The effect of oral administration of lactic acid bacteria isolated from kefir on intestinal microbiota, growth performance and survival in juvenile rainbow trout, Oncorhynchus mykiss
Downloads
Lactic acid bacteria (LAB) are used in the aquaculture industry to improve growth indices and nutrition efficiency of farmed fish. Kefir is a natural probiotic that largely consists of these microorganisms. This study aimed to isolate LAB strains from kefir grains and investigate their effects on the intestinal microbiota and growth indices of juvenile rainbow trout. Based on the results, one isolate was identified as Lactobacillus faraginis (LF) and other one as Enterococcus durans (ED), both were gram positive, non-hemolytic, catalase and oxidase negative. Both strains showed resistance to acidic environments and gastric juice and were able to grow against bile salts i.e. the hydrophobicity potential of both strains was evaluated above 50%. The results showed that both strains had appropriate and acceptable probiotic properties. A total of 480 juvenile fish with were randomly divided into eight groups viz. Control (basal diet), LF1 and LF2 receiving diets supplemented with L. faraginis at 107 and 108 cfu/g, respectively, ED1 and ED2 diets supplemented with E. durans at 107 and 108 cfu/g, respectively, Bactocell group receiving a diet supplemented with commercial probiotic Bactocell PA-10 (1010 cfu/g), combined treatments LF1+ED1 (5í—106 cfu/g) and LF2+ED2 (5í—107 cfu/g). The strains were prepared in the form of lyophilized powder and added to the basal diet as supplements. Sampling was performed after 0, 30, 15, and 45 days feeding with the diets. In the in vivo investigation, the highest LAB colony counts were obtained for the ED2, Bactocell, LF2+ED2 and LF2 groups, respectively. The highest BWI, SGR, DWG, PER, and CF, and the lowest FCR were observed in the LF2+ED2, Bactocell, ED2, and LF2 groups, respectively. On the other hand, the LF2+ED2, Bactocell and LF2 treatments also had the highest survival rate. Apparently, the use of the tested LAB strains as probiotic in high doses (LF2, ED2) and in combination (LF2+ED2) could improve growth indices, the intestinal LAB population and survival rate in juvenile rainbow trout.
Downloads
Abraham T.J., Babu C.S., Mondal S., Banerjee T. (2007). Effects of dietary supplementation of commercial human probiotic and antibiotic on the growth rate and content of intestinal microflora in ornamental fishes. Bangladesh Journal of Fisheries Research, 11: 57-63
Al-Dohail M.A., Hashim R., Aliyu-Paiko M. (2009). Effects of the probiotic, Lactobacillus acidophilus, on the growth performance, haematology parameters and immunoglobulin concentration in African Catfish (Clarias gariepinus, Burchell 1822) fingerling. Aquaculture Research, 40: 1642-1652.
Aloklah B.A., AlDeen R.A.B., Alsha'ar I.O.A. (2017). Microbial composition of kefir produced by a novel method in Syria. International Journal of ChemTech Research, 10: 215-222.
Aly S.M., Abd-El-Rahman A.M., John G., Mohamed M.F. (2008). Characterization of some bacteria isolated from Oreochromis niloticus and their potential use as probiotics. Aquaculture, 277: 1-6.
Atalan G., Demirkan I., Yaman H., Cihan M., í–nder F., Sözmen M. (2003). Effect of topical kefir application on open wound healing: An in vivo study. Kafkas íœniversitesi Veteriner Fakí¼ltesi Dergisi, 9: 43-47.
Bengoa A.A., Zavala L., Carasi P., Trejo S.A., Bronsoms S., Serradell M.A., Garrote G.L., Abraham A.G. (2018). Simulated gastrointestinal conditions increase adhesion ability of Lactobacillus paracasei strains isolated from kefir to Caco-2 cells and mucin. Food Research International, 103: 462-467.
Bolla P.A., Carasi P., Bolla Mde L., De Antoni G.L., Serradell Mde L. (2013). Protective effect of a mixture of kefir isolated lactic acid bacteria and yeasts in a hamster model of Clostridium difficile infection. Anaerobe, 21: 28-33.
