Comparison of adhesive gut bacteria composition, immunity, and disease resistance in juvenile hybrid tilapia fed two different Lactobacillus strains

Fish and Shellfish Immunology

Volumn 35, Issue 1, 2013, Pages 54-62

  Liu, Wenshu ^a,b   Ren, Pengfei ^b   He, Suxu ^b   Xu, Li ^b   Yang, Yaling ^b   Gu, Zemao ^a   Zhou, Zhigang ^b  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^b INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

Adhesion; Immunity; Intestinal bacteria; Lactobacilli; Tilapia

Indexed keywords

AEROMONAS HYDROPHILA; BACTERIA (MICROORGANISMS); LACTOBACILLUS; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS BREVIS; TILAPIA;

EID: 84878485703     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2013.04.010     Document Type: Article

References (53)

1. Fuller R. Areview: probiotics in man and animals. JAppl Bacteriol 1989, 66:365-378.
2. Ringø E., Gatesoupe F.J. Lactic acid bacteria in fish: a review. Aquaculture 1998, 160:177-203.
3. Gatesoupe F.J. The use of probiotics in aquaculture. Aquaculture 1999, 180:147-165.
4. Saarela M., Mogensen G., Fondénc R., Mättö J., Mattila-Sandholm T. Probiotic bacteria: safety, functional and technological properties. JBiotechnol 2000, 84:197-215.
5. Taoka Y., Maeda H., Jo J.Y., Kim S.M., Park S.I., Yoshikawa T., et al. Use of live and dead probiotic cells in tilapia Oreochromis niloticus. Fish Sci 2006, 72:755-766.
6. Lødemel J.B., Mayhew T.M., Myklebust R., Olsen R.E., Espelid S., Ringø E. Effect of three dietary oils on disease susceptibility in Arctic charr (Salvelinus alpinus L.) during cohabitant challenge with Aeromonas salmonicida ssp. salmonicida. Aquac Res 2001, 32:935-945.
7. Lewus C.B., Kaiser A., Montville T.J. Inhibition of food-borne bacterial pathogens by bacteriocins from lactic acid bacteria isolated from meat. Appl Environ Microbiol 1991, 57:1683-1688.
8. Santos J.A., Lopez-Diaz T., Garcia-Fernandez M.C., Garcia-Lopez M.L., Otero A. Effect of lactic starter culture on the growth and protease activity of Aeromonas hydrophila. JAppl Bacteriol 1996, 80:13-18.
9. Venkat H.K., Sahu N.P., Jain K.K. Effect of feeding Lactobacillus-based probiotics on the gut microflora, growth and survival of postlarvae of Macrobrachium rosenbergii (de Man). Aquac Res 2004, 35:501-507.
10. Aiba Y.S., Nobuyuki M., Abu M., Kabir T., Atushi, Yasuhiro Koga M.Y. Lactic acid-mediated suppression of Helicobacter pylori by the oral administration of Lactobacillus salivarius as a probiotic in a gnotobiotic murine model. Am J Gastroenterol 1998, 93:2097-2101.
11. Kirjavainen P.V., El-Nezami H.S., Salminen S.J., Ahokas J.T., Wright P.F.A. The effect of orally administrated viable probiotic and dairy lactobacilli on mouse lymphocyte proliferation. FEMS Immunol Med Microbiol 1999, 26:131-135.
12. Ljungh A., Wadström T. Lactic acid bacteria as probiotics. Curr. Issue Intestinal Microbiol 2006, 7:73-90.
13. Nikoskelainen S., Ouwehand A., Salminen S., Bylund G. Protection of rainbow trout (Oncorhynchus mykiss) from furunculosis by Lactobacillus rhamnosus. Aquaculture 2001, 198:229-236.
14. Rinkinen M., Westermarck E., Salminen S., Ouwehand A.C. Absence of host specificity for invitro adhesion of probiotic lactic acid bacteria to intestinal mucus. Vet Microbiol 2003, 97:55-61.
15. Ibrahim F., Ouwehand A.C., Salminen S.J. Effect of temperature on invitro adhesion of potential fish probiotics. Microb Ecol Health Dis 2004, 16:222-227.
16. Balcázar J.L., Vendrell D.V., de Blas I., Ruiz-Zarzuela I., Múzquiz J.L., Gironés O. Characterization of probiotic properties of lactic acid bacteria isolated from intestinal microbiota of fish. Aquaculture 2008, 278:188-191.
17. Merrifield D.L., Harper G.M., Dimitroglou A., Ringø E., Davies S.J. Possible influence of probiotic adhesion to intestinal mucosa on the activity and morphology of rainbow trout (Oncorhynchus mykiss) enterocytes. Aquac Res 2010, 41:1268-1272.
