Isolation of microorganisms from Kazakh dairy products with antagonistic activity against yeast species from the Candida genus
DOI:
https://doi.org/10.26577/eb-2019-2-1421Abstract
An increase in the number of severe candidiasis, the growing incidence of antimicrobial resistance of the pathogens responsible for these infections, as well as their harmful side effects, necessitate developing new and more effective antifungal agents. In this context, the elaboration and utilization of functional fermented milk products with microorganisms harbouring antifungal activity and thus promoting the elimination of opportunistic Candida yeasts from the body, could be of great interest. The microbiota of Kazakh national sour-milk beverages derived from mare's and camel's milk has a multidirectional health effect on the human body, but the antagonistic activity of members of these microbiota against yeast species responsible for candidiasis have not yet been studied.
The aim of this work was to isolate microorganisms, with antagonistic activity against Candida yeast species from Kazakh national fermented milk beverages.
The study of antagonistic activities of various dairy products of local (both domestic and commercial) production against C. albicans using well-diffusion assays showed effective suppression of yeast growth with homemade koumiss samples. Associations of microorganisms from various koumiss samples also showed antagonistic activities after performing successive inoculations and fermentations of cow's milk and whey. When cultured in cow's milk, these associations had an increased activity against C. krusei 25. The highest antagonistic activity against C. glabrata 589 was found for three associations cultured in whey. After plating the most promising associations on MRS media, 41 bacteria with were isolated from selected associations based on their colony morphotype, 28 of which were lactic acid bacteria, while the other were presumptive acetic bacteria. Thirty-four yeast isolates were also selected.
In the present study, autochthonous strains of microorganisms that inhibited Candida spp. growth, including Candida strains exhibiting a high resistance to both lactic acid bacteria metabolites (intestinal and vaginal isolates of C. albicans) and antifungal antibiotic fluconazole (C. glabrata 589 and S. krusei 25), were selected for the first time. The isolated microorganisms will be used to create consortia and apply as starters to develop new functional beverages with antifungal activity against opportunistic Candida yeast species.
Key words/phrases: koumiss, lactic acid bacteria, Candida yeast antagonists.
References
1 Шевяков М.А. Диагностика и лечение кандидоза кишечника // Терапевтический архив, 2003, №11. - С. 77-79.
2 Gouba N., Drancourt M. Digestive tract mycobiota: A source of infection // Médecine et maladies infectieuses. – 2015. – Vol. 45. – P. 9–16.
3 Coogan M.M., Fidel P.L., Komesu M.C., Maeda L.P. Candida and mycotic infections // Adv. Dent. Res. – 2006. – Vol. 19. – P. 130-138.
4 Clark T. A., Hajjeh R. A. Recent trends in the epidemiology of invasive mycoses // Curr. Opin. Infect. Dis. 2002. – Vol. 15. – P. 569–574.
5 Segal E. Candida, still number one – what do we know and where are we going from there? // Mycoses. – 2005. – Vol. 48, Issue s1. – P. 3-11.
6 Jyoti B., Suresh A.K., Venkatesh K. Diacetyl production and growth of Lactobacillus rhamnosus on multiple substrates // World J Microbiol Biotechnol. – 2003. – Vol. 19. – P. 509–515.
7 Lanciotti R., Patrignani F., Bagnolini F., Guerzoni M.E., Gardini F. Evaluation of diacetyl antimicrobial activity against Escherichia coli, Listeria monocytogenes and Staphylococcus aureus // Food Microbiol. – 2003. – Vol. 20. – P. 537–543.
8 Schnürer, J., Magnusson J. Antifungal lactic acid bacteria as biopreservatives // Trends Food Sci. Technol. – 2005. – Vol. 16. – P. 70–78.
9 Dalié D.K.D., Deschamps A.M., Richard-Forget F. Lactic acid bacteria—Potential for control of mould growth and mycotoxins: A review // Food Control. – 2010. – Vol. 21. – P. 370–380.
10 Crowley S., Mahony, J., van Sinderen D. Current perspectives on antifungal lactic acid bacteria as natural bio-preservatives // Trends Food Sci. Technol. – 2013. – Vol. 33. – P. 93–109.
11 Le Lay C., Coton E., Le Blay G., Chobert J. M., Haertlé Th., Choiset Y., Van Long N. N., Meslet-Cladière L., Mounier J. Identification and quantification of antifungal compounds produced by lactic acid bacteria and propionibacteria // International Journal of Food Microbiology. – 2016. - Vol. 239. – P. 79-85.
12 Pothuraju R., Sharma R.K. Interplay of gut microbiota, probiotics in obesity: a review // Endocrine, metabolic and immune disorders-drug targets. – 2018. – Vol. 18. – P. 212–220.
13 Vijayaram S., Kannan S. Probiotics: the marvelous factor and health benefits // Biomed Biotechnol Res J. - 2018. – Vol. 2. – P. 1–8.
14 Wagner R.D., Johnson S.J. Probiotic lactobacillus and estrogen effects on vaginal epithelial gene expression responses to Candida albicans // J Biomed Sci. – 2012. – Vol. 19. – P. 58.