Balcazar J.L., Blas I., Ruiz-Zarzuela I., Cunningham D., Vendrell D., Muzquiz J.L. (2006). The role of probiotics in aquaculture. Veterinary Microbiology, 114: 173-186.
Balcazar J.L., de Blas, I., Ruiz-Zarzuela I., Vendrell D., Gironés O., Muzquiz J.L. (2007). Enhancement of the immune response and protection induced by probiotic lactic acid bacteria against furunculosis in rainbow trout (Oncorhynchus mykiss). FEMS Immunology and Medical Microbiology, 51: 185-93.
Balcazar J.L., Vendrell D., Blas I., Ruiz-Zarzuela I., Girones O., Muzquiz J.L. (2008). In vitro competitive adhesion and production of antagonistic compounds by lactic acid bacteria against fish pathogens. Veterinary Microbiology, 122: 373-380.
Balouiri M., SadikiI M., Ibnsouda S. (2016). Methods for in vitro evaluating antimicrobial activity: A review. Journal of Pharmaceutical Analysis, 6: 71-79.
Brunt J., Newaj-Fyzul A., Austin B. (2007). The development of probiotics for the control of multiple bacterial diseases of rainbow trout, Oncorhynchus mykiss (Walbaum). Journal of Fish Diseases, 30: 573-57
Carasi P., Jacquot C., Romanin D.E., Elie A.M., De Antoni G.L., Urdaci M.C., Serradell M.A. (2014). Safety and potential beneficial properties of Enterococcus strains isolated from kefir. International Dairy Journal, 39: 193-200.
Collins M.D., Jones D., Farrow J.A.E, Kilpper-Balz R., Schleifer K.H. (1984). Enterococcus avium nom. rev., comb. nov.; E. casselipavus norn. rev., comb. nov.; E. durans norn. rev., comb. nov.; E. gallinarum comb. nov.; and E. malodoratus sp. Nov. International Journal of Systematic and Evolutionary Bacteriology, 34: 220-223.
Dehaghani P.G., Baboli M.J., Moghadam A.T., Ziaei-Nejad S., Pourfarhadi M. (2015). Effect of synbiotic dietary supplementation on survival, growth performance, and digestive enzyme activities of common carp (Cyprinus carpio) fingerlings. Czech Journal of Animal Science, 60: 224-232.
Devriese L.A., Vancanneyt M., Descheemaeker P., Baele, M., Van Landuyt H.W., Gordts B., Haesebrouck F. (2002). Differentiation and identification of Enterococcus durans, E. hirae and E. villorum. Journal of Applied Microbiology, 92: 821-827.
Didari T., Solki S., Mozaffari S., Nikfar S., Abdollahi M.A. (2014). Systematic review of the safety of probiotics. Expert Opinion on Drug Safety, 13: 227-239.
Dworkin M., Falkow S., Rosenberg E., Schleifer K.H., Stackebrandt E. (2006). The Prokaryotes. A handbook on the Biology of Bacteria: Ecophysiology and Biochemistry. 3th ed., New York: Springer-Verlag. 1143 p.
Endo A., Okada S. (2007a). Lactobacillus composti sp. nov., a lactic acid bacterium isolated from a compost of distilled shochu residue. International Journal of Systematic Evolutionary and Microbiology, i57: 870-872.
Endo A., Okada S. (2007b). Lactobacillus farraginis sp. nov. and Lactobacillus parafarraginis sp. nov., heterofermentative lactobacilli isolated from a compost of distilled shochu residue. Journal of Systematic Evolutionary and Microbiology, 57: 708-712.
Esteban M.í., Cordero H., Martínez-Tomé M., Jiménez-Monreal A.M., Bakhrouf A., Mahdhi A. (2014). Effect of dietary supplementation of probiotics and palm fruits extracts on the antioxidant enzyme gene expression in the mucosae of gilthead seabream (Sparus aurata L.). Fish and Shellfish Immunology, 39: 532-540.
Farrow J.A.E., Jones D., Phillips B.A., Collins M.D. (1983). Taxonomic studies on some group D streptococci. Journal of General Microbiology, 129: 1423-1432.
