Probiotic Potential of Bifidobacterium animalis Isolated from Humans and Animals
Abstract
This research aimed to isolate and identify Bifidobacterium spp. from infants, chickens, and swines. Probiotic properties of isolated Bifidobacterium spp. strains were also evaluated. Total number of 16 bacterial isolates inherited morphological and biochemical characteristics of Bifidobacterium spp. were retrieved and they were closely related to B. animalis based on phylogenetic analysis of 16S rRNA. Investigation of probiotics properties revealed that strains that were isolated from infants’ faeces (H1-05, H9-01 and H9-02) and from piglet stool samples (P8-S01) showed the best characteristics of probiotics since they had over 85% survival rate after exposure to acidic (pH 2.0) and 1% oxgall conditions. They showed high adhesion efficiency to intestinal mucus and they were able to survive at the maximum temperature of 60OC. In addition, strain P8-S01 was able to grow in aerobic conditions. Keywords : Bifidobacterium animalis, probiotics, infants, chickens, swinesReferences
Arboleya, S., Ruas-Madiedo, P., Margolles, A., Solís, G., Salminen, S., de Los Reyes-Gavilán, C. G., & Gueimonde, M. (2011). Characterization and in vitro properties of potentially probiotic Bifidobacterium strains isolated from breast-milk. International Journal of Food Microbiology,
149(1), 28-36.
BAAC research and development center. (2016). World and Thailand economic outlook in 2017. Retrieved Jan 16, 2017, from https:// www.pandinthong.com%2Fcritic-dwl- th%2F382991791801&usg= AFQjCNFqkP6-Do3RWS5V0IVljuFzD8oajQ&bvm=bv.152479541,d.c2I (in Thai)
Bevilacqua, A., Cagnazzo, M. T., Caldarola, C., Ciuffreda, E., Dragano, A. R., Franchino, S., Lauriola, R., Pacifico, A., Corbo, M. R., & Sinigaglia, M. (2012). Bifidobacteria as potential functional starter cultures:
a case study by MSc students in food science and technology (University of Foggia, Southern Italy). Food and Nutrition Sciences, 3, 55-63.
Bottacini, F., Ventura, M., van Sinderen, D., & O'Connell Motherway, M. (2014). Diversity, ecology and intestinal function of bifidobacteria. Microbial Cell Factories, 13(1), S4.
Chae, M. H., & Jhon, D. Y. (2006) Preparation of kimchi containing Bifidobacterium animalis DY-64. Journal of Microbiology and Biotechnology, 16, 431-437.
Chung, H. S., Kim, Y. B., Chun, S. L., & Ji, G. E. (1999). Screening and selection of acid and bile resistant bifidobacteria. Journal of Food Microbiology, 47(1-2), 25-32.
Collado, M. C., Meriluoto, J., & Salminen, S. (2007). In vitro analysis of probiotic strain combinations to inhibit pathogen adhesion to human intestinal mucus. Food Research International, 40, 629-636.
Ehrmann, M. A., Kurzak, P., Bauer, J., & Vogel, R. F. (2002). Characterization of lactobacilli towards their use as probiotic adjuncts in poultry. Jounal of Applied Microbiology, 92(5), 966-975.
Erkkila, S. & Petaja, E. (2000). Screening of commercial meat starter cultures at low pH and in the presence of bile salts for potential probiotic use. Meat science, 55(3), 297-300.
Fijan, S. (2014). Microorganisms with claimed probiotic properties: an overview of recent literature. International Journal of Environmental Research and Public Health, 11(5), 4745–4767.
Gaggia, F., Mattarelli, P., & Biavati, B. (2010). Probiotics and prebiotic in animal feeding for safe food production. Journal of Food Microbiology, 141, S15-S28.
Grimm, V., Westermann, C., & Riedel, C.U. (2014). Bifidobacteria-host interactions-an update on colonisation
factors. BioMed Research International, 1-10.
