Effects of a novel marine probiotic, Lactobacillus plantarum AH 78, on growth performance and immune response of Nile tilapia (Oreochromis niloticus)

Journal of Applied Microbiology

Volumn 120, Issue 4, 2016, Pages 1061-1073

  Hamdan, A M ^a   El Sayed, A F M ^a   Mahmoud, M M ^a  

^a Alexandria University Faculty Of Science   (Egypt)

Author keywords

Immune response; Lactobacillus plantarum; Marine probiotic; Nile tilapia; Performance

Indexed keywords

BACILLI; DISEASE CONTROL; FISH; GENE EXPRESSION REGULATION; LACTIC ACID;

GROWTH PERFORMANCE; HYDROPHILA; IMMUNE RESPONSE; LACTOBACILLUS PLANTARUM; MARINE PROBIOTIC; NILE TILAPIA; OREOCHROMIS NILOTICUS; PERFORMANCE; PROBIOTIC LACTOBACILLI; PROBIOTICS;

GENE EXPRESSION;

AMPICILLIN; CEFALEXIN; CEFTRIAXONE; DOXYCYCLINE; GAMMA INTERFERON; GENTAMICIN; INTERFERON; INTERLEUKIN 12; INTERLEUKIN 4; NALIDIXIC ACID; NITROFURANTOIN; OFLOXACIN; PROBIOTIC AGENT; VANCOMYCIN; CYTOKINE;

ARTIFICIAL DIET; BACTERIAL DISEASE; BACTERIUM; CICHLID; GENE EXPRESSION; GROWTH RATE; IMMUNE RESPONSE; JUVENILE; PEST OUTBREAK; PROBIOTICS; SURVIVAL;

AEROMONAS HYDROPHILA; ANIMAL TISSUE; ANTIBIOTIC SENSITIVITY; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL COUNT; BACTERIUM COLONY; BACTERIUM IDENTIFICATION; BODY GROWTH; CELLULAR IMMUNITY; CONTROLLED STUDY; DIET; DRY WEIGHT; FOOD INTAKE; GROWTH RATE; HEMOLYSIS; HISTOPATHOLOGY; HUMORAL IMMUNITY; IMMUNE RESPONSE; INHIBITION ZONE; INTESTINE MUCOSA; KLEBSIELLA PNEUMONIAE; LACTOBACILLUS PLANTARUM; LIVER; LIVEWEIGHT GAIN; NONHUMAN; OREOCHROMIS NILOTICUS; PHAGOCYTOSIS; PROTEIN EXPRESSION; PSEUDOMONAS AERUGINOSA; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS INIAE; SURVIVAL; ADOLESCENT; ANALYSIS; ANIMAL; ANIMAL FOOD; AQUACULTURE; CICHLID; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOLOGY; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PROCEDURES; UPREGULATION;

AEROMONAS HYDROPHILA; BACTERIA (MICROORGANISMS); LACTOBACILLUS PLANTARUM; OREOCHROMIS NILOTICUS;

ADOLESCENT; AEROMONAS HYDROPHILA; ANIMAL FEED; ANIMALS; AQUACULTURE; CICHLIDS; CYTOKINES; DIET; HOST-PATHOGEN INTERACTIONS; HUMANS; INTESTINAL MUCOSA; LACTOBACILLUS PLANTARUM; PROBIOTICS; UP-REGULATION;

EID: 84959864869     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.13081     Document Type: Article

References (63)

