Selection of antagonistically active strains of lactic acid bacteria from milk of various animal species
DOI:
https://doi.org/10.26577//eb.2020.v83.i2.08Abstract
Dairy products make up the bulk of functional fermented foods with a wide range of health benefits. One of the beneficial effects of fermented products is the ability of bacteria used as starter cultures to suppress pathogens and food spoilage microorganisms. Milk of various animal species is noted in the scientific literature as a valuable source for the isolation of new types of microorganisms. We selected 28 isolates of biotechnologically valuable lactic acid bacteria from raw mare, camel and goat milk. The antagonistic activity of isolates from raw milk of various animal species and fermented mare's milk (koumiss) in relation to a number of bacterial test cultures was studied. A wide spectrum of antibacterial activity of isolates from koumiss against Escherichia coli, Sarcina flava, S. flava T, Salmonella dublin, Mycobacterium citreum, M. rubrum, I Tsenkovsky vaccine was shown. Molecular genetic identification of 12 selected microorganisms was carried out. Antagonistically active lactic acid bacteria of koumiss are defined as L. paracasei, L. fermentum, L. rhamnosus and L. diolivorans. Selected microorganisms will be used to create starter cultures for table and preventive beveragess and products with directed action.
Key words: koumiss, lactic acid bacteria, antagonism, antibacterial activity, molecular genetic identification.
References
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8 Pihlanto A., Korhonen H. (2015) Bioactive peptides from fermented foods and health promotion. In: Advances in Fermented Foods and Beverages. Ed. W. Holzapfel. Cambridge: Woodhead Publishing. Elsevier Ltd., pp. 39-74.
9 Fekete A., Givens D., (2003) Lovegrove J. Casein-derived lactotripeptides reduce systolic and diastolic blood pressure in a meta-analysis of randomised clinical trials. Nutrients, vol. 7, pp. 659-681.
10 Filannino P., Bai Y., Di Cagno R., Gobbetti M., Gänzle M.G. (2015) Metabolism of phenolic compounds by Lactobacillus spp. during fermentation of cherry juice and broccoli puree. Food Microbiol., vol. 46, pp. 272-279.
11 Bai Y., Findlay B., Sanchez Maldonado A.F., Schieber A., Vederas J.C., Gänzle M.G. (2014) Novel pyrano and vinylphenol adducts of deoxyanthocyanidins in sorghum sourdough. J Agric Food Chem, vol. 62, pp.11536-11546.
12 Senger D.R., Li D., Jaminet S.C., Cao S. (2016) Activation of the Nrf2 cell defense pathway by ancient foods: disease prevention by important molecules and microbes lost from the modern western diet. PLOS ONE. DOI: 10.1371/journal.pone.0148042.
13 Laatikainen R., Koskenpato J., Hongisto S.M., Loponen J., Poussa T., Hillilä M., Korpela R. (2016) Randomised clinical trial: low-FODMAP rye bread vs. regular rye bread to relieve the symptoms of irritable bowel syndrome. Aliment PharmacolTher., vol. 44, pp. 460-470.
14 Ziegler J.U., Steiner D., Longin C.F.H., Würschum T., Schweiggert R.M., Carle R. (2016) Wheat and the irritable bowel syndrome FODMAP levels of modern and ancient species and their retention during bread making. Journal of Functional Foods.,vol. 25, pp. 257-266.
15 Iraporda C., Errea A., Romanin D.E., Cayet D., Pereyra E., Pignataro O., Sirard J.C., Garrote G.L., Abraham A.G., Rumbo M. (2015) Lactate and short chain fatty acids produced by microbial fermentation downregulateproinflammatory responses in intestinal epithelial cells and myeloid cells. Immunobiology, vol. 220, pp. 1161-1169.
16 Özer B.H., Kirmaci H.A. (2010) Functional milks and dairy beverages. Dairy Technology, vol. 63, Issue 1.pp. 1-15.