Gueimonde, M., Noriega, L., Margolles, A., Reyes-Gavilan, C. G., & Salmimen, S. (2005). Ability of
Bifidobacterium strains with acquired resistance to bile to adhere to human intestinal mucus. International Jounal of Food Microbiology, 101, 341-346.
He, F., Ouwehand, A. C., Hashimoto, H., Isolauri, E., Benno, Y., & Salminen, S. (2001). Adhesion of Bifidobacterium Spp. to Human Intestinal Mucus. Microbiology and Immunology, 45, 259–262.
Homayouni, A., Ehsani, M. R., Azizi, A., Razavi, S. H., & Yarmand, M. S. (2008) Spectrophotometricaly
Evaluation of probiotic growth in liquid media. Asian Journal of Chemistry, 20(3), 2414-2420.
Kharchenko, N. V., Cherdyntseva, T. A., & Netrusov, A. I. (2015). New approaches for the isolation of
Bifidobacterial strains, their molecular characterization, and assessment of their probiotic potential. Microbiology, 84(3), 419-424.
Kok, R. G., Waal, A. D., Schut, F., Welling, G. W., Weenk, G., & Hellingwerf, K. J. (1996). Specific detection and analysis of a probiotic Bifidobacterium strain in infant feces. Applied and Environmental Microbiology, 62(10), 3668-3672.
Krungsri research. (2016). Frozen & processed chicken industry. Retrieved Jan 16, 2017, from https://www.krungsri.com/bank/getmedia/547be15f-6d5d-44c3-ace7-996f3d03e4dc/ IO_Chicken_2016_EN.aspx
Landers, T. F., Cohen, B., Wittum, T. E., & Larson, E. L. (2012). A review of antibiotic use in food animals: perspective, policy, and potential. Public Health Reports, 127(1), 4–22.
Lee, J. H. & O'Sullivan, D. J. (2010). Genomic insights into Bifidobacteria. Microbiology and Molecular Biology Reviews, 74(3), 378–416.
Lertworapreecha, N. (2007). Selection of potential Enterococcus faecium isolated from native chicken for probiotic use according to the in vitro properties. Master of Science Thesis, Department of Veterinary Pathology, Faculty of Veterinary Science, Chulalongkorn University. (In Thai)
Loquasto, J. R., Barrangou, R., Dudley, E. G., & Roberts R. F. (2011) Short communication: The complete genome sequence of Bifidobacterium animalis subspecies animalis ATCC 25527T and comparative analysis of growth in milk with B. animalis subspecies lactis DSM 10140T. Journal of Dairy Science, 94(12),
5864 – 5870.
Maxwell, F. J., Duncan, S. H., Hold, G., & Stewart, C. S. (2004). Isolation, growth on prebiotics and probiotic potential of novel bifidobacteria from pigs. Anaerobe, 10(1), 33-39.
MOAC (Ministry of Agriculture and Cooperatives). (2016, 26 December). Notification of MOAC entitled Feed additives, quantities and restrictions to inhibit production, import and selling animal feeds. Vol.113, No.306, pp18-26.
MOPH (Ministry of Public Health). (2011, 3 August). Notification of MOPH entitled Applications of probiotics in
food. Vol.128, No.86, pp21-25.
Morelli, L., & Lucio, C. (2012). FAO/WHO guidelines on probiotics: 10 years later. Journal of Clinical Gastroenterology, 46, S1-S2.
Nishiyama, K., Kawanabe, A., Miyauchi, H., Abe, F., Tsubokawa, D., Ishihara, K., Yamanmoto, Y., & Mukai, T.
(2014). Evaluation of bifidobacterial adhesion to acidic sugar chain of porcins of porcine colonic mucins. Bioscience Biotechnology and Biochemistry, 78(8), 1444-1451.
Presti, I., Orazio, G. D., Labra, M., La Ferla, B., Mezzasalma, V., Bizzaro, G., Giardina, S., Michelotti, A., Tursi, F., Vassallo, M. & Di Gennaro, P. (2015). Evaluation of the probiotic properties of new Lactobacillus and Bifidobacterium strains and their in vitro effect. Applied Microbiology and Biotechnology, 99(13), 5613-5626.