1. Abd El-Rhman, A.M., Khattab, Y.A.E. and Shalaby, A.M.E. (2009) Micrococcus luteus and Pseudomonas species as probiotics for promoting the growth performance and health of Nile tilapia, Oreochromis niloticus. Fish Shellfish Immunol 27, 175-180.
2. Abdel-Rahman, M.A., Tashiro, Y., Zendo, T., Shibata, K. and Sonomoto, K. (2011) Isolation and characterisation of lactic acid bacterium for effective fermentation of cellobiose into optically pure homo L-(+)-lactic acid. Appl Microbiol Biotechnol 189, 1039-1049.
3. Abdel-Tawwab, M., Abdel-Rahman, A.M. and Ismael, N.E.M. (2008) Evaluation of commercial live bakers' yeast, Saccharomyces cerevisiae as a growth and immunity promoter for Fry Nile tilapia, Oreochromis niloticus (L.) challenged in situ with Aeromonas hydrophila. Aquaculture 280, 185-189.
4. Alishahi, M. and Buchmann, K. (2006) Temperature-dependent protection against Ichthyophthirius multifiliis following immunisation of rainbow trout using live theronts. Dis Aquat Organ 72, 269-273.
5. Allen, H., Trachsel, J., Looft, T. and Casey, T. (2014) Finding alternatives to antibiotics. Ann N Y Acad Sci 1323, 91-100.
6. Aly, S.M., Abd-El-Rahman, A.M., John, G. and Mohamed, F.M. (2008) Characterization of some bacteria isolated from Oreochromis niloticus and their potential use as probiotics. Aquaculture 277, 1-6.
7. American Fisheries Society (2014) Guidelines for the Use of Fishes in Research. Bethesda, MA, USA: American Fisheries Society.
8. Austin, B. and Austin, D.A. (2007) Bacterial Fish Pathogens: Diseases of Farmed and Wild Fish, 4th edn. Chichester, UK: Springer-Praxis.
9. Ayo-Olalusi, C., Adeiga, A., Akintunde, G., Oramadike, C. and Awoderu, T. (2014) Viability of Lactobacillus brevis1, Lactobacillus plantarum and Pediococcus pentosaceus2 isolated from fish gut after incorporation into the fish feed. Int J Biotechnol Res 2, 97-101.
10. Bairagi, A., Ghosh, K.S., Sen, S.K. and Ray, A.K. (2002) Enzyme producing bacterial flora isolated from fish digestive tracts. Aquacult Int 10, 109-121.
11. Balcázar, J.L., de Blas, I., Ruiz-Zarzuela, I., Cunningham, D., Vendrell, D. and Múzquiz, J.L. (2006) The role of probiotics in aquaculture. Vet Microbiol 144, 173-186.
12. Barton, M. (2000) Antibiotic use in animal feed and its impact on human health. Nut Res Rev 13, 279-299.
13. Bernardeau, M., Guguen, M. and Vernoux, J.P. (2006) Beneficial lactobacilli in food and feed: long-term use, biodiversity and proposals for specific and realistic safety assessments. FEMS Microbiol Rev 30, 487-513.
14. Bhatnagar, A. and Raparia, S. (2014) Optimum dietary inclusion level of Bacillus coagulans for growth and digestibility improvement for Catla Catla (Hamilton). Int J Curr Res Rev 6, 1-10.
15. Biradar, S., Bahagvati, S. and Shegunshi, B. (2004) Probiotics and antibiotics: a brief overview. Internet J Nutr Wellness 2, 1-6.
16. Cabello, F. (2006) Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environ Microbiol 8, 1137-1144.
17. Carlet, J., Jarlier, V., Harbarth, S., Voss, A., Goossens, H. and Pittet, D. (2012) Ready for a world without antibiotics? The Pensières antibiotic resistance call to action. Antimicrob Resist Infect Control 1, 11.
18. Chi, C., Jiang, B., Yu, X.-B., Liu, T.-Q., Xia, L. and Wang, G.-X. (2014) Effects of three strains of intestinal autochthonous bacteria and their extracellular products on the immune response and disease resistance of common carp, Cyprinus carpio. Fish Shellfish Immunol 36, 9-18.
19. Cho, S.H., Lee, S.-M., Park, B.H., Ji, S.-C., Lee, J., Bae, J. and Oh, S. (2007) Effect of dietary inclusion of various sources of green tea on growth, body composition and blood chemistry of the juvenile olive flounder Paralichthys olivaceus. Fish Physiol Biochem 33, 49-57.
20. De Vuyst, L., Foulquie, R. and Revets, H. (2003) Screening for enterocins and detection of hemolysin and vancomycin resistance in Enterococci of different origins. Int J Food Microbiol 84, 299-318.
21. Ellis, A.E. (1990) Lysozyme assay. In Techniques in Fish Immunology ed. Stolen, J.S., Fletcher, T.C., Anderson, D.P., Roberson, B.S. and Van Muiswinkel, W.B., pp. 101-103. New Jersey, NJ, USA: SOS Publications.
22. El-Sayed, A.M., El-Ghobashy, A.E. and El-Mezayen, M.M. (2013) Effects of feed color on growth and feed utilization efficiency of Nile tilapia (Oreochromis niloticus L.) fry and fingerlings. Aquac Nutr 19, 870-876.
