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Probiotic effects of Lactobacillus plantarum and L. delbrueckii ssp. bulguricus on some immune-related parameters in Barbus grypus

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Abstract

Two main probiotics (Lactobacillus plantarum and L. delbrueckii ssp. bulguricus) were isolated from the intestine of Barbus grypus and their characteristics were determined using biochemical, molecular and probiotical tests (bacterial antagonistic effects and lack of pathogenicity to fish). The effect that these lactic acid bacteria (LAB) had on the immune response of juveniles B. grypus and their resistance to Aeromonas hydrophila when fed as a dietary supplement was examined in the present study. The fish were randomly divided into four groups of 120 fish and were fed with diet containing 5 × 107 CFU g−1 of each isolated LAB, Lactobacillus casei PTCC 1608 or a control diet with no bacteria for 60 days, after which half of the fish from each group were challenged with A. hydrophila, while the remaining fish were fed with the control diets for a further 15 days. Various immune parameters were examined at 30 and 60 days post-feeding (dpf), and also 15 days after stopping feeding the probiotic. The results showed that dietary administration of L. plantarum significantly increased serum lysozyme, complement and respiratory burst activities in the serum of B. grypus by 30 dpf. The highest bactericidal activity was observed in the serum of fish fed the diet containing L. delbruecki ssp. bulguricus. Fish fed with diet containing L. delbruecki and L. plantarum had significantly higher survival rates than those fed the control diet after challenge with A. hydrophila. The results suggest that dietary supplementation with L. plantarum and L. delbrueck, isolated from B. grypus, can stimulate selected immune parameters in B. grypus infected with A. hydrophila and increase their survival against this bacterium. These appear to be potential probiotic species for use in aquaculture to improve the health status and disease resistance of juveniles’ B. grypus.

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References

  • Amábile-Cuevas CF, Cárdenas-García M, Ludgar M (1995) Antibiotic resistance. Am Sci:320–329

  • Amann RI, Ludwig W, Schleifer K-H (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59(1):143–169

    PubMed  CAS  PubMed Central  Google Scholar 

  • Andani H, Tukmechi A, Meshkini S, Sheikhzadeh N (2012) Antagonistic activity of two potential probiotic bacteria from fish intestines and investigation of their effects on growth performance and immune response in rainbow trout (Oncorhynchus mykiss). J Appl Ichthyol 28(5):728–734

    Article  Google Scholar 

  • Aoki T, Kanazawa T, Kitao T (1985) Epidemiological surveillance of drug resistant Vibrio anguillarum strains [isolated from diseased ayu Plecoglossus altivelis in various areas of Japan]. Fish Pathol (Japan) 20:199–208

    Article  CAS  Google Scholar 

  • Bairagi A, Ghosh KS, Sen SK, Ray AK (2002) Enzyme producing bacterial flora isolated from fish digestive tracts. Aquac Int 10(2):109–121

    Article  CAS  Google Scholar 

  • Balcázar JL, Rojas-Luna T (2007) Inhibitory activity of probiotic Bacillus subtilis UTM 126 against Vibrio species confers protection against vibriosis in juvenile shrimp (Litopenaeus vannamei). Curr Microbiol 55(5):409–412

    Article  PubMed  Google Scholar 

  • Barta O (1993) Veterinary clinical immunology laboratory. Bar-Lab Inc., PO Box 11819

  • Brunt J, Austin B (2005) Use of probiotic to control laclococcosis and streptococcosis in rainbow trout, Oncorhynchus mykiss (Walbaum). J Fish Dis 28(12):693–701

    Article  PubMed  CAS  Google Scholar 

  • Choi SH, Yoon TJ (2008) Non-specific immune response of rainbow trout (Oncorhynchus Mykiss) by dietary heat-inactivated potential probiotics. Immune Netw 8(3):67–74

    Article  Google Scholar 

  • Cross ML (2002) Immunoregulation by probiotic lactobacilli: pro-Th1 signals and their relevance to human health. Clin Appl Immunol Rev 3(3):115–125

    Article  CAS  Google Scholar 

  • Fletcher TC, White A (1973) Lysozyme activity in the plaice (Pleuronectes platessa L.). Cell Mol Life Sci 29(10):1283–1285

    Article  CAS  Google Scholar 

  • Gatesoupe F (1999) The use of probiotics in aquaculture. Aquaculture 180(1):147–165