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. Journal of Functional Foods, 8, 18-25.
Rinkinen, M., Westermarck, E., Salminen, S., & Ouwehand, A. C. (2003). Absence of host specificity for in vitro adhesion of probiotic lactic acid bacteria to intestinal mucus. Veterinary Microbiology, 97(1), 55-61.
Sambrook, J., & Russell, D. W. (2001). Molecular cloning. (3rd ed.). USA: Cold Spring Harbor Laboratory Press.
Simpson, P. J., Fitzgerald, G. F., Stanton, C., & Ross, R. P. (2004).The evaluation of a mupirocin-based selective medium for the enumeration of bifidobacteria from probiotic animal feed. Journal of Microbiological Methods, 57(1), 9-16.
Simpson, P. J., Stanton, C., Fitzgerald, G. F., & Ross, R. P. (2005). Intrinsic tolerance of Bifidobacterium species
to heat and oxygen and survival following spray drying and storage. Journal of Applied Microbiology, 99 (3), 493-501.
Song, D., Ibrahim, S., & Hayek, S. (2012). Recent application of probiotics in food and agricultural science. In E. C. Rigobelo (Ed.), Probiotics (pp. Ch. 01). Rijeka: InTech.
Tassell, M. L. V., & Miller, M. J. (2011). Lactobacillus adhesion to mucus. Nutrients, 3(5), 613–636.
Ventura, M. Elli, M., & Zink, R. (2001). Molecular microbial analysis of Bifidobacterium isolates from different environments by the species-specific amplified ribosomal DNA restriction analysis (ARDRA). FEMS
Microbiology Ecology, 36(2-3), 113-121.
Waite, D. W. & Taylor, M. W. (2014). Characterizing the avian gut microbiota: membership, driving influences, and potential function. Frontiers in Microbiology, 5(223), 1-12.
Williams, B. A., Verstegen, M.W.A., & Tamminga, S. (2001). Fermentation in the large intestine of single-
stomached animals and its relationship to animal health. Nutrition Research Reviews, 14(2), 207-228.
Zhang, R., He, L., Zhang, L., Li, C., & Zhu, Q. (2016). Screening of cholesterol-lowering Bifidobacterium from Guizhou Xiang pigs, and evaluation of its tolerance to oxygen, acid, and bile. Korean Journal of Food Science of Animal Resources, 36(1), 37-43.
Zuo, F., Yu, R., Feng, X., Chen, L., & Zeng, Z., Khaskheli, G. B., & Chen, S. (2016). Characterization and in vitro properties of potential probiotic Bifidobacterium strains isolated from breast-fed infant feces. Annals of Microbiology, 66(3), 1027-1037.
149(1), 28-36.
BAAC research and development center. (2016). World and Thailand economic outlook in 2017. Retrieved Jan 16, 2017, from https:// www.pandinthong.com%2Fcritic-dwl- th%2F382991791801&usg= AFQjCNFqkP6-Do3RWS5V0IVljuFzD8oajQ&bvm=bv.152479541,d.c2I (in Thai)
Bevilacqua, A., Cagnazzo, M. T., Caldarola, C., Ciuffreda, E., Dragano, A. R., Franchino, S., Lauriola, R., Pacifico, A., Corbo, M. R., & Sinigaglia, M. (2012). Bifidobacteria as potential functional starter cultures:
a case study by MSc students in food science and technology (University of Foggia, Southern Italy). Food and Nutrition Sciences, 3, 55-63.
Bottacini, F., Ventura, M., van Sinderen, D., & O'Connell Motherway, M. (2014). Diversity, ecology and intestinal function of bifidobacteria. Microbial Cell Factories, 13(1), S4.
Chae, M. H., & Jhon, D. Y. (2006) Preparation of kimchi containing Bifidobacterium animalis DY-64. Journal of Microbiology and Biotechnology, 16, 431-437.
Chung, H. S., Kim, Y. B., Chun, S. L., & Ji, G. E. (1999). Screening and selection of acid and bile resistant bifidobacteria. Journal of Food Microbiology, 47(1-2), 25-32.