15 Ranadheera C.S., Evans C. A., Adams M. C., Baines S. K. Effect of dairy probiotic combinations on in vitro gastrointestinal tolerance, intestinal epithelial cell adhesion and cytokine secretion // J Funct Foods. – 2014. – Vol. 8. – P. 18–25.
16 Matsubara V. H., Wang Y., Bandara H. M., Mayer M. P., Samaranayake L. P. Probiotic lactobacilli inhibit early stages of Candida albicans biofilm development by reducing their growth, cell adhesion, and filamentation // Appl Microbiol Biotechnol. – 2016. – Vol. 100(14). – P. 6415-6426.
17 Tan Y., Leonhard M., Moser D., Ma S., Schneider-Stickler B. Inhibitory effect of probiotic lactobacilli supernatants on single and mixed non-albicans Candida species biofilm // Archives of Oral Biology. – 2018. –Vol. 85. – P. 40-45.
18 Aartia Ch., Khusroa A., Vargheseb R., Arasuc M. V., Agastiana P., Al-Dhabic N. A., Ilavenild S., Choid K. Ch. // In vitro investigation on probiotic, anti-Candida, and antibiofilm properties of Lactobacillus pentosus strain LAP1// Archives of Oral Biology. – 2018. - Vol. 89. - P. 99-106.
19 Cross M. L. Microbes versus microbes: immune signals generated by probiotic lactobacilli and their role in protection against microbial pathogens // FEMS Immunology and Medical Microbiology. – 2002. – Vol. 34, Issue 4. – P. 245-253.
20 Kanmani P., Kumar R. S., Yuvaraj N., Paari K.A., Pattukumar V., Arul V. Probiotics and its functionally valuable products-a review // Crit. Rev. Food Sci. Nutr. – 2013. – Vol. 53. – P. 641e658.
21 Delavenne E., Mounier J., Déniel F., Barbier G., Le Blay G. Biodiversity of antifungal lactic acid bacteria isolated from raw milk samples from cow, ewe and goat over one-year period // Int J Food Microbiol. – 2012. – Vol. 155(3). – P.185-190.
22 Song Y. G., Lee S. H. Inhibitory effects of Lactobacillus rhamnosus and Lactobacillus casei on Candida biofilm of denture surface // Arch Oral Biol. – 2017. – Vol. 76. – P. 1-6.
23 Prabhurajeshwar C., Chandrakanth R.K. Probiotic potential of Lactobacilli with antagonistic activity against pathogenic strains: an in vitro validation for the production of inhibitory substances // Biom J. – 2017. – Vol. 40. – P. 270–283.
24 Шигаева М.Х, Оспанова М.Ш. Микрофлора национальных кисломолочных напитков. - Алма-Ата: Наука, 1983. - 150 с.
25 Ермолаева А.Н., Алгожина У.Ж., Тен О.А., Балпанов Д.С. Изучение культур молочнокислых микроорганизмов, выделенных из кумыса различных регионов Северного Казахстана // Биотехнология. Теория и практика. – 2012. – №3. – С. 87-90.
26 Баубекова А.С., Конуспаева Г.С., Ахметсадыкова Ш.Н., Ахметсадыков Н.Н. Подготовка промышленного производства заквасок– выделение и идентификация бактерий для кумыса и шубата // Вестник КазНУ. Серия биологическая. №1/2 (60). - 2014. – С. 178-181.
27 Ringo E., Andersen R., Sperstad S., Zhou Zh., Ren P., Breines E.M., Hareide E., Yttergård G.J., Opsal K., Johansen H.M., Andreassen A.K., Kousha A., Godfroid J., Holzapfel W.Bacterial Community of koumiss from Mongolia investigated by culture and culture-independent methods // Food Biotechnology. - 2014. - Vol. 28. – P. 333–353.
28 Yao G., Yu J., Hou Q., Hui W., Liu W., Kwok L.-Y., Menghe B., Sun T., Zhang H., Zhang W. A Perspective Study of Koumiss Microbiome by Metagenomics Analysis Based on Single-Cell Amplification Technique // Frontiers in microbiology. – 2017. – Vol. 8. – Art. 165.
29 Behera S.K., Panda S.K., Kayitesi E., Mulaba-Bafubiandi A.F. Kefir and Koumiss. Origin, Health Benefits and Current Status of Knowledge // Ramesh C. Ray and Didier Montet (eds.) Fermented Food—Part II: Technological Interventions. – Boca Raton, London, New York: CRC Press, 2017. – P. 400-417.
30 Oleinikova E.A., Aitzhanova A.A., Saubenova M.G., Amangeldy A.A., Kebekbaeva, Elubaeva M.E. Isolation and selection of lactic acid bacteria antagonistically active against opportunistic Candida yeast // Микробиология және вирусология. – 2018. - № 3(22). – С. 103-109.
31 Magnusson J., Schnurer J. Lactobacillus coryniformis subsp. coryniformis strain Si3 produces a broad-spectrum proteinaceous antifungal compound // Applied Environ. Microbiol. - 2001. – Vol. 67. – P. 1-5.
