, M., Pisano, M.B. and Cosentino, S. (2017). In vitro screening of Kluyveromyces strains isolated from Fiore Sardo cheese for potential use as probiotics. LWT- Food Science and Technology, 75: 100-106.
Fakruddin, M.D., Hossain, M.N. and Ahmed, M.M. (2017). Antimicrobial and antioxidant activities of Saccharomyces cerevisiae IFST062013, a potential probiotic. BMC Complementary and Alternative Medicine, 17(1): 1-11.
Fekri, A., Torbati, M.A., Yari Khosrowshahi, A., Bagherpour Shamlood, H. and Azadmard-Damirchi, S. (2020). Functional effects of phytate-degrading, probiotic lactic acid bacteria and yeast strains isolated from Iranian traditional sourdough on the technological and nutritional properties of whole wheat bread. Food Chemistry, 306: 125620.
Fernandez-Pacheco, P., Arevalo-Villena, M., Bevilacqua, A., Corbo, M., and Beriones Perez, A. (2018). Probiotic characterization in Saccharomyces cerevisiae strains: application in food industries. LWT- Food Science and Technology, 97: 332-340.
Gil-Rodriguez, A.M., Carrascosa, A.V., and Requena, T. (2015). Yeasts in foods and beverages: In vitro characterization of probiotic traits. LWT- Food Science and Technology, 64: 1156-1162.
Goerges, S., Aigner, U., Silakowski, B. and Scherer, S. (2006). Inhibition of Listeria monocytogenes by foodborne yeasts. Applied and Environmental Microbiology, 72 (1): 313–318.
Goretti, M., Turchetti, B., Buratta, M., Branda, E., Corazzi, l., Vaughan-Martini, et al. (2009). In vitro antimycotic activity of a Williopsis saturnus killer protein against food spoilage yeasts. International Journal of Food Microbiology, 131(2-3): 178-182.
Hatoum, R., Labrie, S. and Fliss, I. (2013). Identification and partial characterization of antilisterial compounds produced by dairy yeasts. Probiotics and Antimicrobial Proteins, 5(1): 8-17.
Ilavenil, S., Vijayakumar, M., Kim, D.H., Arasu, M., Park, H.S. and Ravikumar, S. (2016). Assessment of probiotic, antifungal and cholesterol lowering properties of Pediococcus pentosaceus KCC-23 isolated from Italian Ryegrass. Journal of the Science of Food and Agriculture, 96(2): 593–601.
Janković, T., Frece, J., Abram, M. and Gobin, I. (2012). Aggregation ability of potential probiotic Lactobacillus plantarum International Journal of Sanitary Engineering Research, 6(1): 19-24.
Kanafani, Z.A. and Perfect, J.R. (2008). Resistance to antifungal agents: mechanisms and clinical impact. Clinical Infectious Diseases, 46(1): 120-128.
Kapetanakou, A.E., Kollias, J.N., Drosinos, E.H. and Skandamis, P.N. (2012). Inhibition of A. carbonarius growth and reduction of ochratoxin A by bacteria and yeast composites of technological importance in culture media and beverages. International Journal of Food Microbiology, 152(3): 91-99.
Magnusson, J., Ström, K., Roos, S., Sjögren, J. and Schnürer, J. (2003). Broad and complex antifungal activity among environmental isolates of lactic acid bacteria. FEMS Microbiology Letters, 219(1): 129-135.
Maia Danielski, G., Didimo Imazaki, P.H., Daube, G., Ernlund Freitas de Macedo, R. and Clinquart, A. (2017). In vitro evaluation of the competing effect of Carnobacterium maltaromaticum isolated from vacuum packed meat against food pathogens. BAMST Symposium: Meet the Belgian meat researchers, Melle 7th.
Montville, T.J. and Matthews, K.R. (2012). Physiology, growth, and inhibition of microbes in foods. Food Microbiology, Fundamentals and Frontiers, 1-18
Moroni, A.V., Arendt, E.K. and Dal Bello, F. (2011). Biodiversity of lactic acid bacteria and yeasts in spontaneously-fermented buckwheat and teff sourdoughs. Food Microbiology, 28(3): 497-502.