Collado, M. C., Meriluoto, J., & Salminen, S. (2007). In vitro analysis of probiotic strain combinations to inhibit pathogen adhesion to human intestinal mucus. Food Research International, 40, 629-636.
Ehrmann, M. A., Kurzak, P., Bauer, J., & Vogel, R. F. (2002). Characterization of lactobacilli towards their use as probiotic adjuncts in poultry. Jounal of Applied Microbiology, 92(5), 966-975.
Erkkila, S. & Petaja, E. (2000). Screening of commercial meat starter cultures at low pH and in the presence of bile salts for potential probiotic use. Meat science, 55(3), 297-300.
Fijan, S. (2014). Microorganisms with claimed probiotic properties: an overview of recent literature. International Journal of Environmental Research and Public Health, 11(5), 4745–4767.
Gaggia, F., Mattarelli, P., & Biavati, B. (2010). Probiotics and prebiotic in animal feeding for safe food production. Journal of Food Microbiology, 141, S15-S28.
Grimm, V., Westermann, C., & Riedel, C.U. (2014). Bifidobacteria-host interactions-an update on colonisation
factors. BioMed Research International, 1-10.
Gueimonde, M., Noriega, L., Margolles, A., Reyes-Gavilan, C. G., & Salmimen, S. (2005). Ability of
Bifidobacterium strains with acquired resistance to bile to adhere to human intestinal mucus. International Jounal of Food Microbiology, 101, 341-346.
He, F., Ouwehand, A. C., Hashimoto, H., Isolauri, E., Benno, Y., & Salminen, S. (2001). Adhesion of Bifidobacterium Spp. to Human Intestinal Mucus. Microbiology and Immunology, 45, 259–262.
Homayouni, A., Ehsani, M. R., Azizi, A., Razavi, S. H., & Yarmand, M. S. (2008) Spectrophotometricaly
Evaluation of probiotic growth in liquid media. Asian Journal of Chemistry, 20(3), 2414-2420.
Kharchenko, N. V., Cherdyntseva, T. A., & Netrusov, A. I. (2015). New approaches for the isolation of
Bifidobacterial strains, their molecular characterization, and assessment of their probiotic potential. Microbiology, 84(3), 419-424.
Kok, R. G., Waal, A. D., Schut, F., Welling, G. W., Weenk, G., & Hellingwerf, K. J. (1996). Specific detection and analysis of a probiotic Bifidobacterium strain in infant feces. Applied and Environmental Microbiology, 62(10), 3668-3672.
Krungsri research. (2016). Frozen & processed chicken industry. Retrieved Jan 16, 2017, from https://www.krungsri.com/bank/getmedia/547be15f-6d5d-44c3-ace7-996f3d03e4dc/ IO_Chicken_2016_EN.aspx
Landers, T. F., Cohen, B., Wittum, T. E., & Larson, E. L. (2012). A review of antibiotic use in food animals: perspective, policy, and potential. Public Health Reports, 127(1), 4–22.
Lee, J. H. & O'Sullivan, D. J. (2010). Genomic insights into Bifidobacteria. Microbiology and Molecular Biology Reviews, 74(3), 378–416.
Lertworapreecha, N. (2007). Selection of potential Enterococcus faecium isolated from native chicken for probiotic use according to the in vitro properties. Master of Science Thesis, Department of Veterinary Pathology, Faculty of Veterinary Science, Chulalongkorn University. (In Thai)
Loquasto, J. R., Barrangou, R., Dudley, E. G., & Roberts R. F. (2011) Short communication: The complete genome sequence of Bifidobacterium animalis subspecies animalis ATCC 25527T and comparative analysis of growth in milk with B. animalis subspecies lactis DSM 10140T. Journal of Dairy Science, 94(12),
5864 – 5870.
Maxwell, F. J., Duncan, S. H., Hold, G., & Stewart, C. S. (2004). Isolation, growth on prebiotics and probiotic potential of novel bifidobacteria from pigs. Anaerobe, 10(1), 33-39.