32 Иркитова А.Н., Каган Я.Р., Соколова Г.Г. Сравнительный анализ методов определения антагонистической активности молочнокислых бактерий // Известия Алтайского государственного университета. – 2012. - № 3-1. – С. 41-44.
33 Черкасов С.В., Семенов А.В. Микробная регуляция антагонистической активности лактобактерий // Сибирский медицинский журнал. – 2012. - №2. – С. 78-82.
34 Иркитова А.Н., Каган Я.Р., Соколова Г.Г. Сравнительный анализ методов определения антагонистической активности молочнокислых бактерий // Известия АлтГУ. – 2012. - №3-1. URL: https://cyberleninka.ru/article/n/sravnitelnyy-analiz-metodov-opredeleniya-antagonisticheskoy-aktivnosti-molochnokislyh-bakteriy
35 Гланц С. Медико-биологическая статистика. - М.: Практика, 1998. – С. 459.
36 Лысак, В. В. Микробиология. Практикум: пособие / В. В. Лысак, Р. А. Желдакова, О. В. Фомина. – Минск : БГУ, 2015. – C. 34.
References
1 Shevjakov M.A. (2003) Diagnostika i lechenie kandidoza kishechnika [Diagnosis and treatment of intestinal candidiasis]. Terapevticheskij arhiv, no 11, pp. 77-79.
2 Gouba N., Drancourt M. (2015) Digestive tract mycobiota: A source of infection. Médecine et maladies infectieuses, vol. 45, pp. 9–16.
3 Coogan M.M., Fidel P.L., Komesu M.C., Maeda L.P. (2006) Candida and mycotic infections. Adv. Dent. Res., vol. 19, pp. 130-138.
4 Clark T. A., Hajjeh R. A. (2002) Recent trends in the epidemiology of invasive mycoses. Curr. Opin. Infect. Dis.. vol. 15, pp. 569–574.
5 Segal E. (2005) Candida, still number one – what do we know and where are we going from there? Mycoses. vol. 48, Issue s1, pp. 3-11.
6 Jyoti B., Suresh A.K., Venkatesh K. (2003) Diacetyl production and growth of Lactobacillus rhamnosus on multiple substrates. World J Microbiol Biotechnol., vol. 19, pp. 509–515.
7 Lanciotti R., Patrignani F., Bagnolini F., Guerzoni M.E., Gardini F. (2003) Evaluation of diacetyl antimicrobial activity against Escherichia coli, Listeria monocytogenes and Staphylococcus aureus. Food Microbiol., vol. 20, pp. 537–543.
8 Schnürer, J., Magnusson J. Antifungal lactic acid bacteria as biopreservatives (2005) Trends Food Sci. Technol., vol. 16, pp. 70–78.
9 Dalié D.K.D., Deschamps A.M., Richard-Forget F. (2010) Lactic acid bacteria—Potential for control of mould growth and mycotoxins: A review. Food Control., vol. 21, pp. 370–380.
10 Crowley S., Mahony, J., van Sinderen D. (2013) Current perspectives on antifungal lactic acid bacteria as natural bio-preservatives. Trends Food Sci. Technol., vol. 33, pp. 93–109.
11 Le Lay C., Coton E., Le Blay G., Chobert J. M., Haertlé Th., Choiset Y., Van Long N. N., Meslet-Cladière L., Mounier J. (2016) Identification and quantification of antifungal compounds produced by lactic acid bacteria and propionibacteria. International Journal of Food Microbiology., vol. 239, pp. 79-85.
12 Pothuraju R., Sharma R.K. (2018) Interplay of gut microbiota, probiotics in obesity: a review. Endocrine, metabolic and immune disorders-drug targets, vol. 18, pp. 212–220.
13 Vijayaram S., Kannan S. Probiotics: the marvelous factor and health benefits (2018) Biomed Biotechnol Res J., vol. 2, pp. 1–8.
14 Wagner R.D., Johnson S.J. (2012) Probiotic lactobacillus and estrogen effects on vaginal epithelial gene expression responses to Candida albicans. J Biomed Sci., vol. 19, pp. 58.
15 Ranadheera C.S., Evans C. A., Adams M. C., Baines S. K. (2014) Effect of dairy probiotic combinations on in vitro gastrointestinal tolerance, intestinal epithelial cell adhesion and cytokine secretion. J Funct Foods., vol. 8, pp. 18–25.
16 Matsubara V. H., Wang Y., Bandara H. M., Mayer M. P., Samaranayake L. P. (2016) Probiotic lactobacilli inhibit early stages of Candida albicans biofilm development by reducing their growth, cell adhesion, and filamentation. Appl Microbiol Biotechnol., vol. 100(14), pp. 6415-6426.
17 Tan Y., Leonhard M., Moser D., Ma S., Schneider-Stickler B. (2018) Inhibitory effect of probiotic lactobacilli supernatants on single and mixed non-albicans Candida species biofilm. Archives of Oral Biology., vol. 85., pp. 40-45.