23. FAO (Food and Agriculture Organization) (2015). Global Aquaculture Production. Rome, Italy. http://www.fao.org/fishery/statistics/global-aquaculture-production/query/en.
24. Ghosh, K., Sen, S.K. and Ray, A.K. (2002) Characterization of bacilli isolated from the gut of rohu, Labeo rohita fingerlings and its significance in digestion. J Appl Aquac 12, 33-42.
25. Gonçalves, A.T., Maita, M., Futami, K., Endo, M. and Katagiri, T. (2011) Effects of a probiotic bacterial Lactobacillus rhamnosus dietary supplement on the crowding stress response of juvenile Nile tilapia Oreochromis niloticus. Fish Sci 77, 633-642.
26. Hemaiswarya, S., Raja, R., Ravikumar, R. and Carvalho, I. (2013) Mechanism of action of probiotics. Braz Arch Biol Technol 56, 113-119.
27. Imhoff, J.F., Labes, A. and Wiese, J. (2011) Bio-mining the microbial treasures of the ocean: new natural products. Biotechnol Adv 29, 468-482.
28. Irianto, A. and Austin, B. (2002) Use of probiotics to control furunculosis in rainbow trout, Oncorhynchus mykiss (Walbaum). J Fish Dis 25, 333-342.
29. Ishikawa, M., Nakajima, K., Itamiya, Y., Furukawa, S., Yamamoto, Y. and Yamasato, K. (2005) Halolactibacillus halophilus gen. nov., sp. nov. and Halolactibacillus miurensis sp. nov., halophilic and alkaliphilic marine lactic acid bacteria constituting a phylogenetic lineage in Bacillus rRNA group 1. Int J Sys Evol Microbiol 55, 2427-2439.
30. Jeeva, S., Packia Lekshmi, N., Raja Brindha, J. and Vasudevan, A. (2013) Studies on antibiotic subsceptibility of Aeromonas hydrophila isolated from gold fish (Carassius auratus). Int J Curr Microbiol Appl Sci 2, 7-13.
31. Kathiresan, K. and Thiruneelakandan, G. (2008) Prospects of lactic acid bacteria of marine origin. Indian J Biotechnol 7, 170-177.
32. Kesarcodi-Watson, A., Kaspar, H., Lategan, M.J. and Gibson, L. (2008) Probiotics in aquaculture: the need, principles and mechanisms of action and screening processes. Aquaculture 274, 1-14.
33. Khalil, R., Mahrous, H., El-Halafawy, K., Kamaly, K., Frank, J. and El Soda, M. (2007) Evaluation of the probiotic potential of lactic acid bacteria isolated from faeces of breast-fed infants in Egypt. Afr J Biotechnol 6, 939-949.
34. Kim, D.H. and Austin, B. (2008) Characterization of probiotic carnobacteria isolated from rainbow trout (Oncorhynchus mykiss) intestine. Lett Appl Microbiol 47, 141-147.
35. Kim, S.K. and Dewapriya, P. (2013) Active ingredients from marine microorganisms for modern nutraceuticals. In Marine Nutraceuticals: Prospects and Perspectives ed. Kim, S.K., pp. 195-196. Basel: CRC Press.
36. T Method. Methods 25, 402-408.
37. Maron, D., Smith, T. and Nachman, K. (2013) Restrictions on antimicrobial use in food animal production: an international regulatory and economic survey. Global Health 9, 48.
38. Merrifield, D.L., Burnard, D., Bradley, G., Davies, S.J. and Baker, R.T.M. (2011) Assessment of the effects of vegetative and lyophilized Pediococcus acidilactici on growth, feed utilization, intestinal colonization and health parameters of rainbow trout (Oncoryhnchus mykiss Walbaum). Aquac Nutr 17, 73-79.
39. Molinski, T.F., Dalisay, D.S., Lieyens, S.L. and Saludes, J. (2009) Drug development from marine natural products. Nat Rev Drug Discov 8, 69-85.
40. Muñoz, P., Sitjà-Bobadilla, A. and Alvarez-Pellitero, P. (2000) Cellular and humoral immune response of European sea bass (Dicentrarchus labrax L.) (Teleostei: Serranidae) immunized with Sphaerospora dicentrarchi (Myxosporea: Bivalvulida). Parasitology 120, 465-512.
41. Murray, A.G. and Peeler, E.J. (2005) A framework for understanding the potential for emerging diseases in aquaculture. Prev Vet Med 67, 223-235.
42. Navinchandran, M., Iyapparaj, P., Moovendhan, S., Ramasubburayan, R., Prakash, S., Immanuel, G. and Palavesam, A. (2014) Influence of Probiotic bacterium Bacillus cereus isolated from the gut of wild shrimp Penaeus monodon in turn as a potent growth promoter and immune enhancer in P. monodon. Fish Shellfish Immunol 36, 38-45.
43. Nayak, S.K. (2010) Probiotics and immunity: a fish perspective. Fish Shellfish Immunol 29, 2-14.