Farzanfar A. (2006). The use of probiotics in shrimp aquaculture. FEMS Immunology and Medical Microbiology, 48: 149-58.
Felis G.E., Dellaglio F. (2007). Taxonomy of lactobacilli and bifidobacterial, Current Issues in Intestinal Microbiology, 8: 44-61.
Foulquie Moreno M.R., Sarantinopoulos P., Tsakalidou E., De Vuyst L. (2006). The role and application of enterococci in food and health. International Journal of Food Microbiology, 106: 1-24.
Franz C.M.A.P., Huch M., Abriouel H., Holzapfel W., Gálvez A. (2011). Enterococci as probiotics and their implications in food safety. International Journal of Food Microbiology, 151: 125-140.
Fioramonti J., Theodorou V., Bueno L. (2003). Probiotics: What are they? What are their effects on gut physiology? Best Practice and Research Clinical Gastroenterology, 17: 711-724.
Gao X., Li B. (2016). Chemical and microbiological characteristics of kefir grains and their fermented dairy products: A review. Cogent Food and Agriculture, 2: 1-10.
Giannenas I., Karamaligas I., Margaroni M., Pappas I., Mayer E., Encarnaí§í£o P., Karagouni E. (2015). Effect of dietary incorporation of a multi-strainprobiotic on growth performance and health status in rainbow trout (Oncorhynchus mykiss). Fish Physiology and Biochemistry, 41: 119-128.
Gobi N., Vaseeharan B., Chen J.C., Rekha R., Vijayakumar S., Anjugam M., Iswarya A. (2018). Dietary supplementation of probiotic Bacillus licheniformis Dahb1 improves growth performance, mucus and serum immune parameters, antioxidant enzyme activity as well as resistance against Aeromonas hydrophila in tilapia Oreochromis mossambicus. Fish and Shellfish Immunology, 74: 501-508.
Goldberg S., Doyle R.J., Rosenberg M. (1990). Mechanism of enhancement of microbial cell hydrophobicity by cationic polymers. Journal of Bacteriology, 172: 5650-5654.
Gomez-Gil B., Roque A., Turnbull J.F. (2000). The use and selection of probiotic bacteria for use in the culture of larval aquatic organisms. Aquaculture, 191: 259-270.
Gopal A., Shah N.P., Roginski H. (1996). Bile tolerance, taurocholate and cholesterol removal by Lactobacillus acidophilus and Bifidobacterium spp. Milchwissenschaft, 51: 619-622
Guo L., Li T., Tang Y., Yang L., Huo G. (2016). Probiotic properties of Enterococcus strains isolated from traditional naturally fermented cream in China. Microbial Biotechnology, 9: 7377-7745
Guzel-Seydim Z.B., Kok-Tas T., Greene A.K., Seydim A.C. (2011). Review: Functional properties of kefir. Critical Reviews in Food Science and Nutrition, 51: 261-268.
Hai N.V. (2015). The use of probiotics in aquaculture. Journal of Applied Microbiology, 119: 917-935.
Hammes W.P., Hertel C. (2002). Research approaches for pre- and probiotics: challenges and outlook. Food Research International, 35: 165-170.
Harrigan F.W., McCance M.E. (1976). Laboratory Methods in food and dairy microbiology. Rev ed. Academic Press, London. 200 p.
Hoseini S.M., Gharavi B., Iri Y. (2019b). Assessment of vital organ histopathology and plasma oxidative conditions of rainbow trout (Oncorhynchus mykiss) reared in earthen saltwater pond. RUDN Journal of Agronomy and Animal Industries, 14(3): 255-265.
Hoseini S.M., Mirghaed A.T., Ghelichpour M., Paghe E., Iri Y., Kor A. (2019a). Effects of dietary tryptophan supplementation and stocking density on growth performance and stress responses in rainbow trout (Oncorhynchus mykiss). Aquaculture, 734908.
Hoseini S.M., Mirghaed A.T., Iri Y., Ghelichpour M. (2018). Effects of dietary cineole administration on growth performance, hematological and biochemical parameters of rainbow trout (Oncorhynchus mykiss). Aquaculture, 495: 766-772.