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18 Kechagia M. Basoulis D., Konstantopoulou S., Dimitriadi D., Gyftopoulou K., Skarmoutsou N., Fakiri E.M. (2013) Health benefits of probiotics: a review. ISRN Nutrition, -481651.DOI: 10.5402/2013/481651
19 Stoyanova L.G., Ustyugova E.A., Netrusov A.I. (2012) Antimicrobial metabolites of lactic acid bacteria: diversity and properties (review). Applied biochemistry and Microbiology, vol.48(3), pp. 259-275.
20 Inglin R.C., Stevens M.J.A., Meile L., Lacroix C., Meile L. (2015) High-throughput screening assays for antibacterial and antifungal activities of Lactobacillus species. Journal of Microbiological Method, vol. 114, pp. 26-29.
21 Lee Y.K. (2000) Quantitative approach in the study of adhesion of lactic acid bacteria to intestinal cells ant their competition with enterobacteria. Appl. Envir. Microbiol, vol. 66 (9), pp 3692-3697.
22 O’Sullivan D.J. (2001) Screening of intestinal microflora for effective probiotic bacteria. J. Ag. Food Chem., vol. 49, pp. 1751-1760.
23 Greene J.D. (1994) Factors involved in adherence of lactobacilli to human Caco-2 cells. Appl. Envir. Microbiol, vol. 60, pp. 4487-4494.
24 Tannock G.W. (2001) Molecular assessment of intestinal microflora. Am. J. Clin. Nutr. vol.73. pp. 410-414.
25 Hunter J.O. (2002) A review of the role of the gut microflora in irritable bowel syndrome and the effects of probiotics. Br. J. Nutr, vol. 88, pp. 67-72.
26 Caffrey N., Invik J., Waldner S.L., Ramsay D., Checkley S.L. (2019) Risk assessments evaluating foodborne antimicrobial resistance in human. Microbial Risk Analysis., vol. 11, pp. 31-46.
27 Ghosh C., Sarkar P., Issa R., Haldar J. (2019) Alternatives of conventional antibiotics in the era of antimicrobial resistance. Trends in Microbiology, vol. 27, No. 4. pp. 323-338.
28 Gupta R. (2019) NIAID cooperation in Eurasia region and AMR a topic of research priority. Alternative approaches in combatting anti-microbial resistance: regional workshop. Almaty, p. 7.
29 Garcia S.N., Osburn B.I., Cullor J.S. (2019) A one health perspective on dairy production and dairy food safety. One Health, vol. pii: 100086.
30 Hoffmann V., Moser C., Saak A. (2019) Food safety in low and middle-income countries: The evidence through an economic lens. World Fevelopment, vol. 12, pii:104611.
31 Hu K., Liu J., Li B., Liu L., Gharibzahedi S. M. T., Su Y., Jiang Y., Tan J., Wang Y., Guo Y. (2019) Global research trends in food safety in agriculture and industry from 1991 to 2018: A data-driven analysis. Trends in Food Science & Technology.,vol. 85, pp. 262-276.
32 Nayak R., Waterson P. (2019) Global food safety as a complex adaptive system: Key concepts and future prospects. Trends in Food Science & Technology.,vol. 91, pp. 409-425.
33 Sharman N., Wallace C.A., Jespersen L. (2020) Terminology and the understanding of culture, climate, and behavioural change – Impact of organisational and human factors on food safety management. Trends in Food Science & Technology, vol. 96, pp. 13-20.
34 Soon J.M., Brazier A.K.M., Wallace C.A. (2008-2018) Determining common contributory factors in food safety incidents - A review of global outbreaks and recalls. Trends in Food Science & Technology., vol. 97, pp. 76-87.
35 Behera S. K.,Panda S. K.,Kayites E., Mulaba-Bafubiandi A. F. (2017) Kefir and koumiss origin, health benefits and current status of knowledge, In: Fermented Food—Part II: Technological Interventions Ramesh C. Ray and Didier Montet (eds.) CRC Press, pp. 400-417.
