The effect of Pediococcus acidilactici on the gut microbiota and immune status of on-growing red tilapia (Oreochromis niloticus)

Journal of Applied Microbiology

Volumn 109, Issue 3, 2010, Pages 851-862

  Ferguson, R M W ^a   Merrifield, D L ^a   Harper, G M ^b   Rawling, M D ^a   Mustafa, S ^a   Picchietti, S ^c   Balcazar J L ^d   Davies, S J ^a  

^a UNIVERSITY OF PLYMOUTH   (United Kingdom)

^b UNIVERSITY OF PLYMOUTH   (United Kingdom)

^c UNIVERSITY OF TUSCIA   (Italy)

^d UNIVERSITY OF GIRONA   (Spain)

Author keywords

fish; health; histology; PCR DGGE; probiotic

Indexed keywords

DIETARY SUPPLEMENTS; POLYMERASE CHAIN REACTION;

GROWTH PERFORMANCE; GUT MICROBIOTA; INTESTINAL BACTERIAL COMMUNITIES; INTESTINAL TRACT; LEUCOCYTES; MICROBIAL COMMUNITIES; OREOCHROMIS NILOTICUS; PCR-DGGE; PEDIOCOCCUS ACIDILACTICI; PROBIOTICS;

BACTERIA;

ALBUMIN; GLOBULIN; HEMOGLOBIN; LYSOZYME;

ANTAGONISM; BACTERIUM; CICHLID; FOOD SUPPLEMENTATION; GROWTH RESPONSE; HISTOLOGY; IMMUNE RESPONSE; IMMUNE SYSTEM; MICROBIAL COMMUNITY; POLYMERASE CHAIN REACTION; PROBIOTICS; SERUM; STOMACH CONTENT; SURVIVAL;

ALBUMIN BLOOD LEVEL; ARTICLE; BACTERIAL SURVIVAL; BACTERIUM COLONY; CONTROLLED STUDY; DEVELOPMENTAL, AGE AND GROWTH PARAMETERS; DIET SUPPLEMENTATION; ENZYME ACTIVITY; ERYTHROCYTE COUNT; FEED CONVERSION RATIO; FEEDING; FOOD COMPOSITION; GROWTH; HEMATOCRIT; HEMOGLOBIN BLOOD LEVEL; HISTOLOGY; IMMUNE STATUS; INTESTINE; INTESTINE FLORA; LEUKOCYTE COUNT; MALE; MEAN CORPUSCULAR HEMOGLOBIN; MEAN CORPUSCULAR VOLUME; MICROSCOPY; NONHUMAN; OREOCHROMIS; PEDIOCOCCUS ACIDILACTICI; POLYMERASE CHAIN REACTION; PROTEIN BLOOD LEVEL; PROTEIN EFFICIENCY RATIO; RESPIRATORY BURST; SPECIFIC GROWTH RATE; WEIGHT GAIN;

BACTERIA (MICROORGANISMS); OREOCHROMIS NILOTICUS; PEDIOCOCCUS ACIDILACTICI; TILAPIA;

EID: 77955819988     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2010.04713.x     Document Type: Article

References (59)