18 Aartia Ch., Khusroa A., Vargheseb R., Arasuc M. V., Agastiana P., Al-Dhabic N. A., Ilavenild S., Choid K. Ch. (2018) In vitro investigation on probiotic, anti-Candida, and antibiofilm properties of Lactobacillus pentosus strain LAP1.. Archives of Oral Biology, vol. 89, - pp. 99-106.
19 Cross M. L. (2002) Microbes versus microbes: immune signals generated by probiotic lactobacilli and their role in protection against microbial pathogens. FEMS Immunology and Medical Microbiology, vol. 34, Issue 4, pp. 245-253.
20 Kanmani P., Kumar R. S., Yuvaraj N., Paari K.A., Pattukumar V., Arul V. (2013) Probiotics and its functionally valuable products-a review. Crit. Rev. Food Sci. Nutr., vol. 53, pp. 641e658.
21 Delavenne E., Mounier J., Déniel F., Barbier G., Le Blay G. (2012) Biodiversity of antifungal lactic acid bacteria isolated from raw milk samples from cow, ewe and goat over one-year period. Int J Food Microbiol., vol. 155(3), pp.185-190.
22 Song Y. G., Lee S. H. (2017) Inhibitory effects of Lactobacillus rhamnosus and Lactobacillus casei on Candida biofilm of denture surface. Arch Oral Biol., vol. 76, pp. 1-6.
23 Prabhurajeshwar C., Chandrakanth R.K. (2017) Probiotic potential of Lactobacilli with antagonistic activity against pathogenic strains: an in vitro validation for the production of inhibitory substances. Biom J, vol. 40, pp. 270–283.
24 Shigaeva M.H, Ospanova M.Sh. (1983) Mikroflora nacional'nyh kislomolochnyh napitkov [Microflora of national fermented milk drinks]. Alma-Ata: Nauka. 150 s.
25 Ermolaeva A.N., Algozhina U.Zh., Ten O.A., Balpanov D.S. (2012) Izuchenie kul'tur molochnokislyh mikroorganizmov, vydelennyh iz kumysa razlichnyh regionov Severnogo Kazahstana [Study of cultures of lactic acid microorganisms isolated from koumiss from various regions of Northern Kazakhstan]. Biotehnologija. Teorija i praktika, no 3, pp. 87-90.
26 Baubekova A.S., Konuspaeva G.S., Ahmetsadykova Sh.N., Ahmetsadykov N.N. (2014) Podgotovka promyshlennogo proizvodstva zakvasok– vydelenie i identifikacija bakterij dlja kumysa i shubata [Preparation of starter industrial production - isolation and identification of bacteria for koumiss and shubat]. Vestnik KazNU. Serija biologicheskaja, no 1/2 (60), pp. 178-181.
27 Ringo E., Andersen R., Sperstad S., Zhou Zh., Ren P., Breines E.M., Hareide E., Yttergård G.J., Opsal K., Johansen H.M., Andreassen A.K., Kousha A., Godfroid J., Holzapfel W.Bacterial (2014) Community of koumiss from Mongolia investigated by culture and culture-independent methods. Food Biotechnology, vol. 28, pp. 333–353.
28 Yao G., Yu J., Hou Q., Hui W., Liu W., Kwok L.-Y., Menghe B., Sun T., Zhang H., Zhang W. (2017) A Perspective Study of Koumiss Microbiome by Metagenomics Analysis Based on Single-Cell Amplification Technique. Frontiers in microbiology, vol. 8, Art. 165.
29 Behera S.K., Panda S.K., Kayitesi E., Mulaba-Bafubiandi A.F. (2017) Kefir and Koumiss. Origin, Health Benefits and Current Status of Knowledge. In: Ramesh C. Ray and Didier Montet (eds.) Fermented Food—Part II: Technological Interventions. Boca Raton, London, New York: CRC Press, pp. 400-417.
30 Oleinikova E.A., Aitzhanova A.A., Saubenova M.G., Amangeldy A.A., Kebekbaeva, Elubaeva M.E. (2018) Isolation and selection of lactic acid bacteria antagonistically active against opportunistic Candida yeast. Mikrobiologija zhәne virusologija, no. 3(22), pp. 103-109.
31 Magnusson J., Schnurer J. (2001) Lactobacillus coryniformis subsp. coryniformis strain Si3 produces a broad-spectrum proteinaceous antifungal compound. Applied Environ. Microbiol., vol. 67, pp. 1-5.
32 Irkitova A.N., Kagan Ja.R., Sokolova G.G. (2012) Sravnitel'nyj analiz metodov opredelenija antagonisticheskoj aktivnosti molochnokislyh bakterij [Comparative analysis of methods for determining the antagonistic activity of lactic acid bacteria]. Izvestija Altajskogo gosudarstvennogo universiteta, no 3-1, pp. 41-44.
33 Cherkasov S.V., Semenov A.V. (2012) Mikrobnaja reguljacija antagonisticheskoj aktivnosti laktobakterij [Microbial regulation of the antagonistic activity of lactobacilli]. Sibirskij medicinskij zhurnal, no 2, pp. 78-82.