36 Ranadheera C. S., Naumovski N., Ajlouni S. (2018) Non-bovine milk products as emerging probiotic carriers: recent developments and innovations, Current Opinion in Food Science., vol. 22, pp. 109–114.
37 Orazov A. Zh., Nadtochiy L. A., Bozymov K.K., Nasambaev E.G., Dzhumagalieva A.A. (2018) Сamel milk and fermented milk products based on It as sources of potential probiotic strains (review). Bulletin of the Orenburg scientific center of Uro RAS (electronic journal)., vol. 3, pp.6.
38 Aitzhanova A.A., Saubenova M.G., Munye J., Oleynikova E.A., Berzhanova R.J. (2019) Isolation of strains of microorganisms from Kazakh fermented milk products with antagonistic activity against yeast of the genus Candida. VestnikKazNU. Ser. Biological., vol. 2 (79), pp. 54-63.
39 Glanc S. (1998) Medico-biological statistics. Per. from the English.- Moscow: Praktika, pp.459.
40 Shigaeva M.Kh., Ospanova M.Sh. (1983) Microflora of national fermented milk drinks. Science.
Alma-Ata, pp. 151.
41 Wu R., Wang L., Wang J., Menghe B., Wu J., Guo M., Zhang H. (2009) Isolation and preliminary probiotic selection of lactobacilli from koumiss in Inner Mongolia. J Basic Microbiol, vol. 49(3), pp. 318-326.
42 Hao Y., Zhao L., Zhang H., Zhai Z., Huang Y., Liu X., Zhang L. (2010) Identification of the bacterial biodiversity in koumiss by denaturing gradient gel electrophoresis and species-specific polymerase chain reaction. Journal of Dairy Science, vol. 93, no. 5, pp. 1926-1933.
43 Kozhakhmetov S., Tynybayeva I., Baikhanova D., Saduakhasova S., Shakhabayeva G., Kushugulova A., Nurgozhin T., Zhumadilov Z. (2014) Metagenomic analysis of koumiss in Kazakhstan. Cent Asian J Glob Health, vol. 3(Suppl):163. doi: 10.5195/cajgh.2014.163.
44 Dheva T., Mishra V., Kumar N., Sangu K. P. S. (2015) Koumiss: nutritional and therapeutic values. In: Fermented Milk and Dairy Products, Edition: Chapter: 18, Publisher: Boca Raton, FL: CRC Press., Editors: A.K Puniya, pp.483-494.
45 Alexandraki V., Kazou M., Angelopoulou A., Arena M.P., Capozzi V., Russo P., Fiocco D., Spano G., Papadimitriou K., Tsakalidou E. (2016) The microbiota of non-cow milk and products. In: Non-Bovine Milk and Milk Products. Academic Press, pp. 117-159.
46 Choi S. (2016) H.Characterization of airag collected in Ulaanbaatar, Mongolia with emphasis on isolated lactic acid bacteria. Journal of Animal Science and Technology, vol. 58: DOI 10.1186/s40781-016-0090-8.
47 Aryantini N.P., Yamasaki E., Kurazono H., Sujaya I.N., Urashima T., Fukuda K. (2017) In vitro safety assessments and antimicrobial activities of Lactobacillus rhamnosus strains isolated from a fermented mare's milk. AnimSci J., vol. 88(3), pp. 517-525.
2 Marco M. L., Heeney D., Binda S., Cifelli C. J., Cotter P. D., Foligne B., Ga¨ nzle M., Kort R., Pasin G., Pihlanto A., Smid E. J., Hutkins R. (2017) Health benefits of fermented foods: microbiota and beyond Current Opinion in Biotechnology., vol. 44, pp. 94–102.
3 Erkus O., De Jager VCL, Spus M, van Alen-boerrigter IJ, van Rijswijck IMH, Hazelwood L., Janssen P.W.M., van Hijum SAFT, Kleerebezem M., Smid E.J. (2013) Multifactorial diversity sustains microbial community stability. IntSocMicrob Ecol., vol.7, pp. 2126-2136.