Hoseini S.M., Yousefi M. (2019). Beneficial effects of thyme (Thymus vulgaris) extract on oxytetracycline induced stress response, immunosuppression, oxidative stress and enzymatic changes in rainbow trout (Oncorhynchus mykiss). Aquaculture nutrition, 25(2): 298-309.
Hoseini S.M., Yousefi M., Rajabiesterabadi H., Paktinat M. (2014). Effect of short-term (0–72 h) fasting on serum biochemical characteristics in rainbow trout (Oncorhynchus mykiss). Journal of Applied Ichthyology, 30(3): 569-573.
Hoseinifar S.H., Hoseini S.M., Bagheri D. (2017). Effects of galactooligosaccharide and Pediococcus acidilactici on antioxidant defence and disease resistance of rainbow trout, Oncorhynchus mykiss. Annals of animal science, 17: 217-227.
Hoseinifar S.H., Hosseini S.M., Paknejad H., Safari R., Jafar A., Yousefi M., Van Doan H., Torfi Mozanzadeh M (2019). Enhanced mucosal immune responses, immune related genes and growth performance in common carp (Cyprinus carpio) juveniles fed dietary Pediococcus acidilactici MA18/5M and raffinose. Developmental & Comparative Immunology, 94: 59-65.
Huys G., Botteldoorn N., Delvigne F., De Vuyst L., Heyndrickx M., Pot B. (2013). Microbial characterization of probiotics–advisory report of the working group "8651 probiotics" of the Belgian superior health council (SHC). Molecular Nutrition and Food Research, 57: 1479-1504.
Irianto A., Austin B. (2002). Probiotics in aquaculture: review. Journal of Fish Diseases, 25: 633-642.
Jamuna M., Jeevaratnam K. (2004). Isolation and characterization of lactobacilli from some traditional fermented foods and evaluation of the bacteriocin. Journal of General and Applied Microbiology, 50: 79-90.
John G., Day J.G., Stacey G.N. (2007). Cryopreservation and Freeze-Drying Protocols. 2th ed. Humana Press Inc.: pp: 21-30.
Kandler O., Weiss N. (1986). Regular, Non-Sporing Gram-Positive Rods. In: H.A. Sneath, N.S. Mair, M.E. Sharpe, J.G. Holt (Eds.). Bergey's Manual of Systematic Bacteriology, Williams and Wilkins, Baltimore. pp: 1208-1234.
Kennedy S.B., Tucker J.W., Neidig C.L., Vermeer G.K., Cooper V.R., et al. (1998) Bacterial management strategies for stock enhancement of warm water marine fish: A case study with common snook (Centropomus undecimalis). Journal of Bulletin of Marine Science, 62: 573-588.
Krieg N.R., Padgett P.J. (2011). Phenotypic and physiological characterization methods in Methods in microbiology. vol. 38,1th ed. In: F. Rainey, A. Oren (Eds.). Academic Press, Elsevier's Science & Technology Rights Department in Oxford, UK. pp: 15–61.
Klayraung S., Viernstein H., Sirithunyalug J., Okonogi S. (2008). Probiotic Properties of Lactobacilli Isolated from Thai Traditional Food. Scientia Pharmaceutica, 76: 485-503.
Kumura H., Tanoue Y., Tsukahara M., Tanaka T., Shimazaki K. (2004). Screening of dairy yeast strains for probiotic applications. Journal of Dairy Science, 87: 4050-4056.
Lazado C.C., Caipang C.M. (2014). Bacterial viability differentially influences the immunomodulatory capabilities of potential host-derived probiotics in the intestinal epithelial cells of Atlantic cod Gadus morhua. Journal of Applied Microbiology, 116:9 90-998.
Leite A.M.O., Miguel M.A.L., Peixoto R.S., Ruas-Madiedo P., Paschoalin V.M.F., Mayo B., Delgado S. (2015). Probiotic potential of selected lactic acid bacteria strains isolated from Brazilian kefir grains. Journal of Dairy Science, 98: 3622-3632.
Li Z., Li G., Liu H., Zhao J., Jing Y., Yang F. (2012). The analysis of the impacting factors of probiotics on immune responses. African Journal of Microbiology Research, 6: 2735-2743.