Palla, M., Agnolucci, M., Calzone, A., Giovannetti, M., Di Cagno, R., Gobbetti, M., et al. (2018). Exploitation of autochthonous Tuscan sourdough yeasts as potential starters. International Journal of Food Microbiology, 302: 59-68.
Perricone, M., Bevilacqua, A., Corbo, M. and 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 Microbiology, 38: 26-35.
Rima, H., Steve, L. and Ismail, I. (2012). Antimicrobial and probiotic properties of yeasts: from fundamental to novel applications. Frontiers in Microbiology, 3: 421.
Rojo-Bezares, B., Sáenz, Y., Poeta, P., Zarazaga, M., Ruiz-Larrea, F. and Torres, C. (2006). Assessment of antibiotic susceptibility within lactic acid bacteria strains isolated from wine. International Journal of Food Microbiology, 111(3): 234-240.
Rolim, F.R.L., dos Santos, K.M.O., de Barcelos, S.C., do Egito, A.S., Ribeiro, T.S. and da Conceição, M.L. (2015). Survival of Lactobacillus rhamnosus EM1107 in simulated gastrointestinal conditions and its inhibitory effect against pathogenic bacteria in semi-hard goat cheese. LWT- Food science and Technology, 63(2): 807-813.
Ruggirello, M., Nucera, D., Cannoni, M., Peraino, A., Rosso, F., Fontana, M., et al. (2019). Antifungal activity of yeasts and lactic acid bacteria isolated from cocoa bean fermentations. Food Research International, 115: 519-525.
Saad, N., Delattre, C., Urdaci, M., Schmitter, J.M. and Bressollier, P. (2013). An overview of the last advances in probiotic and prebiotic field. LWT- Food Science and Technology, 50(1): 1-16.
Saarela, M., Mogensen, G., Fonden, R., Mättö, J., and Mattila-Sandholm, T. (2000). Probiotic bacteria: safety, functional and technological properties. Journal of Biotechnology, 84(3): 197-215.
Sakandar, H.A., Usman, K. and Imran, M. (2018). Isolation and characterization of gluten-degrading and Wickerhamomyces anomalus, potential probiotic strains from indigenously fermented sourdough Enterococcus mundtii (Khamir). LWT- Food Science and Technology, 91: 271-277.
Suvarna, S., Dsouza, J., Ragavan, M. L. and Das, N. (2018). Potential probiotic characterization and effect of encapsulation of probiotic yeast strains on survival in simulated gastrointestinal tract condition. Food Science and Biotechnology, 27(3): 745-753.
White, T.J., Bruns, T., Lee, S.J.W.T. and Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR protocols: a guide to methods and applications, 18(1): 315-322.
Zullo, B.A. and Ciafardini, G. (2019). Evaluation of physiological properties of yeasts strains isolated from olive oil and their in vitro probiotic trait. Food Microbiology, 78: 179-187.
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AACC International. (2010). Approved methods of the American association of cereal chemists. 11th The St. Paul.
Abdulla, A.A., Abed, T.A. and Saeed, A.M. (2014). Adhesion, auto-aggregation and hydrophobicity of six LactobacillusBritish Microbiology Research Journal, 4(4): 381-391.
Andrabi, S.T., Bhat, B., Gupta, M. and Bajaj, BK. (2016). Phytase-producing potential and other functional attributes of lactic acid bacteria isolates for prospective probiotic applications. Probiotics and Antimicrobial Proteins, 8(3):121-129.
Angmo, K., Kumari, A. and Bhalla, TC. (2016). Probiotic characterization of lactic acid bacteria isolated from fermented foods and beverage of Ladakh. LWT-Food Science and Technology, 66: 428-435.
Bajaj, B.K., Claes, I.J. and Lebeer, S. (2021). Functional mechanisms of probiotics. Journal of Microbiology, Biotechnology and Food Sciences, 2021: 321-327.
Banik, A., Mondal, J., Rakshit, S., Ghosh, K., Sha, S.P., Kumar Halder, S., et al. (2019). Amelioration of cold-induced gastric injury by a yeast probiotic isolated from traditional fermented foods. Journal of Functional Foods, 59: 164-173.