4 Eussen S.J., PM, van Dongen M.C., Wijckmans N., den Biggelaar L., Oude Elferink S.J., Singh-Povel C.M., Schram M.T., Sep S.J., van der Kallen C.J., Koster A. (2016) et al. Consumption of dairy foods in relation to impaired glucose metabolism and type 2 diabetes mellitus: the Maastricht Study Br J Nutr, vol. 115(8). pp. 1453-1461.
5 Walsh A.M., Crispie F, Kilcawley K, O’Sullivan O, O’Sullivan MG, Claesson MJ, Cotter PD. (2016) Microbial succession and flavor production in the fermented dairy beverage kefir. mSystems, vol. 1(5). pii: e00052-16.DOI:10.1128/mSystems.00052-16.
6 Hutkins R.W. (2018) Microbiology and technology of fermented Foods.2nd Edition. Wiley-Blackwell. 616 pp.
7 Ebner S., Smug L.N., Kneifel W., Salminen S.J., Sanders M.E. (2014) Probiotics in dietary guidelines and clinical recommendations outside the European Union. World J Gastroenterol., vol. 20, pp. 16095-16100.
8 Pihlanto A., Korhonen H. (2015) Bioactive peptides from fermented foods and health promotion. In: Advances in Fermented Foods and Beverages. Ed. W. Holzapfel. Cambridge: Woodhead Publishing. Elsevier Ltd., pp. 39-74.
9 Fekete A., Givens D., (2003) Lovegrove J. Casein-derived lactotripeptides reduce systolic and diastolic blood pressure in a meta-analysis of randomised clinical trials. Nutrients, vol. 7, pp. 659-681.
10 Filannino P., Bai Y., Di Cagno R., Gobbetti M., Gänzle M.G. (2015) Metabolism of phenolic compounds by Lactobacillus spp. during fermentation of cherry juice and broccoli puree. Food Microbiol., vol. 46, pp. 272-279.
11 Bai Y., Findlay B., Sanchez Maldonado A.F., Schieber A., Vederas J.C., Gänzle M.G. (2014) Novel pyrano and vinylphenol adducts of deoxyanthocyanidins in sorghum sourdough. J Agric Food Chem, vol. 62, pp.11536-11546.
12 Senger D.R., Li D., Jaminet S.C., Cao S. (2016) Activation of the Nrf2 cell defense pathway by ancient foods: disease prevention by important molecules and microbes lost from the modern western diet. PLOS ONE. DOI: 10.1371/journal.pone.0148042.
13 Laatikainen R., Koskenpato J., Hongisto S.M., Loponen J., Poussa T., Hillilä M., Korpela R. (2016) Randomised clinical trial: low-FODMAP rye bread vs. regular rye bread to relieve the symptoms of irritable bowel syndrome. Aliment PharmacolTher., vol. 44, pp. 460-470.
14 Ziegler J.U., Steiner D., Longin C.F.H., Würschum T., Schweiggert R.M., Carle R. (2016) Wheat and the irritable bowel syndrome FODMAP levels of modern and ancient species and their retention during bread making. Journal of Functional Foods.,vol. 25, pp. 257-266.
15 Iraporda C., Errea A., Romanin D.E., Cayet D., Pereyra E., Pignataro O., Sirard J.C., Garrote G.L., Abraham A.G., Rumbo M. (2015) Lactate and short chain fatty acids produced by microbial fermentation downregulateproinflammatory responses in intestinal epithelial cells and myeloid cells. Immunobiology, vol. 220, pp. 1161-1169.
16 Özer B.H., Kirmaci H.A. (2010) Functional milks and dairy beverages. Dairy Technology, vol. 63, Issue 1.pp. 1-15.