34 Irkitova A.N., Kagan Ja.R., Sokolova G.G. (2012) Sravnitel'nyj analiz metodov opredelenija antagonisticheskoj aktivnosti molochnokislyh bakterij [Сравнительный анализ методов определения антагонистической активности молочнокислых бактерий]. Izvestija AltGU, no 3-1. URL: https://cyberleninka.ru/article/n/sravnitelnyy-analiz-metodov-opredeleniya-antagonisticheskoy-aktivnosti-molochnokislyh-bakteriy
35 Glanc S. (1998) Mediko-biologicheskaja statistika [Медико-биологическая статистика] . M., Praktika, pp. 459.
36. Lysak, V. V. (2015) Mikrobiologija. Praktikum: posobie [Микробиология. Практикум: пособие] / V. V. Lysak, R. A. Zheldakova, O. V. Fomina. – Minsk : BGU, P. 34.
2 Gouba N., Drancourt M. Digestive tract mycobiota: A source of infection // Médecine et maladies infectieuses. – 2015. – Vol. 45. – P. 9–16.
3 Coogan M.M., Fidel P.L., Komesu M.C., Maeda L.P. Candida and mycotic infections // Adv. Dent. Res. – 2006. – Vol. 19. – P. 130-138.
4 Clark T. A., Hajjeh R. A. Recent trends in the epidemiology of invasive mycoses // Curr. Opin. Infect. Dis. 2002. – Vol. 15. – P. 569–574.
5 Segal E. Candida, still number one – what do we know and where are we going from there? // Mycoses. – 2005. – Vol. 48, Issue s1. – P. 3-11.
6 Jyoti B., Suresh A.K., Venkatesh K. Diacetyl production and growth of Lactobacillus rhamnosus on multiple substrates // World J Microbiol Biotechnol. – 2003. – Vol. 19. – P. 509–515.
7 Lanciotti R., Patrignani F., Bagnolini F., Guerzoni M.E., Gardini F. Evaluation of diacetyl antimicrobial activity against Escherichia coli, Listeria monocytogenes and Staphylococcus aureus // Food Microbiol. – 2003. – Vol. 20. – P. 537–543.
8 Schnürer, J., Magnusson J. Antifungal lactic acid bacteria as biopreservatives // Trends Food Sci. Technol. – 2005. – Vol. 16. – P. 70–78.
9 Dalié D.K.D., Deschamps A.M., Richard-Forget F. Lactic acid bacteria—Potential for control of mould growth and mycotoxins: A review // Food Control. – 2010. – Vol. 21. – P. 370–380.
10 Crowley S., Mahony, J., van Sinderen D. Current perspectives on antifungal lactic acid bacteria as natural bio-preservatives // Trends Food Sci. Technol. – 2013. – Vol. 33. – P. 93–109.
11 Le Lay C., Coton E., Le Blay G., Chobert J. M., Haertlé Th., Choiset Y., Van Long N. N., Meslet-Cladière L., Mounier J. Identification and quantification of antifungal compounds produced by lactic acid bacteria and propionibacteria // International Journal of Food Microbiology. – 2016. - Vol. 239. – P. 79-85.
12 Pothuraju R., Sharma R.K. Interplay of gut microbiota, probiotics in obesity: a review // Endocrine, metabolic and immune disorders-drug targets. – 2018. – Vol. 18. – P. 212–220.
13 Vijayaram S., Kannan S. Probiotics: the marvelous factor and health benefits // Biomed Biotechnol Res J. - 2018. – Vol. 2. – P. 1–8.
14 Wagner R.D., Johnson S.J. Probiotic lactobacillus and estrogen effects on vaginal epithelial gene expression responses to Candida albicans // J Biomed Sci. – 2012. – Vol. 19. – P. 58.
15 Ranadheera C.S., Evans C. A., Adams M. C., Baines S. K. Effect of dairy probiotic combinations on in vitro gastrointestinal tolerance, intestinal epithelial cell adhesion and cytokine secretion // J Funct Foods. – 2014. – Vol. 8. – P. 18–25.
16 Matsubara V. H., Wang Y., Bandara H. M., Mayer M. P., Samaranayake L. P. Probiotic lactobacilli inhibit early stages of Candida albicans biofilm development by reducing their growth, cell adhesion, and filamentation // Appl Microbiol Biotechnol. – 2016. – Vol. 100(14). – P. 6415-6426.
17 Tan Y., Leonhard M., Moser D., Ma S., Schneider-Stickler B. Inhibitory effect of probiotic lactobacilli supernatants on single and mixed non-albicans Candida species biofilm // Archives of Oral Biology. – 2018. –Vol. 85. – P. 40-45.
18 Aartia Ch., Khusroa A., Vargheseb R., Arasuc M. V., Agastiana P., Al-Dhabic N. A., Ilavenild S., Choid K. Ch. // In vitro investigation on probiotic, anti-Candida, and antibiofilm properties of Lactobacillus pentosus strain LAP1// Archives of Oral Biology. – 2018. - Vol. 89. - P. 99-106.