Bonatsou, S., Karamouza, M., Zoumpopoulou, G., Mavrogonatou, E., Kletsas, D. and Papadimitriou, K. (2018). Evaluating the probiotic potential and technological characteristics of yeasts implicated in cv. Kalamata natural black olive fermentation. International Journal of Food Microbiology, 271: 48-59.
Cai, Y., Luo, Q., Sun, M. and Corke, H. (2004). Antioxidant activity and phenolic compounds of 112 traditional Chinese medicinal plants associated with anticancer. Life Sciences, 74(17): 2157-2184.
Cavalero, D.A. and Cooper, D.G. (2003). The effect of medium composition on the structure and physical state of sophorolipids produced by Candida bombicola Journal of Biotechnology, 103(1): 31–41.
Cernicka, J., Kozovska, Z., Hnatova, M., Valachovic, m., Hapala, I., Riedl, Z., et al. (2007). Chemosensitisation of drug-resistant and drug-sensitive yeast cells to antifungals. International Journal of Antimicrobial Agents, 29(2): 170-178.
Chen, L.S., Ma, Y., Maubois, J.L., He, S.H., Chen, L.J. and Li, H.M. (2010). Screening for the potential probiotic yeast strains from raw milk to assimilate cholesterol. Dairy Science & Technology, 90(5): 537-548.
Czerucka, D., Piche, T. and Rampal, P. (2007). Review article: Yeast as probiotics: Saccharomyces boulardii. Alimentary Pharmacology & Therapeutics, 26(6): 767-778.
Fadda, M.E., Mossa, V., Deplano, M., Pisano, M.B. and Cosentino, S. (2017). In vitro screening of Kluyveromyces strains isolated from Fiore Sardo cheese for potential use as probiotics. LWT- Food Science and Technology, 75: 100-106.
Fakruddin, M.D., Hossain, M.N. and Ahmed, M.M. (2017). Antimicrobial and antioxidant activities of Saccharomyces cerevisiae IFST062013, a potential probiotic. BMC Complementary and Alternative Medicine, 17(1): 1-11.
Fekri, A., Torbati, M.A., Yari Khosrowshahi, A., Bagherpour Shamlood, H. and Azadmard-Damirchi, S. (2020). Functional effects of phytate-degrading, probiotic lactic acid bacteria and yeast strains isolated from Iranian traditional sourdough on the technological and nutritional properties of whole wheat bread. Food Chemistry, 306: 125620.
Fernandez-Pacheco, P., Arevalo-Villena, M., Bevilacqua, A., Corbo, M., and Beriones Perez, A. (2018). Probiotic characterization in Saccharomyces cerevisiae strains: application in food industries. LWT- Food Science and Technology, 97: 332-340.
Gil-Rodriguez, A.M., Carrascosa, A.V., and Requena, T. (2015). Yeasts in foods and beverages: In vitro characterization of probiotic traits. LWT- Food Science and Technology, 64: 1156-1162.
Goerges, S., Aigner, U., Silakowski, B. and Scherer, S. (2006). Inhibition of Listeria monocytogenes by foodborne yeasts. Applied and Environmental Microbiology, 72 (1): 313–318.
Goretti, M., Turchetti, B., Buratta, M., Branda, E., Corazzi, l., Vaughan-Martini, et al. (2009). In vitro antimycotic activity of a Williopsis saturnus killer protein against food spoilage yeasts. International Journal of Food Microbiology, 131(2-3): 178-182.
Hatoum, R., Labrie, S. and Fliss, I. (2013). Identification and partial characterization of antilisterial compounds produced by dairy yeasts. Probiotics and Antimicrobial Proteins, 5(1): 8-17.
Ilavenil, S., Vijayakumar, M., Kim, D.H., Arasu, M., Park, H.S. and Ravikumar, S. (2016). Assessment of probiotic, antifungal and cholesterol lowering properties of Pediococcus pentosaceus KCC-23 isolated from Italian Ryegrass. Journal of the Science of Food and Agriculture, 96(2): 593–601.
Janković, T., Frece, J., Abram, M. and Gobin, I. (2012). Aggregation ability of potential probiotic Lactobacillus plantarum International Journal of Sanitary Engineering Research, 6(1): 19-24.
Kanafani, Z.A. and Perfect, J.R. (2008). Resistance to antifungal agents: mechanisms and clinical impact. Clinical Infectious Diseases, 46(1): 120-128.