17 Hill C., Guarner F., Reid G., Gibson G.R., Merestein D.J., Pot B., Morelli L., Canani R.B., Flint H.J., Salminen S., Calder P.C., Sanders M.E. (2014) Expert consensus document: the international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nature Reviewes Gastroenterology and Hepatology, vol. 11, pp. 506-514.
18 Kechagia M. Basoulis D., Konstantopoulou S., Dimitriadi D., Gyftopoulou K., Skarmoutsou N., Fakiri E.M. (2013) Health benefits of probiotics: a review. ISRN Nutrition, -481651.DOI: 10.5402/2013/481651
19 Stoyanova L.G., Ustyugova E.A., Netrusov A.I. (2012) Antimicrobial metabolites of lactic acid bacteria: diversity and properties (review). Applied biochemistry and Microbiology, vol.48(3), pp. 259-275.
20 Inglin R.C., Stevens M.J.A., Meile L., Lacroix C., Meile L. (2015) High-throughput screening assays for antibacterial and antifungal activities of Lactobacillus species. Journal of Microbiological Method, vol. 114, pp. 26-29.
21 Lee Y.K. (2000) Quantitative approach in the study of adhesion of lactic acid bacteria to intestinal cells ant their competition with enterobacteria. Appl. Envir. Microbiol, vol. 66 (9), pp 3692-3697.
22 O’Sullivan D.J. (2001) Screening of intestinal microflora for effective probiotic bacteria. J. Ag. Food Chem., vol. 49, pp. 1751-1760.
23 Greene J.D. (1994) Factors involved in adherence of lactobacilli to human Caco-2 cells. Appl. Envir. Microbiol, vol. 60, pp. 4487-4494.
24 Tannock G.W. (2001) Molecular assessment of intestinal microflora. Am. J. Clin. Nutr. vol.73. pp. 410-414.
25 Hunter J.O. (2002) A review of the role of the gut microflora in irritable bowel syndrome and the effects of probiotics. Br. J. Nutr, vol. 88, pp. 67-72.
26 Caffrey N., Invik J., Waldner S.L., Ramsay D., Checkley S.L. (2019) Risk assessments evaluating foodborne antimicrobial resistance in human. Microbial Risk Analysis., vol. 11, pp. 31-46.
27 Ghosh C., Sarkar P., Issa R., Haldar J. (2019) Alternatives of conventional antibiotics in the era of antimicrobial resistance. Trends in Microbiology, vol. 27, No. 4. pp. 323-338.
28 Gupta R. (2019) NIAID cooperation in Eurasia region and AMR a topic of research priority. Alternative approaches in combatting anti-microbial resistance: regional workshop. Almaty, p. 7.
29 Garcia S.N., Osburn B.I., Cullor J.S. (2019) A one health perspective on dairy production and dairy food safety. One Health, vol. pii: 100086.
30 Hoffmann V., Moser C., Saak A. (2019) Food safety in low and middle-income countries: The evidence through an economic lens. World Fevelopment, vol. 12, pii:104611.
31 Hu K., Liu J., Li B., Liu L., Gharibzahedi S. M. T., Su Y., Jiang Y., Tan J., Wang Y., Guo Y. (2019) Global research trends in food safety in agriculture and industry from 1991 to 2018: A data-driven analysis. Trends in Food Science & Technology.,vol. 85, pp. 262-276.
32 Nayak R., Waterson P. (2019) Global food safety as a complex adaptive system: Key concepts and future prospects. Trends in Food Science & Technology.,vol. 91, pp. 409-425.
33 Sharman N., Wallace C.A., Jespersen L. (2020) Terminology and the understanding of culture, climate, and behavioural change – Impact of organisational and human factors on food safety management. Trends in Food Science & Technology, vol. 96, pp. 13-20.
34 Soon J.M., Brazier A.K.M., Wallace C.A. (2008-2018) Determining common contributory factors in food safety incidents - A review of global outbreaks and recalls. Trends in Food Science & Technology., vol. 97, pp. 76-87.