18. Zhou Z.G., Wang W.W., Liu W.S., Xu L., Cao Y.N., Yao B., et al. Diversity and dynamics of autochthonous gut Lactobacillus in zebrafish (Danio rerio) identified by partial rpoB gene sequence analysis. Aquaculture 2012, 370-371:150-157.
19. Wang W.W., Zhou Z.G. Molecular ecology of Lactobacillus spp. in the gastrointestine of fish 2011, 72-90. M. S. Dissertation.
20. Verdegem M.C.J., Hilbrands A.D., Boon J.H. Influence of salinity and dietary composition on blood parameter values of hybrid tilapia, Oreochromis niloticus♀.×O. Mossambicus♂. Aquac Res 1997, 28:453-459.
21. Jacobsen C., Rosenfeldt Nielsen V., Hayford A., Moller P., Michaelsen K., Parregaard A., et al. Screening of probiotic activities of forty-seven strains of Lactobacillus spp. by invitro techniques and evaluation of the colonization ability of five selected strains in humans. Appl Environ Microbiol 1999, 65:4949-4956.
22. Barbosa T.M., Serra C.R., La Ragione R.M., Woodward M.J., Henriques A.O. Screening for Bacillus isolates in the broiler gastrointestinal tract. Appl Environ Microbiol 2005, 71:968-978.
23. Lv H., Zhou Z., Rudeaux F., Respondek F. Effects of dietary short chain fructo-oligosaccharides on intestinal microflora, mortality and growth perormance of Oreochromis aureus♂× Oreochromis niloticus♀. Chin J Anim Nutr 2007, 19:691-697.
24. 3) on aerobic bacterial populations associated with the epithelial mucosa of Arctic charr (Salvelinus alpinus L.). Can J Microbiol 1993, 39:1169-1173.
25. He S., Zhou Z., Liu Y., Shi P., Yao B., Ringø E., et al. Effects dietary yeast culture (DVAQUA) on growth performance, intestinal autochthonous bacterial community and non-specific immunity of hybrid tilapia (Oreochromis niloticus♀×O.aureus ♂) cultured in cages. Aquaculture 2009, 294:99-107.
26. Yu Z., Morrison M. Improved extraction of PCR-quality community DNA from digesta and fecal samples. Biotechniques 2004, 36:808-812.
27. Liu Y., Zhou Z., Yao B., Shi P., He S., Hølvold L., et al. The 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 2008, 39:635-646.
28. Zhou Z.G., He S.X., Liu Y.C., Shi P., Huang G.X., Yao Bin The effects of dietary yeast culture or short-chain fructo-oligosaccharides on the intestinal autochthonous bacterial communities in juvenile hybrid tilapia, Oreochromis niloticus♀×Oreochromis aureus♂. JWorld Aquacult Soc 2009, 40:450-459.
29. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-δδCT method. Methods 2001, 25:402-408.
30. Gildberg A., Johansen A., Bøgwald J. Growth and survival of Atlantic salmon (Salmo salar) fry given diets supplemented with fish protein hydrolysate and lactic acid bacteria during a challenge trial with Aeromonas salmonicida. Aquaculture 1995, 138:23-34.
31. Gildberg A., Mikkelsen H., Sandaker E., Ringø E. Probiotic effect of lactic acid bacteria in the feed on growth and survival of fry of Atlantic cod (Gadus morhua). Hydrobiologia 1997, 352:279-285.
32. Dai Z.L., Zhang J., Wu G., Zhu W.Y. Utilization of amino acids by bacteria from the pig small intestine. Amino Acids 2010, 39:1201-1215.
33. Dai Z.L., Li X.L., Xi P.B., Zhang J., Wu G., Zhu W.Y. Metabolism of select amino acids in bacteria from the pig small intestine. Amino Acids 2011, 42:1597-1608.
34. Muyzer G., De Waal E.C., Uitterlinden A.G. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 1993, 59:695-700.
35. Sáenz de Rodrigáñez M.A., Díaz-Rosales P., Chabrillón M., Smidt H., Arijo S., León-Rubio J.M., et al. Effect of dietary administration of probiotics on growth and intestine functionality of juvenile Senegalese sole (Solea senegalensis, Kaup 1858). Aquacult Nutr 2009, 15:177-185.
36. Yang H.L., Sun Y.Z., Ma R.H., Ye J.D. PCR-DGGE analysis of the autochthonous gut microbiota of grouper Epinephelus coioides following probiotic Bacillus clausii administration. Aquac Res 2012, 43(4):489-497.