44. Ngamkala, S., Futami, K., Endo, M., Maita, M. and Katagiri, T. (2010) Immunological effects of glucan and Lactobacillus rhamnosus GG, a probiotic bacterium, on Nile tilapia Oreochromis niloticus intestine with oral Aeromonas challenges. Fish Sci 76, 833-840.
45. Nils, H.A. (1983) Handbook of Immunoprecipitation- in Gel Techniques, pp. 7-21. Oxford, London: Blackwell Scientific Publications.
46. Pan, W.-H., Li, P.-L. and Liu, Z. (2006) The correlation between surface hydrophobicity and adherence of Bifidobacterium strains from centenarians′ faeces. Anaerobe 12, 148-152.
47. Parthasarathy, R. and Ravi, D. (2011) Probiotic bacteria as growth promoter and biocontrol agent against Aeromonas hydrophila in Catla catla (Hamilton, 1822). Indian J Fish 58, 87-93.
48. Pérez-Sánchez, T., Balcázar, J.L., Merrifield, D.L., Carnevali, O., Gioacchini, G., de Blas, I. and Ruiz-Zarzuela, I. (2011) Expression of immune-related genes in rainbow trout (Oncorhynchus mykiss) induced by probiotic bacteria during Lactococcus garvieae infection. Fish Shellfish Immunol 31, 196-201.
49. Pirarat, N., Pinpimai, K., Endo, M., Katagiri, T., Ponpornpisit, A., Chansue, N. and Maita, N. (2001) Modulation of intestinal morphology and immunity in Nile tilapia (Oreochromis niloticus) by Lactobacillus rhamnosus GG. Res Vet Sci 91, 92-97.
50. Plaza-Diaz, J., Gomez-Llorente, C., Fontana, L. and Gil, A. (2014) Modulation of immunity and inflammatory gene expression in the gut, in inflammatory diseases of the gut and in the liver by probiotics. World J Gastroenterol 20, 15632-15649.
51. Ranzani-Paiva, T., Ishikawa, M., Eiras, C. and Silveira, R. (2004) Effects of an experimental challenge with Mycobacterium marinum on the blood parameters of Nile tilapia, Oreochromis nitoticus (Linnaeus, 1757). Braz Arch Biol Technol 47, 945-953.
52. ® on red tilapia (Oreochromis niloticus) growth performance and health. Aquaculture 294, 118-122.
53. Sahu, M., Swarnakumar, N., Sivakumar, K., Thangaradjou, T. and Kannan, L. (2008) Probiotics in aquaculture: importance and future perspectives. Indian J Microbiol 48, 299-308.
54. Sarker, N., Islam, S., Hasan, M., Kabir, F., Aftab Uddin, M. and Noor, R. (2013) Use of multiplex PCR assay for detection of diarrheagenic Escherichia coli in street vended food items. Am J Life Sci 1, 267-272.
55. Sihag, R. and Sharma, P. (2012) Probiotics: the new ecofriendly alternative measures of disease control for sustainable aquaculture. J Fish Aquat Sci 7, 72-103.
56. Standen, B.T., Rawling, M.D., Davies, S.J., Castex, M., Foey, A., Gioacchini, G. and Merrifield, D.L. (2013) Probiotic Pediococcus acidilactici modulates both localised intestinal- and peripheral-immunity in tilapia (Oreochromis niloticus). Fish Shellfish Immunol 35, 1097-1104.
57. Subasinghe, R.P. (2005) Epidemiological approach to aquatic animal health management: opportunities and challenges for developing countries to increase aquatic production through aquaculture. Prev Vet Med 67, 117-124.
58. Talpur, A.D., Munir, M.B., Mary, A. and Hashim, R. (2014) Dietary probiotics and prebiotics improved food acceptability, growth performance, haematology and immunological parameters and disease resistance against Aeromonas hydrophila in snakehead (Channa striata) fingerlings. Aquaculture 426-427, 14-20.
59. Taoka, Y., Maeda, H., Jo, J.-Y., Kim, S.-M., Park, S.-I., Yoshikawa, T. and Sakata, T. (2006) Use of live and dead probiotic cells in tilapia Oreochromis niloticus. Fish Sci 72, 755-766.
60. Toffin, L., Zink, K., Kato, C., Pignet, P., Bidault, A., Bienvenu, N., Birrien, J.-L. and Prieur, D. (2005) Marinilactibacillus piezotolerans sp. nov., a novel marine lactic acid bacterium isolated from deep sub-seafloor sediment of the Nankai Trough. Int J Sys Evol Microbiol 55, 345-351.
61. Wang, T. and Secombes, C.J. (2013) The cytokine networks of adaptive immunity in fish. Fish Shellfish Immunol 35, 1703-1718.
62. Welker, T.L. and Lim, C. (2011) Use of probiotics in diets of tilapia. J Aquac Res Dev 1, 1-8.
63. Zhang, Q., Yu, H., Tong, T., Tong, W., Dong, L., Xu, M. and Wang, Z. (2014) Dietary supplementation of Bacillus subtilis and fructooligosaccharide enhance the growth, non-specific immunity of juvenile ovate pompano, Trachinotus ovatus and its disease resistance against Vibrio vulnificus. Fish Shellfish Immunol 38, 7-14.