1. Aly, S.M., Mohamed, M.F. John, G. (2008a) Effect of probiotics on the survival, growth and challenge infection in Tilapia nilotica (Oreochromis niloticus). Aquac Res 39, 647 656.
2. Aly, S.M., Abdel-Galil Ahmed, Y., Abdel-Aziz Ghareeb, A. Mohamed, M.F. (2008b) Studies on Bacillus subtilis and Lactobacillus acidophilus, as potential probiotics, on the immune response and resistance of Tilapia nilotica (Oreochromis niloticus) to challenge infections. Fish Shellfish Immunol 25, 128 136.
3. Anastasiadou, S., Papagianni, M., Filiousis, F., Ambrosiadis, I. Koidis, P. (2008) Pediocin SA-1, an antimicrobial peptide from Pediococcus acidilactici NRRL B5627: production conditions, purification and characterization. Bioresour Technol 99, 5384 5390.
4. AOAC (1990) Official Methods of Analysis of Association of Official Analytical Chemists.
5. Aubin, J., Gatesoupe, F., Labbe, L. Lebrun, L. (2005) Trial of probiotics to prevent the vertebral column compression syndrome in rainbow trout (Oncorhynchus mykiss Walbaum). Aquac Res 36, 758 767.
6. Balcázar, J.L., Blas, I., Ruiz-Zarzuela, I., Cunningham, D., Vendrell, D. Múzqui, J.L. (2006) The role of probiotics in aquaculture. Vet Microbiol 114, 173 186.
7. Balcázar, J.L., de Blas, I., Ruiz-Zarzuela, I., Vendrell, D., Calvo, A.C., Márquez, I., Gironés, O. Muzquiz, J.L. (2007) Changes in intestinal microbiota and humoral immune response following probiotic administration in brown trout (Salmo trutta). Br J Nutr 97, 522 527.
8. Beaulieu, L., Aomari, H., Groleau, D. Subirade, M. (2006) An improved and simplified method for the large-scale purification of pediocin PA-I produced by Pediococcus acidilactici. Biotechnol Appl Biochem 43, 77 84.
9. Begon, M., Harper, J.L. Townsend, C.R. (2003) The influence of predation and disturbance on community structure. Ecology: Individuals, Populations and Communities. p. 801.
10. Bhunia, A.K., Johnson, M.C., Ray, B. Belden, E.L. (1990) Antigenic property of pediocin AcH produced by Pediococcus acidilactici H. J Appl Bacteriol 69, 211 215.
11. Brunt, J. Austin, B. (2005) Use of a probiotic to control lactococcosis and streptococcosis in rainbow trout, Oncorhynchus mykiss (Walbaum). J Fish Dis 28, 693 701.
12. Carnevali, O., Zamponi, M.C., Sulpizio, R., Rollo, A., Nardi, M., Orpianesi, C., Silvi, S., Caggiano, M. et al. (2004) Administration of probiotic strain to improve sea bream wellness during development. Aquac Int 12, 377 386.
13. Carnevali, O., de Vivo, L., Sulpizio, R., Gioacchini, G., Olivotto, I., Silvi, S. Cresci, A. (2006) Growth improvement by probiotic in European sea bass juveniles (Dicentrarchus labrax, L.), with particular attention to IGF-1, myostatin and cortisol gene expression. Aquaculture 258, 430 438.
14. Castex, M., Chim, L., Pham, D., Lemaire, P., Wabete, N., Nicolas, J.-L., Schmidely, P. Mariojouls, C. (2008) Probiotic P. acidilactici application in shrimp Litopenaeus stylirostris culture subject to vibriosis in New Caledonia. Aquaculture 275, 182 193.
15. Castex, M., Lemaire, P., Wabete, N. Chim, L. (2009) Effect of dietary probiotic Pediococcus acidilactici on antioxidant defences and oxidative stress status of shrimp Litopenaeus stylirostris. Aquaculture 294, 306 313.
16. Cintas, L.M., Rodriguez, J.M., Fernandez, M.F., Sletten, K., Nes, I.F., Hernandez, P.E. Holo, H. (1995) Isolation and characterization of pediocin L50, a new bacteriocin from Pediococcus acidilactici with a broad inhibitory spectrum. Appl Environ Microbiol 61, 2643 2648.
17. Clarke, K.R. Gorley, R.N. (2006) Primer V6: User ManualTutorial.
18. Di Giancamillo, A., Vitari, F., Savoini, G., Contempo, V., Bersani, C., Dell'Orto, V. Domeneghini, C. (2008) Effects of orally administered probiotic Pediococcus acidilactici on the small and large intestine of weaning piglets. A qualitative and quantitative micro-anatomical study. Histol Histopathol 23, 651 664.
19. Dimitroglou, A., Merrifield, D.L., Moate, R., Davies, S.J., Spring, P., Sweetman, J. Bradley, G. (2009) Dietary mannan oligosaccharide supplementation modulates intestinal microbial ecology and improves gut morphology of rainbow trout, Oncorhynchus mykiss (Walbaum). J Anim Sci 87, 3226 3234.