    Article  Google Scholar 

  • Geng X et al (2012) Effects of dietary probiotic on the growth performance, non-specific immunity and disease resistance of cobia, Rachycentron canadum. Aquac Nutr 18(1):46–55

    Article  CAS  Google Scholar 

  • Gildberg A, Mikkelsen H (1998) Effects of supplementing the feed to Atlantic cod (Gadus morhua) fry with lactic acid bacteria and immuno-stimulating peptides during a challenge trial with Vibrio anguillarum. Aquaculture 167(1):103–113

    Article  CAS  Google Scholar 

  • Giri SS, Sukumaran V, Oviya M (2013) Potential probiotic Lactobacillus plantarum VSG3 improves the growth, immunity, and disease resistance of tropical freshwater fish, Labeo rohita. Fish Shellfish Immunol 34(2):660–666

    Article  PubMed  CAS  Google Scholar 

  • Gomez-Gil B, Roque A, Turnbull JF (2000) The use and selection of probiotic bacteria for use in the culture of larval aquatic organisms. Aquaculture 191(1):259–270

    Article  Google Scholar 

  • Harikrishnan R, Balasundaram C, Heo M-S (2010) Lactobacillus sakei BK19 enriched diet enhances the immunity status and disease resistance to streptococcosis infection in kelp grouper, Epinephelus bruneus. Fish Shellfish Immunol 29(6):1037–1043

    Article  PubMed  CAS  Google Scholar 

  • Holland MCH, Lambris JD (2002) The complement system in teleosts. Fish Shellfish Immunol 12(5):399–420

    Article  PubMed  CAS  Google Scholar 

  • Holt J, Krieg N, Sneath P (1984) Bergey’s manual of systematic bacteriology, vol 1. The Williams and Wilkins Co, Baltimore

    Google Scholar 

  • Irianto A, Austin B (2002) Use of probiotics to control furunculosis in rainbow trout, Oncorhynchus mykiss (Walbaum). J Fish Dis 25(6):333–342

    Article  CAS  Google Scholar 

  • Kajita Y, Sakai M, Atsuta S, Kobayashi M (1990) The immunomodulatory effects of levamisole on rainbow trout, Oncorhynchus mykiss. Fish Pathol 25(2):93–98

    Article  CAS  Google Scholar 

  • Kamgar M, Ghane M (2012) Evaluation of Bacillus subtilis effect as probiotic on hematological parameters of rainbow trout, Oncorhynchus mykiss (Walbaum) following experimental infection with Streptococcus iniae. J Fish Aquat Sci 7(6):422–430

    Article  Google Scholar 

  • Kennedy S, Tucker J, Thoresen M, Sennett D (1998) Current methodology for the use of probiotic bacteria in the culture of marine fish larvae. Aquaculture 98:286

    Google Scholar 

  • Kesarcodi-Watson A, Kaspar H, Lategan MJ, Gibson L (2008) Probiotics in aquaculture: the need, principles and mechanisms of action and screening processes. Aquaculture 274(1):1–14

    Article  Google Scholar 

  • Khattab YA, Shalaby AM, Abdel-Rhman A (2005) Use of probiotic bacteria as growth promoters, anti-bacterial and their effects on physiological parameters of Oreochromis niloticus. In: Proceedings of international symposium on Nile Tilapia in aquaculture, 7:156–165

  • Kim D-H, Austin B (2006) Innate immune responses in rainbow trout (Oncorhynchus mykiss, Walbaum) induced by probiotics. Fish Shellfish Immunol 21(5):513–524

    Article  PubMed  CAS  Google Scholar 

  • Korkea-aho TL, Heikkinen J, Thompson KD, Von Wright A, Austin B (2011) Pseudomonas sp. M174 inhibits the fish pathogen Flavobacterium psychrophilum. J Appl Microbiol 111(2):266–277

    Article  PubMed  CAS  Google Scholar 

  • Korkea-aho TL, Papadopoulou A, Heikkinen J, Von Wright A, Adams A, Austin B, Thompson KD (2012) Pseudomonas M162 confers protection against rainbow trout fry syndrome by stimulating immunity. J Appl Microbiol 113(1):24–35

    Article  PubMed  CAS  Google Scholar 

  • Lewus CB, Kaiser A, Montville TJ (1991) Inhibition of food-borne bacterial pathogens by bacteriocins from lactic acid bacteria isolated from meat. Appl Environ Microbiol 57(6):1683–1688