35 Behera S. K.,Panda S. K.,Kayites E., Mulaba-Bafubiandi A. F. (2017) Kefir and koumiss origin, health benefits and current status of knowledge, In: Fermented Food—Part II: Technological Interventions Ramesh C. Ray and Didier Montet (eds.) CRC Press, pp. 400-417.
36 Ranadheera C. S., Naumovski N., Ajlouni S. (2018) Non-bovine milk products as emerging probiotic carriers: recent developments and innovations, Current Opinion in Food Science., vol. 22, pp. 109–114.
37 Orazov A. Zh., Nadtochiy L. A., Bozymov K.K., Nasambaev E.G., Dzhumagalieva A.A. (2018) Сamel milk and fermented milk products based on It as sources of potential probiotic strains (review). Bulletin of the Orenburg scientific center of Uro RAS (electronic journal)., vol. 3, pp.6.
38 Aitzhanova A.A., Saubenova M.G., Munye J., Oleynikova E.A., Berzhanova R.J. (2019) Isolation of strains of microorganisms from Kazakh fermented milk products with antagonistic activity against yeast of the genus Candida. VestnikKazNU. Ser. Biological., vol. 2 (79), pp. 54-63.
39 Glanc S. (1998) Medico-biological statistics. Per. from the English.- Moscow: Praktika, pp.459.
40 Shigaeva M.Kh., Ospanova M.Sh. (1983) Microflora of national fermented milk drinks. Science.
Alma-Ata, pp. 151.
41 Wu R., Wang L., Wang J., Menghe B., Wu J., Guo M., Zhang H. (2009) Isolation and preliminary probiotic selection of lactobacilli from koumiss in Inner Mongolia. J Basic Microbiol, vol. 49(3), pp. 318-326.
42 Hao Y., Zhao L., Zhang H., Zhai Z., Huang Y., Liu X., Zhang L. (2010) Identification of the bacterial biodiversity in koumiss by denaturing gradient gel electrophoresis and species-specific polymerase chain reaction. Journal of Dairy Science, vol. 93, no. 5, pp. 1926-1933.
43 Kozhakhmetov S., Tynybayeva I., Baikhanova D., Saduakhasova S., Shakhabayeva G., Kushugulova A., Nurgozhin T., Zhumadilov Z. (2014) Metagenomic analysis of koumiss in Kazakhstan. Cent Asian J Glob Health, vol. 3(Suppl):163. doi: 10.5195/cajgh.2014.163.
44 Dheva T., Mishra V., Kumar N., Sangu K. P. S. (2015) Koumiss: nutritional and therapeutic values. In: Fermented Milk and Dairy Products, Edition: Chapter: 18, Publisher: Boca Raton, FL: CRC Press., Editors: A.K Puniya, pp.483-494.
45 Alexandraki V., Kazou M., Angelopoulou A., Arena M.P., Capozzi V., Russo P., Fiocco D., Spano G., Papadimitriou K., Tsakalidou E. (2016) The microbiota of non-cow milk and products. In: Non-Bovine Milk and Milk Products. Academic Press, pp. 117-159.
46 Choi S. (2016) H.Characterization of airag collected in Ulaanbaatar, Mongolia with emphasis on isolated lactic acid bacteria. Journal of Animal Science and Technology, vol. 58: DOI 10.1186/s40781-016-0090-8.
47 Aryantini N.P., Yamasaki E., Kurazono H., Sujaya I.N., Urashima T., Fukuda K. (2017) In vitro safety assessments and antimicrobial activities of Lactobacillus rhamnosus strains isolated from a fermented mare's milk. AnimSci J., vol. 88(3), pp. 517-525.
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Aitzhanova, A. A., Oleinikova, E. A., Saubenova, M. G., Daugalieva, S. T., & Berzhanova, R. Z. (2020). Selection of antagonistically active strains of lactic acid bacteria from milk of various animal species. Experimental Biology, 83(2), 72–81. https://doi.org/10.26577//eb.2020.v83.i2.08
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