20. Doumas, B., Watson, W. Briggs, H. (1971) Albumin standards and the measurement of serum albumin with bromocersol green. Clin Chim Acta 31, 87 96.
21. El-Haroun, E.R., Goda, A.M.A.-S. Kabir Chowdhury, M.A. (2006) Effect of dietary probiotic Biogens supplementation as a growth promoter on growth performance and feed utilization of Nile tilapia Oreochromis niloticus (L.). Aquac Res 37, 1473 1480.
22. El-Rhman, A.M.A., Khattab, Y.A.E. 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.
23. Gatesoupe, F.J. (2002) Probiotic and formaldehyde treatments of Artemia nauplii as food for larval pollack, Pollachius pollachius. Aquaculture 212, 347 360.
24. Gómez, G.D. Balcázar, J.L. (2008) A review on the interactions between gut microbiota and innate immunity of fish. FEMS Immunol Med Microbiol 52, 145 154.
25. Groff, J. LaPatra, S. (2000) Infectious diseases impacting the commercial culture of salmonids. J Appl Aquac 10, 17 90.
26. Halami, P.M., Chandrashekar, A. Joseph, R. (1999) Characterization of bacteriocinogenic strains of lactic acid bacteria in fowl and fish intestines and mushroom. Food Biotechnol 13, 121 136.
27. Hovda, M.B., Lunestad, B.T., Fontanillas, R. Rosnes, J.T. (2007) Molecular characterisation of the intestinal microbiota of farmed Atlantic salmon (Salmo salar L.). Aquaculture 272, 581 588.
28. Huang, J., Lacroix, C., Daba, H. Simard, R.E. (1996) Pediocin 5 production and plasmid stability during continuous free and immobilized cell cultures of Pediococcus acidilactici UL5. J Appl Bacteriol 80, 635 644.
29. Irianto, A. Austin, B. (2002) Use of probiotics to control furunculosis in rainbow trout, Oncorhynchus mykiss (Walbaum). J Fish Dis 25, 333 342.
30. Kesarcodi-Watson, A., Kaspar, H., Lategan, M.J. Gibson, L. (2008) Probiotics in aquaculture: the need, principles and mechanisms of action and screening processes. Aquaculture 274, 1 14.
31. 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.
32. Liu, Y., Zhou, Z., Yao, B., Shi, P., He, S., Benjamisen Hølvold, L. Ringø, E. (2008) Effect of intraperitoneal injection of immunostimulatory substances on allochthonous gut microbiota of Atlantic salmon (Salmo salar L.) determined using denaturing gradient gel electrophoresis. Aquac Res 39, 635 646.
33. Merrifield, D.L., Bradley, G., Harper, G.M., Baker, R.T.M., Munn, C.B. Davies, S.J. (2010a) Assessment of the effects of vegetative and lyophilised Pediococcus acidilactici on growth, feed utilisation, intestinal colonisation and health parameters of rainbow trout (Oncorhynchus mykiss Walbaum). Aquac Nutr. doi :.
34. Merrifield, D.L., Harper, G., Dimitroglou, A., Ringø, E. Davies, S.J. (2010b) Possible influence of probiotic adhesion to intestinal mucosa on the activity and morphology of rainbow trout (Oncorhynchus mykiss) enterocytes. Aquac Res. doi :.
35. Merrifield, D.L., Bradley, G., Baker, R.T.M., Dimitroglou, A. Davies, S.J. (2010c) Probiotic applications for rainbow trout (Oncorhynchus mykiss Walbaum) I. Effects on growth performance, feed utilisation, intestinal microbiota and related health criteria. Aquac Nutr. doi :.
36. Merrifield, D.L., Davies, S.J., Güroy, D., Güroy, B., Emery, M.J., Llewellyn, C. Skill, S. (2010d) Preliminary assessment of Chlorogloeopsis as a dietary supplement for red tilapia (Oreochromis niloticus). Aquaculture, 299, 128 133.
37. Merrifield, D.L., Dinitroglou, A., Foey, A., Davies, S.J., Baker, R.T.M., Bøgwald, J., Castex, M. Ringø, E. (2010e) The current status and future focus of probiotic and prebiotic applications for salmonids. Aquaculture, 302, 1 18.
38. Newaj-Fyzul, A., Adesiyun, A.A., Mutani, A., Ramsubhag, A., Brunt, J. Austin, B. (2007) Bacillus subtilis AB1 controls Aeromonas infection in rainbow trout (Oncorhynchus mykiss, walbaum). J Appl Microbiol 103, 1699 1706.
39. 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. Vet Immunol Immunopathol 102, 379 388.
40. 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.