    PubMed  CAS  PubMed Central  Google Scholar 

  • Majamaa H, Isolauri E, Saxelin M, Vesikari T (1995) Lactic acid bacteria in the treatment of acute rotavirus gastroenteritis. J Pediatr Gastroenterol Nutr 20(3):333–338

    Article  PubMed  CAS  Google Scholar 

  • Merrifield D, Bradley G, Harper G, Baker R, Munn C, Davies S (2011) Assessment of the effects of vegetative and lyophilized Pediococcus acidilactici on growth, feed utilization, intestinal colonization and health parameters of rainbow trout (Oncorhynchus mykiss Walbaum). Aquac Nutr 17(1):73–79

    Article  CAS  Google Scholar 

  • Nayak S (2010) Probiotics and immunity: a fish perspective. Fish Shellfish Immunol 29(1):2–14

    Article  PubMed  CAS  Google Scholar 

  • Nayak S, Swain P, Mukherjee S (2007) Effect of dietary supplementation of probiotic and vitamin C on the immune response of Indian major carp, Labeo rohita (Ham.). Fish Shellfish Immunol 23(4):892–896

    Article  PubMed  CAS  Google Scholar 

  • Nayak S et al (2008) Effect of endotoxin on the immunity of Indian major carp, Labeo rohita. Fish Shellfish Immunol 24(4):394–399

    Article  PubMed  CAS  Google Scholar 

  • Newaj-Fyzul A, Adesiyun 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(5):1699–1706

    Article  PubMed  CAS  Google Scholar 

  • Nikoskelainen S, Ouwehand A, Salminen S, Bylund G (2001) Protection of rainbow trout (Oncorhynchus mykiss) from furunculosis by Lactobacillus rhamnosus. Aquaculture 198(3):229–236

    Article  Google Scholar 

  • Nikoskelainen S, Ouwehand AC, Bylund G, Salminen S, Lilius E-M (2003) Immune enhancement in rainbow trout (Oncorhynchus mykiss) by potential probiotic bacteria (Lactobacillus rhamnosus). Fish Shellfish Immunol 15(5):443–452

    Article  PubMed  CAS  Google Scholar 

  • Pan X, Wu T, Song Z, Tang H, Zhao Z (2008) Immune responses and enhanced disease resistance in Chinese drum, Miichthys miiuy (Basilewsky), after oral administration of live or dead cells of Clostridium butyrium CB2. J Fish Dis 31(9):679–686

    Article  PubMed  CAS  Google Scholar 

  • 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(1):241–254

    Article  Google Scholar 

  • Pelto L, Isolauri E, Lilius E, Nuutila J, Salminen S (1998) Probiotic bacteria down-regulate the milk-induced inflammatory response in milk-hypersensitive subjects but have an immunostimulatory effect in healthy subjects. Clin Exp Allergy 28(12):1474–1479

    Article  PubMed  CAS  Google Scholar 

  • Perdigon G, Alvarez S, Nader de Macias M, Roux M, de Ruiz Pesce, Holgado A (1990) The oral administration of lactic acid bacteria increases the mucosal intestinal immunity in response to enteropathogens. J Food Prot 53(5):404–410

    Google Scholar 

  • Pirarat N, Kobayashi T, Katagiri T, 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(3):339–347

    Article  PubMed  CAS  Google Scholar 

  • Plumb JA, Hanson LA (2011) Health maintenance and principal microbial diseases of cultured fishes. Wiley, NY

    Google Scholar 

  • Reed LV, Muench H (1938) A simple method of estimating fifty percent end points. Am J Hyg 27:493–497

    Google Scholar 

  • Riquelme C, Araya R, Vergara N, Rojas A, Guaita M, Candia M (1997) Potential probiotic strains in the culture of the Chilean scallop Argopecten purpuratus (Lamarck, 1819). Aquaculture 154(1):17–26

    Article  Google Scholar 

  • Robertson P, O’Dowd C, Burrells C, Williams P, Austin B (2000) Use of Carnobacterium sp. as a probiotic for Atlantic salmon (Salmo salar L.) and rainbow trout (Oncorhynchus mykiss, Walbaum). Aquaculture 185(3):235–243

    Article  Google Scholar 

  • Rodrıguez A, Cuesta A, Ortuño J, Esteban M, Meseguer J (2003) Immunostimulant properties of a cell wall-modified whole Saccharomyces cerevisiae strain administered by diet to seabream (Sparus aurata L.). Vet Immunol Immunopathol 96(3):183–192