Liu W., Pang H., Zhang H., Cai Y. (2014). Biodiversity of lactic acid bacteria. In: H. Zhang, Y. Cai Y. (Eds). Lactic Acid Bacteria, Berlin: Springer. pp: 103-203.
Lara-Flores M., Olvera-Novoa M.A., Guzmán-Méndez B.E., López-Madrid W. (2003) Use of the bacteria Streptococcus faecium and Lactobacillus acidophilus, and the yeast Saccharomyces cerevisiae as growth promoters in Nile tilapia (Oreochromis niloticus). Aquaculture, 216: 193-201.
Lara-Flores M., Olvera-Novoa M.A. (2013). The use of lactic acid bacteria isolated from intestinal tract of Nile tilapia (Oreochromis niloticus), as growth promoters in fish fed low protein diets. 491 Latin American Journal of Aquatic Research, 41: 490-497.
MacFaddin J.F. (2000). Catalase-Peroxidase tests. Biochemical tests for identification of medical bacteria. 3rd ed. Philadelphia: Lippincott Williams and Wilkins. pp: 78-97.
Mahious A.S., Gatesoupe F.J., Hervi M., Metailler R., Ollevier F. (2006). Effect of dietary inulin and oligosaccharides as prebiotics for weaning Turbot (Psetta maxima). Aquaculture International, 14: 219-229.
Makarova K., Slesarev A., Wolf Y., Sorokin A., Mirkin B., Koonin E., Pavlov A., Pavlova N., Karamychev V., Polouchine N., et al. (2006). Comparative genomics of the lactic acid bacteria. Proceeding of the National Academy of Sciences, 103: 15611-15616.
Marmur J. (1961). A procedure for the isolation of deoxyribonucleic acid from microorganisms. Journal of Molecular Biology, 3: 208-218.
Mercenier A., Lenoir-Wijnkoop I., Sanders M.E. (2008). Physiological and functional properties of probiotics, International Dairy Federation, 429: 2-6.
Mohanty S.N., Swain S.K., and Tripathi S.D., 1996. Rearing of catle (Catla catla ham.) Spawn on formulated diets. Journal of Aquaculture in the Tropics, 11: 253-258
Mohapatra S., Chakraborty T., Kumar V., De Boeck G., Mohanta K.N. (2012a). Aquaculture and stress management: a review of probiotic intervention. Journal of Animal Physiology and Animal Nutrition, 14: 1-26.
Mohapatra S., Chakraborty T., Prusty A.K., Das P., Paniprasad K., et al. (2012b). Use of different microbial probiotics in the diet of Rohu, Labeo rohita fingerling: Effects on growth, nutrient digestibility and retention, digestive enzyme activities and intestinal microflora. Aquaculture Nutrition, 18: 1-11.
Morandi S., Brasca M., Andrighetto C., Lombardi A., Lodi R. (2006). Technological and molecular characterization of enterococci isolated from north-west Italian dairy products. International Dairy Journal, 16: 867-875.
Mukai T., Toba T., Itoh T., Adachi S. (1988). Structural microheterogeneity of kefiran from kefir grains. Japanese Journal of Zootechnology, 59: 167-176.
Mukai T., Watanabe N., Toba T., Itoh T., Adachi S. (1991). Gelforming characteristic and rheological properties of kefiran. Journal of Food Science, 56: 1017-1026.
Muñoz-Atienza E., Araújo C. Magadán S., Hernández P.E., Herranz C., Santos Y., Cintas L.M. (2014). In vitro and in vivo evaluation of lactic acid bacteria of aquatic origin as probiotics for turbot (Scophthalmus maximus L.) farming. Fish and Shellfish Immunology, 41: 570-580.
Nayak S.K. (2010). Probiotics and immunity: A fish perspective. Fish and Shellfish Immunology, 29: 2-14.
Nikoskelainen S., Ouwehand A.C., Bylund G., Salminen S., Lilius E.M. (2003). Immune enhancement in rainbow trout (Oncorhynchus mykiss) by potential probiotic bacteria (Lactobacillus rhamnosus). Fish and Shellfish Immunology, 15: 443-52.