41. Panigrahi, A., Kiron, V., Satoh, S., Hirono, I., Kobayashi, T., Sugita, H., Puangaew, J. Aoki, T. (2007) Immune modulation and expression of cytokine genes in rainbow trout Oncorhychus mykiss upon probiotic feeding. Dev Comp Immunol 31, 372 382.
42. Paulsen, S.M., Engstad, R.E. Robertsen, B. (2001) Enhanced lysozyme production in Atlantic salmon (Salmo salar L.) macrophages treated with yeast -glucan and bacterial lipopolysaccharide. Fish Shellfish Immunol 11, 23 37.
43. Picchietti, S., Mazzini, M., Taddei, A.R., Renna, R., Fausto, A.M., Mulero, V., Carnevali, O., Cresci, A. et al. (2007) Effects of administration of probiotic strains on GALT of larval gilthead seabream: immunohistochemical and ultrastructural studies. Fish Shellfish Immunol 22, 57 67.
44. Picchietti, S., Fausto, A.M., Randelli, E., Carnevali, O., Taddei, A.R., Buonocore, F., Scapigliati, G. Abelli, L. (2009) Early treatment with Lactobacillus delbrueckii strain induces an increase in intestinal T-cells and granulocytes and modulates immune-related genes of larval Dicentrarchus labrax (L.). Fish Shellfish Immunol 26, 368 376.
45. Pirarat, N., Kobayashi, T., Atagiri, T.K., Maita, M. Endo, M. (2006) Protective effects and mechanisms of a probiotic bacterium Lactobacillus rhamnosus against experimental Edwardsiella tarda infection in tilapia (Oreochromis niloticus). Vet Immunol Immunopathol 113, 339 347.
46. ® on red tilapia (Oreochromis niloticus) growth performance and health. Aquaculture 294, 118 122.
47. Ringø, E., Salinas, I., Olsen, R.E., Nyhaug, A., Myklebust, R. Mayhew, T.M. (2007a) Histological changes in intestine of Atlantic salmon (Salmo salar L.) following in vitro exposure to pathogenic and probiotic bacterial strains. Cell Tissue Res 328, 109 116.
48. Ringø, E., Myklebust, R., Mayhew, T.M. Olsen, R.E. (2007b) Bacterial translocation and pathogenesis in the digestive tract of larvae and fry. Aquaculture 268, 251 264.
49. Salinas, I., Abelli, L., Bertoni, F., Picchietti, S., Roque, A., Furones, D., Cuesta, A., Meseguer, J. et al. (2008) Monospecies and multispecies probiotic formulations produce different systemic and local immunostimulatory effects in the gilthead seabream (Sparus aurata L.). Fish Shellfish Immunol 25, 114 123.
50. Schved, F., Lalazar, Y., Henis, Y. Juven, B.J. (1993) Purification, partial characterization and plasmid-linkage of pediocin SJ-1, a bacteriocins produced by Pediococcus acidilactici. J Appl Bacteriol 74, 67 77.
51. Shelby, R., Lim, C., Yildirm-Aksoy, M. Delaney, M. (2006) Effects of probiotic diet supplements on disease resistance and immune response of young Nile Tilapia (Oreochromis niloticus). J Appl Aquac 18, 22 34.
52. Shelby, R.A., Lim, C., Yildirim-Aksoy, M. Klesius, P.H. (2007) Effects of probiotic bacteria as dietary supplements on growth and disease resistance in young channel catfish, Ictalurus punctatus (Rafinesque). J Appl Aquac 19, 81 91.
53. Spanggaard, B., Huber, I., Nielsen, J., Nielsen, T., Appel, K.F. Gram, L. (2000) The microflora of rainbow trout intestine: a comparison of traditional and molecular identification. Aquaculture 182, 1 15.
54. Svobodova, Z., Fravda, D. Palakova, J. (1991) Unified methods of haematological examination of fish. Research Institute of Fish Culture and Hydrobiology.
55. Taoka, Y., Maeda, H., Jo, J.-Y., Kim, S.-M., Park, S.-I., Yoshikawa, T. Sakata, T. (2006) Use of live and dead probiotic cells in tilapia Oreochromis niloticus. Fish Sci 72, 755 766.
56. Vázquez, J.A., Gonzalez, M.P. Murado, M.A. (2005) Effects of lactic acid bacteria cultures on pathogenic microbiota from fish. Aquaculture 245, 149 161.
57. Villamil, L., Tafalla, C., Figueras, A. Novoa, B. (2002) Evaluation of immunomodulatory effects of lactic acid bacteria in turbot (Scophthalmus maximus). Clin Diagn Lab Immunol 9, 1318 1323.
58. Wang, Y., Tian, Z., Yao, J. Li, W. (2008) Effect of probiotics, Enteroccis faecium, on tilapia (Oreochromis niloticus) growth performance and immune response. Aquaculture 277, 203 207.
59. Zhou, X., Tian, Z., Wang, Y. Li, W. (2010) Effect of treatment with probiotics as water additives on tilapia (Oreochromis niloticus) growth performance and immune response. Fish Physiol Biochem. doi :.