    Article  PubMed  Google Scholar 

  • Ruiz C, Roman G, Sanchez J (1996) A marine bacterial strain effective in producing antagonisms of other bacteria. Aquac Int 4(3):289–291

    Article  Google Scholar 

  • Sahoo P et al (2008) Family association between immune parameters and resistance to Aeromonas hydrophila infection in the Indian major carp, Labeo rohita. Fish Shellfish Immunol 25(1):163–169

    Article  PubMed  CAS  Google Scholar 

  • Sakai M, Yoshida T, Atsuta S, Kobayashi M (1995) Enhancement of resistance to vibriosis in rainbow trout, Oncorhynchus mykiss (Walbaum), by oral administration of Clostridium butyricum bacterin. J Fish Dis 18(2):187–190

    Article  Google Scholar 

  • Secombes CJ (1990) Isolation of salmonid macrophages and analysis of their killing activity. Tech Fish Immunol 1:137–154

    Google Scholar 

  • Sharifuzzaman S, Austin B (2009) Influence of probiotic feeding duration on disease resistance and immune parameters in rainbow trout. Fish Shellfish Immunol 27(3):440–445

    Article  PubMed  CAS  Google Scholar 

  • Son VM, Chang C-C, Wu M-C, Guu Y-K, Chiu C-H, Cheng W (2009) Dietary administration of the probiotic, Lactobacillus plantarum, enhanced the growth, innate immune responses, and disease resistance of the grouper Epinephelus coioides. Fish Shellfish Immunol 26(5):691–698

    Article  PubMed  CAS  Google Scholar 

  • Spanggaard B et al (2001) The probiotic potential against vibriosis of the indigenous microflora of rainbow trout. Environ Microbiol 3(12):755–765

    Article  PubMed  CAS  Google Scholar 

  • Sugita H, Miyajima C, Deguchi Y (1991) The vitamin B 12-producing ability of the intestinal microflora of freshwater fish. Aquaculture 92:267–276

    Article  CAS  Google Scholar 

  • Sugita H, Hirose Y, Matsuo N, Deguchi Y (1998) Production of the antibacterial substance by Bacillus sp. strain NM 12, an intestinal bacterium of Japanese coastal fish. Aquaculture 165(3):269–280

    Article  CAS  Google Scholar 

  • Sun Y-Z, Yang H-L, Ma R-L, Lin W-Y (2010) Probiotic applications of two dominant gut Bacillus strains with antagonistic activity improved the growth performance and immune responses of grouper Epinephelus coioides. Fish Shellfish Iimmunol 29(5):803–809

    Article  Google Scholar 

  • Tovar-Ramırez D, Zambonino Infante J, Cahu C, Gatesoupe F, Vázquez-Juárez R (2004) Influence of dietary live yeast on European sea bass (Dicentrarchus labrax) larval development. Aquaculture 234(1):415–427

    Article  Google Scholar 

  • Vendrell D, Luis Balcázar J, de Blas I, Ruiz-Zarzuela I, Gironés O, Luis Múzquiz J (2008) Protection of rainbow trout (Oncorhynchus mykiss) from lactococcosis by probiotic bacteria. Comp Immunol Microbiol Infect Dis 31(4):337–345

    Article  PubMed  Google Scholar 

  • Wang Y-B, Li J-R, Lin J (2008) Probiotics in aquaculture: challenges and outlook. Aquaculture 281(1):1–4

    Google Scholar 

  • Wiegertjes GF, Stet RM, Parmentier HK, van Muiswinkel WB (1996) Immunogenetics of disease resistance in fish: a comparative approach. Dev Comp Immunol 20(6):365–381

    Article  PubMed  CAS  Google Scholar 

  • Yasui H, Nagaoka N, Mike A, Hayakawa K, Ohwaki M (1992) Detection of Bifidobacterium strains that induce large quantities of IgA. Microb Ecol Health Dis 5(3):155–162

    Article  Google Scholar 

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Acknowledgments

This work was funded by a Grant from Shahid Chamran University of Ahvaz Research Council (Grant No: 27176, 1393.3.2).

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Correspondence to Takavar Mohammadian.

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Mohammadian, T., Alishahi, M., Tabandeh, M.R. et al. Probiotic effects of Lactobacillus plantarum and L. delbrueckii ssp. bulguricus on some immune-related parameters in Barbus grypus . Aquacult Int 24, 225–242 (2016). https://doi.org/10.1007/s10499-015-9921-8

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