19 Cross M. L. Microbes versus microbes: immune signals generated by probiotic lactobacilli and their role in protection against microbial pathogens // FEMS Immunology and Medical Microbiology. – 2002. – Vol. 34, Issue 4. – P. 245-253.
20 Kanmani P., Kumar R. S., Yuvaraj N., Paari K.A., Pattukumar V., Arul V. Probiotics and its functionally valuable products-a review // Crit. Rev. Food Sci. Nutr. – 2013. – Vol. 53. – P. 641e658.
21 Delavenne E., Mounier J., Déniel F., Barbier G., Le Blay G. Biodiversity of antifungal lactic acid bacteria isolated from raw milk samples from cow, ewe and goat over one-year period // Int J Food Microbiol. – 2012. – Vol. 155(3). – P.185-190.
22 Song Y. G., Lee S. H. Inhibitory effects of Lactobacillus rhamnosus and Lactobacillus casei on Candida biofilm of denture surface // Arch Oral Biol. – 2017. – Vol. 76. – P. 1-6.
23 Prabhurajeshwar C., Chandrakanth R.K. Probiotic potential of Lactobacilli with antagonistic activity against pathogenic strains: an in vitro validation for the production of inhibitory substances // Biom J. – 2017. – Vol. 40. – P. 270–283.
24 Шигаева М.Х, Оспанова М.Ш. Микрофлора национальных кисломолочных напитков. - Алма-Ата: Наука, 1983. - 150 с.
25 Ермолаева А.Н., Алгожина У.Ж., Тен О.А., Балпанов Д.С. Изучение культур молочнокислых микроорганизмов, выделенных из кумыса различных регионов Северного Казахстана // Биотехнология. Теория и практика. – 2012. – №3. – С. 87-90.
26 Баубекова А.С., Конуспаева Г.С., Ахметсадыкова Ш.Н., Ахметсадыков Н.Н. Подготовка промышленного производства заквасок– выделение и идентификация бактерий для кумыса и шубата // Вестник КазНУ. Серия биологическая. №1/2 (60). - 2014. – С. 178-181.
27 Ringo E., Andersen R., Sperstad S., Zhou Zh., Ren P., Breines E.M., Hareide E., Yttergård G.J., Opsal K., Johansen H.M., Andreassen A.K., Kousha A., Godfroid J., Holzapfel W.Bacterial Community of koumiss from Mongolia investigated by culture and culture-independent methods // Food Biotechnology. - 2014. - Vol. 28. – P. 333–353.
28 Yao G., Yu J., Hou Q., Hui W., Liu W., Kwok L.-Y., Menghe B., Sun T., Zhang H., Zhang W. A Perspective Study of Koumiss Microbiome by Metagenomics Analysis Based on Single-Cell Amplification Technique // Frontiers in microbiology. – 2017. – Vol. 8. – Art. 165.
29 Behera S.K., Panda S.K., Kayitesi E., Mulaba-Bafubiandi A.F. Kefir and Koumiss. Origin, Health Benefits and Current Status of Knowledge // Ramesh C. Ray and Didier Montet (eds.) Fermented Food—Part II: Technological Interventions. – Boca Raton, London, New York: CRC Press, 2017. – P. 400-417.
30 Oleinikova E.A., Aitzhanova A.A., Saubenova M.G., Amangeldy A.A., Kebekbaeva, Elubaeva M.E. Isolation and selection of lactic acid bacteria antagonistically active against opportunistic Candida yeast // Микробиология және вирусология. – 2018. - № 3(22). – С. 103-109.
31 Magnusson J., Schnurer J. Lactobacillus coryniformis subsp. coryniformis strain Si3 produces a broad-spectrum proteinaceous antifungal compound // Applied Environ. Microbiol. - 2001. – Vol. 67. – P. 1-5.
32 Иркитова А.Н., Каган Я.Р., Соколова Г.Г. Сравнительный анализ методов определения антагонистической активности молочнокислых бактерий // Известия Алтайского государственного университета. – 2012. - № 3-1. – С. 41-44.
33 Черкасов С.В., Семенов А.В. Микробная регуляция антагонистической активности лактобактерий // Сибирский медицинский журнал. – 2012. - №2. – С. 78-82.
34 Иркитова А.Н., Каган Я.Р., Соколова Г.Г. Сравнительный анализ методов определения антагонистической активности молочнокислых бактерий // Известия АлтГУ. – 2012. - №3-1. URL: https://cyberleninka.ru/article/n/sravnitelnyy-analiz-metodov-opredeleniya-antagonisticheskoy-aktivnosti-molochnokislyh-bakteriy
35 Гланц С. Медико-биологическая статистика. - М.: Практика, 1998. – С. 459.
36 Лысак, В. В. Микробиология. Практикум: пособие / В. В. Лысак, Р. А. Желдакова, О. В. Фомина. – Минск : БГУ, 2015. – C. 34.
References
1 Shevjakov M.A. (2003) Diagnostika i lechenie kandidoza kishechnika [Diagnosis and treatment of intestinal candidiasis]. Terapevticheskij arhiv, no 11, pp. 77-79.