Nikoskelainen S., Salminen S., Bylund G., Ouwehand A.C. (2001). Characterization of the properties of human- and dairy-derived probiotics for prevention of infectious diseases in fish. Applied Environmental Microbiology, 67: 2430-2435.
Orla-Jensen S. (1919). Thee lactic acid bacteria Fred Host and Son. Copenhagen.
Panigrahi A., Kiron V., Kobayashi T., Puangkaew J., Satoh S., Sugita H. (2004). Immune responses in rainbow trout Oncorhynchus mykiss induced by a potential probiotic bacteria Lactobacillus rhamnosus JCM 1136. Veterinary Immunology and Immunopathology, 102: 379-388.
Panigrahi A., Kiron V., Puangkaew J., Kobayashi T., Satoh S., Sugita H. (2005) The viability of probiotic bacteria as a factor influencing the immune response in rainbow trout (Oncorhynchus mykiss). Aquaculture, 243: 241-254.
Panigrahi A., Azad I.S. (2007). Microbial intervention for better fish health in aquaculture: the Indian scenario. Fish Physiology and Biochemistry, 33: 429-440.
Pieniz S., Andreazza R., Anghinoni T., Camargo F., Brandelli A. (2014). Probiotic potential, antimicrobial and antioxidant activities of Enterococcus durans strain LAB18s. Food Control, 37: 251-256.
Ringo E., Gatesoupe F.J. (1998). Lactic acid bacteria in fish: a review. Aquaculture, 160: 177-203.
Rodrigues K.L., Rita L., Caputo G., Tavares J.C., Evangelista J. (2005). Antimicrobial and healing activity of kefir and kefiran extract. International Journal of Antimicrobial Agents, 25: 404-408.
Rosi J., Rossi J. (1978). Microrganismi del kefir: i fermenti lattici. Scienza e Tecnica Lattiero Casearia, 29: 291-305.
Saarela M., Mogensen G., Fondén R., Mättö J., Mattila-Sandholm T. (2000). Probiotic bacteria: safety, functional and technological properties. Journal of Biotechnology, 84: 197-215.
Safari R., Adel M., Lazado C.C., Caipang M.C.A., Dadar M., (2016). Host-derived probiotics Enterococcus casseliflavus improves resistance against Streptococcus iniae infection in rainbow trout (Oncorhynchus mykiss) via immunomodulation. Fish and Shellfish Immunology, 52: 198-205.
Soccol C.R., Vandenberghe L.P.S., Spier M.R., Medeiros A.B.P., Yamaguishi C.T., Lindner J.D., Pandey A., Soccol V.T. (2010). The potential of probiotics. Food Technology and Biotechnology, 48: 413-434.
Suzer C., í‡oban D., Kamaci H.O., Saka Åž., Firat K., OtgucuoÄŸlu í–., et al. (2008). Lactobacillus spp. bacteria as probiotics in gilthead sea bream (Sparus aurata L.) larvae: Effects on growth performance and digestive enzyme activities. Aquaculture, 280:140-145.
Suslow T.V., Schroth M.N., Isaka M. (1982). Application of a rapid method for gram differentiation of plant pathogenic and saprophytic bacteria without staining. Phytopathology, 72: 917-918.
Swanson K.M.J., Busta F.F., Peterson E.H., Johnson M.G. (1992). Colony count methods, in compendium for microbiological examination of foods, 3rd ed. American Public Health Association, Washington, D.C.
Techo S., Visessanguan W., Vilaichone R.K., Tanasupawat S. (2018). Characterization and antibacterial activity against Helicobacter pylori of lactic acid bacteria isolated from thai fermented rice noodle. Probiotics and Antimicrobial Proteins, 11: 92-102.
Thamacharoensuk T., Taweechotipatr M., Kajikawa A., Okada S., Tanasupawat S. (2017). Induction of cellular immunity interleukin-12, antiproliferative effect, and related probiotic properties of lactic acid bacteria isolated in Thailand. Annals of Microbiology, 67: 511-517.
Uluköy G., Kubilay A., Guzel-Seydim Z., Gumus E., Gí¼ney S., Kok-Tas T., Metin S., Diler O. (2015). Effect of storage temperature on beneficial microbial load in rainbow trout feed supplemented with kefir. The Indian Journal of Fisheries, 62: 137-139.