MOAC (Ministry of Agriculture and Cooperatives). (2016, 26 December). Notification of MOAC entitled Feed additives, quantities and restrictions to inhibit production, import and selling animal feeds. Vol.113, No.306, pp18-26.
MOPH (Ministry of Public Health). (2011, 3 August). Notification of MOPH entitled Applications of probiotics in
food. Vol.128, No.86, pp21-25.
Morelli, L., & Lucio, C. (2012). FAO/WHO guidelines on probiotics: 10 years later. Journal of Clinical Gastroenterology, 46, S1-S2.
Nishiyama, K., Kawanabe, A., Miyauchi, H., Abe, F., Tsubokawa, D., Ishihara, K., Yamanmoto, Y., & Mukai, T.
(2014). Evaluation of bifidobacterial adhesion to acidic sugar chain of porcins of porcine colonic mucins. Bioscience Biotechnology and Biochemistry, 78(8), 1444-1451.
Presti, I., Orazio, G. D., Labra, M., La Ferla, B., Mezzasalma, V., Bizzaro, G., Giardina, S., Michelotti, A., Tursi, F., Vassallo, M. & Di Gennaro, P. (2015). Evaluation of the probiotic properties of new Lactobacillus and Bifidobacterium strains and their in vitro effect. Applied Microbiology and Biotechnology, 99(13), 5613-5626.
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. Journal of Functional Foods, 8, 18-25.
Rinkinen, M., Westermarck, E., Salminen, S., & Ouwehand, A. C. (2003). Absence of host specificity for in vitro adhesion of probiotic lactic acid bacteria to intestinal mucus. Veterinary Microbiology, 97(1), 55-61.
Sambrook, J., & Russell, D. W. (2001). Molecular cloning. (3rd ed.). USA: Cold Spring Harbor Laboratory Press.
Simpson, P. J., Fitzgerald, G. F., Stanton, C., & Ross, R. P. (2004).The evaluation of a mupirocin-based selective medium for the enumeration of bifidobacteria from probiotic animal feed. Journal of Microbiological Methods, 57(1), 9-16.
Simpson, P. J., Stanton, C., Fitzgerald, G. F., & Ross, R. P. (2005). Intrinsic tolerance of Bifidobacterium species
to heat and oxygen and survival following spray drying and storage. Journal of Applied Microbiology, 99 (3), 493-501.
Song, D., Ibrahim, S., & Hayek, S. (2012). Recent application of probiotics in food and agricultural science. In E. C. Rigobelo (Ed.), Probiotics (pp. Ch. 01). Rijeka: InTech.
Tassell, M. L. V., & Miller, M. J. (2011). Lactobacillus adhesion to mucus. Nutrients, 3(5), 613–636.
Ventura, M. Elli, M., & Zink, R. (2001). Molecular microbial analysis of Bifidobacterium isolates from different environments by the species-specific amplified ribosomal DNA restriction analysis (ARDRA). FEMS
Microbiology Ecology, 36(2-3), 113-121.
Waite, D. W. & Taylor, M. W. (2014). Characterizing the avian gut microbiota: membership, driving influences, and potential function. Frontiers in Microbiology, 5(223), 1-12.
Williams, B. A., Verstegen, M.W.A., & Tamminga, S. (2001). Fermentation in the large intestine of single-
stomached animals and its relationship to animal health. Nutrition Research Reviews, 14(2), 207-228.
Zhang, R., He, L., Zhang, L., Li, C., & Zhu, Q. (2016). Screening of cholesterol-lowering Bifidobacterium from Guizhou Xiang pigs, and evaluation of its tolerance to oxygen, acid, and bile. Korean Journal of Food Science of Animal Resources, 36(1), 37-43.
Zuo, F., Yu, R., Feng, X., Chen, L., & Zeng, Z., Khaskheli, G. B., & Chen, S. (2016). Characterization and in vitro properties of potential probiotic Bifidobacterium strains isolated from breast-fed infant feces. Annals of Microbiology, 66(3), 1027-1037.
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2017-07-26
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