37. He S.X., Liu W.S., Zhou Z.Z., Mao W., Ren P.F., Marubashi T., et al. Evaluation of probiotic strain Bacillus subtilis C-3102 as a feed supplement for koi carp (Cyprinus carpio). JAquac Res Dev 2011, S1:005. http://dx.doi.org/10.4172/2155-9546.S1-005.
38. Pirarat N., Kobayashi T., Katagiri T., Maita M., Endo M. Protective effects and mechanisms of a probiotic bacterium Lactobacillus rhamnosus against experimental Edwardsiellatarda infection in tilapia (Oreochromis niloticus). Vet Immunol Immunopathol 2006, 113:339-347.
39. Son V.M., Chang C.C., Wu M.C., Guu Y.K., Chiu C.H., Cheng W. Dietary administration of the probiotic, Lactobacillus plantarum, enhanced the growth, innate immune responses, and disease resistance of the grouper Epinephelus coioides. Fish Shellfish Immun 2009, 26:691-698.
40. Kirjavainen P.V., Ouwehand A.C., Isolauri E., Salminen S.J. The ability of probiotic bacteria to bind to human intestinal mucus. FEMS Microbiol Lett 1998, 167:185-189.
41. Aly S.M., Ahmed Y.A.-G., Ghareeb A.A.-A., Mohamed M.F. 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 Immun 2008, 25:128-136.
42. Mulder I.E., Wadsworth S., Secombes C.J. Cytokine expression in the intestine of rainbow trout (Oncorhynchus mykiss) during infection with Aeromonas salmonicida. Fish Shellfish Immun 2007, 23:747-759.
43. Picchietti S., Fausto A.M., Randelli E., Carnevali O., Taddeic A.R., Buonocore F., et al. 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 Immun 2009, 26:368-376.
44. Kim D.H., Austin B. Cytokine expression in leucocytes and gut cells of rainbow trout, Oncorhynchus mykiss Walbaum, induced by probiotics. Vet Immunol Immunopathol 2006, 114:297-304.
45. Panigrahi A., Kirona V., Satoh S., Hirono I., Kobayashi T., Sugitac H., et al. Immune modulation and expression of cytokine genes in rainbow trout Oncorhynchus mykiss upon probiotic feeding. Dev Comp Immunol 2007, 31:372-382.
46. Pirarat N., Pinpimai K., Endo M., Katagiri T., Ponpornpisit A., Chansue N., et al. Modulation of intestinal morphology and immunity in nile tilapia (Oreochromisniloticus) by Lactobacillus rhamnosus GG. Res Vet Sci 2011, 91:92-97.
47. Sigh J., Linderstrom T., Buchmann K. Expression of pro-inflammatory cytokines in rainbow trout (Oncorhynchus mykiss) during an infection with Ichthyophthirius multifiliis. Fish Shellfish Immun 2004, 17:75-86.
48. Montero D., Mathlouthi F., Tort L., Afonso A.R., Torrecillas S., Fernández-Vaquero A., et al. Replacement of dietary fish oil by vegetable oils affects humoral immunity and expression of pro-inflammatory cytokines genes in gilthead sea bream Sparus aurata. Fish Shellfish Immun 2010, 29:1073-1081.
49. Rollo A., Sulpizio R., Nardi M., Silvi S., Orpianesi C., Caggiano M., et al. Live microbial feed supplement in aquaculture for improvement of stress tolerance. Fish Physiol Biochem 2006, 32:167-177.
50. Avella M.A., Olivotto I., Silvi S., Place A.R., Carnevali O. Effect of dietary probiotics on clownfish: a molecular approach to define how lactic acid bacteria modulate development in a marine fish. Am J Physiol Regul Integr Comp Physiol 2010, 298:359-371.
51. Avella M.A., Place A., Du S.J., Williams E., Silvi S., Zohar Y., et al. Lactobacillus rhamnosus accelerates zebrafish backbone calcification and gonadal differentiation through effects on the GnRH and IGF systems. PLoS One 2012, 7(9):e45572.
52. Avella M.A., Gioacchini G., Decamp O., Makridis P., Bracciatelli C., Carnevali O. Application of multi-species of Bacillus in sea bream larviculture. Aquaculture 2010, 305:12-19.
53. Avella M.A., Olivotto I., Silvi S., Ribecco C., Cresci A., Cresci F., et al. Use of Enterococcus faecium to improve common sole (Solea solea) larviculture. Aquaculture 2011, 315:384-393.