Kapetanakou, A.E., Kollias, J.N., Drosinos, E.H. and Skandamis, P.N. (2012). Inhibition of A. carbonarius growth and reduction of ochratoxin A by bacteria and yeast composites of technological importance in culture media and beverages. International Journal of Food Microbiology, 152(3): 91-99.
Magnusson, J., Ström, K., Roos, S., Sjögren, J. and Schnürer, J. (2003). Broad and complex antifungal activity among environmental isolates of lactic acid bacteria. FEMS Microbiology Letters, 219(1): 129-135.
Maia Danielski, G., Didimo Imazaki, P.H., Daube, G., Ernlund Freitas de Macedo, R. and Clinquart, A. (2017). In vitro evaluation of the competing effect of Carnobacterium maltaromaticum isolated from vacuum packed meat against food pathogens. BAMST Symposium: Meet the Belgian meat researchers, Melle 7th.
Montville, T.J. and Matthews, K.R. (2012). Physiology, growth, and inhibition of microbes in foods. Food Microbiology, Fundamentals and Frontiers, 1-18
Moroni, A.V., Arendt, E.K. and Dal Bello, F. (2011). Biodiversity of lactic acid bacteria and yeasts in spontaneously-fermented buckwheat and teff sourdoughs. Food Microbiology, 28(3): 497-502.
Palla, M., Agnolucci, M., Calzone, A., Giovannetti, M., Di Cagno, R., Gobbetti, M., et al. (2018). Exploitation of autochthonous Tuscan sourdough yeasts as potential starters. International Journal of Food Microbiology, 302: 59-68.
Perricone, M., Bevilacqua, A., Corbo, M. and 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 Microbiology, 38: 26-35.
Rima, H., Steve, L. and Ismail, I. (2012). Antimicrobial and probiotic properties of yeasts: from fundamental to novel applications. Frontiers in Microbiology, 3: 421.
Rojo-Bezares, B., Sáenz, Y., Poeta, P., Zarazaga, M., Ruiz-Larrea, F. and Torres, C. (2006). Assessment of antibiotic susceptibility within lactic acid bacteria strains isolated from wine. International Journal of Food Microbiology, 111(3): 234-240.
Rolim, F.R.L., dos Santos, K.M.O., de Barcelos, S.C., do Egito, A.S., Ribeiro, T.S. and da Conceição, M.L. (2015). Survival of Lactobacillus rhamnosus EM1107 in simulated gastrointestinal conditions and its inhibitory effect against pathogenic bacteria in semi-hard goat cheese. LWT- Food science and Technology, 63(2): 807-813.
Ruggirello, M., Nucera, D., Cannoni, M., Peraino, A., Rosso, F., Fontana, M., et al. (2019). Antifungal activity of yeasts and lactic acid bacteria isolated from cocoa bean fermentations. Food Research International, 115: 519-525.
Saad, N., Delattre, C., Urdaci, M., Schmitter, J.M. and Bressollier, P. (2013). An overview of the last advances in probiotic and prebiotic field. LWT- Food Science and Technology, 50(1): 1-16.
Saarela, M., Mogensen, G., Fonden, R., Mättö, J., and Mattila-Sandholm, T. (2000). Probiotic bacteria: safety, functional and technological properties. Journal of Biotechnology, 84(3): 197-215.
Sakandar, H.A., Usman, K. and Imran, M. (2018). Isolation and characterization of gluten-degrading and Wickerhamomyces anomalus, potential probiotic strains from indigenously fermented sourdough Enterococcus mundtii (Khamir). LWT- Food Science and Technology, 91: 271-277.
Suvarna, S., Dsouza, J., Ragavan, M. L. and Das, N. (2018). Potential probiotic characterization and effect of encapsulation of probiotic yeast strains on survival in simulated gastrointestinal tract condition. Food Science and Biotechnology, 27(3): 745-753.
White, T.J., Bruns, T., Lee, S.J.W.T. and Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR protocols: a guide to methods and applications, 18(1): 315-322.
Zullo, B.A. and Ciafardini, G. (2019). Evaluation of physiological properties of yeasts strains isolated from olive oil and their in vitro probiotic trait. Food Microbiology, 78: 179-187.