2 Gouba N., Drancourt M. (2015) Digestive tract mycobiota: A source of infection. Médecine et maladies infectieuses, vol. 45, pp. 9–16.
3 Coogan M.M., Fidel P.L., Komesu M.C., Maeda L.P. (2006) Candida and mycotic infections. Adv. Dent. Res., vol. 19, pp. 130-138.
4 Clark T. A., Hajjeh R. A. (2002) Recent trends in the epidemiology of invasive mycoses. Curr. Opin. Infect. Dis.. vol. 15, pp. 569–574.
5 Segal E. (2005) Candida, still number one – what do we know and where are we going from there? Mycoses. vol. 48, Issue s1, pp. 3-11.
6 Jyoti B., Suresh A.K., Venkatesh K. (2003) Diacetyl production and growth of Lactobacillus rhamnosus on multiple substrates. World J Microbiol Biotechnol., vol. 19, pp. 509–515.
7 Lanciotti R., Patrignani F., Bagnolini F., Guerzoni M.E., Gardini F. (2003) Evaluation of diacetyl antimicrobial activity against Escherichia coli, Listeria monocytogenes and Staphylococcus aureus. Food Microbiol., vol. 20, pp. 537–543.
8 Schnürer, J., Magnusson J. Antifungal lactic acid bacteria as biopreservatives (2005) Trends Food Sci. Technol., vol. 16, pp. 70–78.
9 Dalié D.K.D., Deschamps A.M., Richard-Forget F. (2010) Lactic acid bacteria—Potential for control of mould growth and mycotoxins: A review. Food Control., vol. 21, pp. 370–380.
10 Crowley S., Mahony, J., van Sinderen D. (2013) Current perspectives on antifungal lactic acid bacteria as natural bio-preservatives. Trends Food Sci. Technol., vol. 33, pp. 93–109.
11 Le Lay C., Coton E., Le Blay G., Chobert J. M., Haertlé Th., Choiset Y., Van Long N. N., Meslet-Cladière L., Mounier J. (2016) Identification and quantification of antifungal compounds produced by lactic acid bacteria and propionibacteria. International Journal of Food Microbiology., vol. 239, pp. 79-85.
12 Pothuraju R., Sharma R.K. (2018) Interplay of gut microbiota, probiotics in obesity: a review. Endocrine, metabolic and immune disorders-drug targets, vol. 18, pp. 212–220.
13 Vijayaram S., Kannan S. Probiotics: the marvelous factor and health benefits (2018) Biomed Biotechnol Res J., vol. 2, pp. 1–8.
14 Wagner R.D., Johnson S.J. (2012) Probiotic lactobacillus and estrogen effects on vaginal epithelial gene expression responses to Candida albicans. J Biomed Sci., vol. 19, pp. 58.
15 Ranadheera C.S., Evans C. A., Adams M. C., Baines S. K. (2014) Effect of dairy probiotic combinations on in vitro gastrointestinal tolerance, intestinal epithelial cell adhesion and cytokine secretion. J Funct Foods., vol. 8, pp. 18–25.
16 Matsubara V. H., Wang Y., Bandara H. M., Mayer M. P., Samaranayake L. P. (2016) Probiotic lactobacilli inhibit early stages of Candida albicans biofilm development by reducing their growth, cell adhesion, and filamentation. Appl Microbiol Biotechnol., vol. 100(14), pp. 6415-6426.
17 Tan Y., Leonhard M., Moser D., Ma S., Schneider-Stickler B. (2018) Inhibitory effect of probiotic lactobacilli supernatants on single and mixed non-albicans Candida species biofilm. Archives of Oral Biology., vol. 85., pp. 40-45.
18 Aartia Ch., Khusroa A., Vargheseb R., Arasuc M. V., Agastiana P., Al-Dhabic N. A., Ilavenild S., Choid K. Ch. (2018) In vitro investigation on probiotic, anti-Candida, and antibiofilm properties of Lactobacillus pentosus strain LAP1.. Archives of Oral Biology, vol. 89, - pp. 99-106.
19 Cross M. L. (2002) Microbes versus microbes: immune signals generated by probiotic lactobacilli and their role in protection against microbial pathogens. FEMS Immunology and Medical Microbiology, vol. 34, Issue 4, pp. 245-253.
20 Kanmani P., Kumar R. S., Yuvaraj N., Paari K.A., Pattukumar V., Arul V. (2013) Probiotics and its functionally valuable products-a review. Crit. Rev. Food Sci. Nutr., vol. 53, pp. 641e658.
21 Delavenne E., Mounier J., Déniel F., Barbier G., Le Blay G. (2012) Biodiversity of antifungal lactic acid bacteria isolated from raw milk samples from cow, ewe and goat over one-year period. Int J Food Microbiol., vol. 155(3), pp.185-190.
22 Song Y. G., Lee S. H. (2017) Inhibitory effects of Lactobacillus rhamnosus and Lactobacillus casei on Candida biofilm of denture surface. Arch Oral Biol., vol. 76, pp. 1-6.