Uluköy G., Metin S., Kubilay A., Gí¼ney Åž., Yıldırım P., Gí¼zel-Seydim Z., et al. (2016). The Effect of kefir as a dietary supplement on nonspecific immune response and disease resistance in juvenile rainbow trout, Oncorhynchus mykiss (Walbaum 1792). Journal of the World Aquaculture Society, 48: 248-256.
Unal B.íœ., Arslanoglu A. (2013). Phylogenetic identification of bacteria within kefir by both culture-dependent and culture-independent methods. African Journal of Microbiology Research, 36: 4533-4538.
Van Doan H., Hoseinifar S.H., Tapingkae W., Khamtavee P. (2017). The effects of dietary kefir and low molecular weight sodium alginate on serum immune parameters, resistance against Streptococcus agalactiae and growth performance in Nile tilapia (Oreochromis niloticus), Fish and Shellfish Immunology, 62: 139-146.
Vendrell D., Balczar J.L., de Blas I., Ruiz-Zarzuela I., Gironés O., Muzquiz J.L. (2008). Protection of rainbow trout (Oncorhynchus mykiss) from lactococcosis by probiotic bacteria. Comparative Immunology, Microbiology and Infectious Diseases, 31: 337-345.
Walker D.K., Gilliland S.E. (1993). Relationships among bile tolerance, bile salt deconjugation, and assimilation of cholesterol by Lactobacillus acidophilus. Journal of Dairy Science, 76: 956-961.
Wszolek M., Kupiec-Teahan B., Skov Guldager H., Tamime A.Y. (2006). Production of kefir, koumiss and other related products. In: AY Tamime (Ed.). Blackwell U knjizi: Fermented Milks, Publishing, Oxford, UK. pp: 174-216.
Xing Z., Tang W., Geng W., Zheng Y., Wang Y. (2017). In vitro and in vivo evaluation of the probiotic attributes of Lactobacillus kefiranofaciens XL10 isolated from Tibetan kefir grain. Applied Microbiology and Biotechnology, 101: 2467-2477.
Yanyan W., Heping Z., Lei Zh., Wenjun L., Yong Z., Xinchang Z.T. (2010). In vitro assessment of probiotic properties of Bacillus isolated from naturally fermented congee from Inner Mongolia of China. World Journal of Microbiology and Biotechnology, 26: 1369-1377.
Yazici I.S., Hisar O., Yilmaz S., Yigit M. (2015). Effects of different probiotic bacteria on growth, body composition, immune response and hematological parameters of rainbow trout (Oncorhynchus mykiss) under sublethal water temperature. Marine Science and Technology Bulletin, 4: 21-28.
Yousefi M., Paktinat M., Mahmoudi N., Pérez-Jiménez A., Hoseini S.M. (2016). Serum biochemical and non-specific immune responses of rainbow trout (Oncorhynchus mykiss) to dietary nucleotide and chronic stress. Fish Physiology and Biochemistry, 42(5): 1417-1425.
Yu J., Wang W.H., Menghe B.L., Jiri M.T., et al. (2011). Diversity of lactic acid bacteria associated with traditional fermented dairy products in Mongolia. Journal of Dairy Science, 94: 3229-3241
Yuksekdag Z.N., Beyatli Y., Aslim B. (2004). Determination of some characteristic's coccoid forms of lactic acid bacteria isolated from Turkish kefirs with natural probiotic. Lebensmittel-Wissenschaft und-Technologie, 37: 663-667.
Zheng Y., Lu Y., Wang J., Yang L., Pan C., Huang Y. (2013). Probiotic Properties of Lactobacillus Strains Isolated from Tibetan Kefir Grains. Plos One, 8: e69868.
Ziaei-Nejad S., Rezaei M.H., Takami G.A., Lovett D.L., Mirvaghefi A.R., Shakouri M. (2006). The effect of Bacillus spp. bacteria used as probiotics on digestive enzyme activity, survival and growth in the Indian (Fenneropenaeus indicus). Aquaculture, 252: 516-524.