23 Prabhurajeshwar C., Chandrakanth R.K. (2017) Probiotic potential of Lactobacilli with antagonistic activity against pathogenic strains: an in vitro validation for the production of inhibitory substances. Biom J, vol. 40, pp. 270–283.
24 Shigaeva M.H, Ospanova M.Sh. (1983) Mikroflora nacional'nyh kislomolochnyh napitkov [Microflora of national fermented milk drinks]. Alma-Ata: Nauka. 150 s.
25 Ermolaeva A.N., Algozhina U.Zh., Ten O.A., Balpanov D.S. (2012) Izuchenie kul'tur molochnokislyh mikroorganizmov, vydelennyh iz kumysa razlichnyh regionov Severnogo Kazahstana [Study of cultures of lactic acid microorganisms isolated from koumiss from various regions of Northern Kazakhstan]. Biotehnologija. Teorija i praktika, no 3, pp. 87-90.
26 Baubekova A.S., Konuspaeva G.S., Ahmetsadykova Sh.N., Ahmetsadykov N.N. (2014) Podgotovka promyshlennogo proizvodstva zakvasok– vydelenie i identifikacija bakterij dlja kumysa i shubata [Preparation of starter industrial production - isolation and identification of bacteria for koumiss and shubat]. Vestnik KazNU. Serija biologicheskaja, no 1/2 (60), pp. 178-181.
27 Ringo E., Andersen R., Sperstad S., Zhou Zh., Ren P., Breines E.M., Hareide E., Yttergård G.J., Opsal K., Johansen H.M., Andreassen A.K., Kousha A., Godfroid J., Holzapfel W.Bacterial (2014) Community of koumiss from Mongolia investigated by culture and culture-independent methods. Food Biotechnology, vol. 28, pp. 333–353.
28 Yao G., Yu J., Hou Q., Hui W., Liu W., Kwok L.-Y., Menghe B., Sun T., Zhang H., Zhang W. (2017) A Perspective Study of Koumiss Microbiome by Metagenomics Analysis Based on Single-Cell Amplification Technique. Frontiers in microbiology, vol. 8, Art. 165.
29 Behera S.K., Panda S.K., Kayitesi E., Mulaba-Bafubiandi A.F. (2017) Kefir and Koumiss. Origin, Health Benefits and Current Status of Knowledge. In: Ramesh C. Ray and Didier Montet (eds.) Fermented Food—Part II: Technological Interventions. Boca Raton, London, New York: CRC Press, pp. 400-417.
30 Oleinikova E.A., Aitzhanova A.A., Saubenova M.G., Amangeldy A.A., Kebekbaeva, Elubaeva M.E. (2018) Isolation and selection of lactic acid bacteria antagonistically active against opportunistic Candida yeast. Mikrobiologija zhәne virusologija, no. 3(22), pp. 103-109.
31 Magnusson J., Schnurer J. (2001) Lactobacillus coryniformis subsp. coryniformis strain Si3 produces a broad-spectrum proteinaceous antifungal compound. Applied Environ. Microbiol., vol. 67, pp. 1-5.
32 Irkitova A.N., Kagan Ja.R., Sokolova G.G. (2012) Sravnitel'nyj analiz metodov opredelenija antagonisticheskoj aktivnosti molochnokislyh bakterij [Comparative analysis of methods for determining the antagonistic activity of lactic acid bacteria]. Izvestija Altajskogo gosudarstvennogo universiteta, no 3-1, pp. 41-44.
33 Cherkasov S.V., Semenov A.V. (2012) Mikrobnaja reguljacija antagonisticheskoj aktivnosti laktobakterij [Microbial regulation of the antagonistic activity of lactobacilli]. Sibirskij medicinskij zhurnal, no 2, pp. 78-82.
34 Irkitova A.N., Kagan Ja.R., Sokolova G.G. (2012) Sravnitel'nyj analiz metodov opredelenija antagonisticheskoj aktivnosti molochnokislyh bakterij [Сравнительный анализ методов определения антагонистической активности молочнокислых бактерий]. Izvestija AltGU, no 3-1. URL: https://cyberleninka.ru/article/n/sravnitelnyy-analiz-metodov-opredeleniya-antagonisticheskoy-aktivnosti-molochnokislyh-bakteriy
35 Glanc S. (1998) Mediko-biologicheskaja statistika [Медико-биологическая статистика] . M., Praktika, pp. 459.
36. Lysak, V. V. (2015) Mikrobiologija. Praktikum: posobie [Микробиология. Практикум: пособие] / V. V. Lysak, R. A. Zheldakova, O. V. Fomina. – Minsk : BGU, P. 34.
Downloads
How to Cite
Aitzhanova, A. A., Saubenova, M. G., Mounier, J., Oleinikova, E. A., & Berzhanova, R. Z. (2019). Isolation of microorganisms from Kazakh dairy products with antagonistic activity against yeast species from the Candida genus. Experimental Biology, 79(2), 54–63. https://doi.org/10.26577/eb-2019-2-1421
Issue
Section
BIOTECHNOLOGY
