Abstract
In this study, Lactobacillus plantarum subsp. plantarum and L. delbrukei subsp. bulgaricus were used as autochthonous food supplementation for gene expression and hematological investigation. Then, 480 fish (BW, 45 ± 10 g) were randomly divided into four groups (three replications) and were fed with diet containing 5 × 107 CFU g−1 of each isolated LAB and L. casei (PTCC 1608) and a control diet with no bacteria. Feeding trail was conducted for 60 days, following a change to the non-supplemented feed until 15 days (day 75). Samples from blood and head kidney at days 0, 60, and 75 were taken. The in vitro examination showed that L. plantarum had high antimicrobial activity against the Aeromonas hydrophila and Yesinia ruckeri. Results of this study showed that feeding of T. grypus with L. plantarum supplementation diet led to increase Hb and WBC, and induce TNF-α, IL-8, and IL-1β expressions in the head kidney rather than control. Results suggested that L. plantarum can be applied as a dietary supplement to enhance the immunity system of T. grypus.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aboumourad IMK, Abbas TA, Awaad ES, MMN A, El-Shafei K, Sharaf M, Ibrahim A, Sadek I, El-Sayed S (2013) Evaluation of Lactobacillus plantarum as a probiotic in aquaculture: emphasis on growth performance and innate immunity. J Appl Sci Res 9(1):572–582
Agaliya PJ, Jeevaratnam K (2012) Screening of Lactobacillus plantarum isolated from fermented idli batter for probiotic properties. Afr J Biotechnol 11(65):12856–12864. https://doi.org/10.5897/AJB12.1825
Ai Q, Xu H, Mai K, Xu W, Wang J, Zhang W (2011) Effects of dietary supplementation of Bacillus subtilis and fructooligosaccharide on growth performance, survival, non-specific immune response and disease resistance of juvenile large yellow croaker, Larimichthys crocea. Aquaculture 317(1–4):155–161. https://doi.org/10.1016/j.aquaculture.2011.04.036
Al-Dohail MA, 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. Aquac Res 40(14):1642–1652. https://doi.org/10.1111/j.1365-2109.2009.02265.x
Amann RI (1995) In situ identification of micro-organisms by whole cell hybridization with rRNAtargeted nucleic acid probes. In: Akkermans ADL, Van Elsas JD, De Bruijn FJ (eds) Molecular microbial ecology manual, 1st edn. Springer, Berlin
Arguelles-Arias A, Ongena M, Halimi B, Lara Y, Brans A, Joris B, Fickers P (2009) Bacillus amyloliquefaciens GA1 as a source of potent antibiotics and other secondary metabolites for biocontrol of plant pathogens. Microb Cell Factories 8(1):63–74. https://doi.org/10.1186/1475-2859-8-63
Balcázar JL, De Blas I, Ruiz-Zarzuela I, Cunningham D, Vendrell D, Múzquiz JL (2006) The role of probiotics in aquaculture. Vet Microbiol 114(3–4):173–186. https://doi.org/10.1016/j.vetmic.2006.01.009
Balcázar JL, Vendrell D, de Blas I, Ruiz-Zarzuela I, Muzquiz JL, Girones O (2008) Characterization of probiotic properties of lactic acid bacteria isolated from intestinal microbiota of fish. Aquaculture 278(1–4):188–191. https://doi.org/10.1016/j.aquaculture.2008.03.014
Bao Y, Zhang Y, Zhang Y, Liu Y, Wang S, Dong X, Wang Y, Zhang H (2010) Screening of potential probiotic properties of Lactobacillus fermentum isolated from traditional dairy products. Food Control 21(5):695–701. https://doi.org/10.1016/j.foodcont.2009.10.010
Bhatia SJ, Kochar N, Abraham P, Nair NG, Mehta AP (1989) Lactobacillus acidophilus inhibits growth of Campylobacter pylori in vitro. J Clin Microbiol 27(10):2328–2330
Blaxhall P, Daisley K (1973) Routine haematological methods for use with fish blood. J Fish Biol 5(6):771–781. https://doi.org/10.1111/j.1095-8649.1973.tb04510.x
Bondad-Reantaso MG, Subasinghe RP, Arthur JR, Ogawa K, Chinabut S, Adlard R, Tan Z, Shariff M (2005) Disease and health management in Asian aquaculture. Vet Parasitol 132(3–4):249–272. https://doi.org/10.1016/j.vetpar.2005.07.005
Buntin N, Chanthachum S, Hongpattarakere T (2008) Screening of lactic acid bacteria from gastrointestinal tracts of marine fish for their potential use as probiotics. Sonklanakarin J Sci Technol 30(1):141–148
Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55(4):611–622. https://doi.org/10.1373/clinichem.2008.112797
Capkin E, Altinok I (2009) Effects of dietary probiotic supplementations on prevention/treatment of yersiniosis disease. J Appl Microbiol 106(4):1147–1153. https://doi.org/10.1111/j.1365-2672.2008.04080.x
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(1–4):430–438. https://doi.org/10.1016/j.aquaculture.2006.04.025
Cebeci A, Gürakan C (2003) Properties of potential probiotic Lactobacillus plantarum strains. Food Microbiol 20(5):511–518. https://doi.org/10.1016/S0740-0020(02)00174-0
Charteris WP, Kelly PM, Morelli L, Collins JK (1998) Ingredient selection criteria for probiotic microorganisms in functional dairy foods. Int J Dairy Technol 51(4):123–136. https://doi.org/10.1111/j.1471-0307.1998.tb02516.x
Chiu CH, Guu YK, Liu CH, Pan TM, Cheng W (2007) Immune responses and gene expression in white shrimp, Litopenaeus vannamei, induced by Lactobacillus plantarum. Fish Shellfish Immunol 23(2):364–377. https://doi.org/10.1016/j.fsi.2006.11.010
Cotter PD, Ross RP, Hill C (2013) Bacteriocins—a viable alternative to antibiotics? Nat Rev Microbiol 11(2):95–105. https://doi.org/10.1038/nrmicro2937
Darling CL (1975) Standardization and evaluation of the CAMP reaction for the prompt, presumptive identification of Streptococcus agalactiae (Lancefield group B) in clinical material. J Clin Microbiol 1(2):171–174
Das A, Sahoo P, Mohanty B, Jena J (2011) Pathophysiology of experimental Aeromonas hydrophila infection in Puntius sarana: early changes in blood and aspects of the innate immune-related gene expression in survivors. Vet Immunol Immunopathol 142(3–4):207–218. https://doi.org/10.1016/j.vetimm.2011.05.017
Das A, Nakhro K, Chowdhury S, Kamilya D (2013) Effects of potential probiotic Bacillus amyloliquifaciens FPTB16 on systemic and cutaneous mucosal immune responses and disease resistance of catla (Catla catla). Fish Shellfish Immunol 35(5):1547–1553. https://doi.org/10.1016/j.fsi.2013.08.022
Dawood MA, Koshio S, Ishikawa M, Yokoyama S (2015) Effects of heat killed Lactobacillus plantarum (LP20) supplemental diets on growth performance, stress resistance and immune response of red sea bream, Pagrus major. Aquaculture 442:29–36. https://doi.org/10.1016/j.aquaculture.2015.02.005
de La Banda IG, Lobo C, León-Rubio JM, Tapia-Paniagua S, Balebona MC, Moriñigo MA, Moreno-Ventas X, Lucas LM, Linares F, Arce F (2010) Influence of two closely related probiotics on juvenile Senegalese sole (Solea senegalensis, Kaup 1858) performance and protection against Photobacterium damselae subsp. piscicida. Aquaculture 306(1–4):281–288. https://doi.org/10.1016/j.aquaculture.2010.05.008
Díaz-Rosales P, Arijo S, Chabrillón M, Alarcón F, Tapia-Paniagua S, Martínez-Manzanares E, Balebona M, Moriñigo M (2009) Effects of two closely related probiotics on respiratory burst activity of Senegalese sole (Soleasenegalensis, Kaup) phagocytes, and protection against Photobacterium damselae subsp. piscicida. Aquaculture 293(1–2):16–21. https://doi.org/10.1016/j.aquaculture.2009.03.050
Dinarello CA (1996) Biologic basis for interleukin-1 in disease. Blood 87(6):2095–2147
Erkkilä S, Petäjä E (2000) Screening of commercial meat starter cultures at low pH and in the presence of bile salts for potential probiotic use. Meat Sci 55(3):297–300. https://doi.org/10.1016/S0309-1740(99)00156-4
Gill H (1998) Stimulation of the immune system by lactic cultures. Int Dairy J 8(5–6):535–544. https://doi.org/10.1016/S0958-6946(98)00074-0
Gioacchini G, Smith P, Carnevali O (2008) Effects of Ergosan on the expression of cytokine genes in the liver of juvenile rainbow trout (Oncorhynchus mykiss) exposed to enteric red mouth vaccine. Vet Immunol Immunopathol 123(3–4):215–222. https://doi.org/10.1016/j.vetimm.2008.01.037
Gionchetti P, Rizzello F, Helwig U, Venturi A, Lammers KM, Brigidi P, Vitali B, Poggioli G, Miglioli M, Campieri M (2003) Prophylaxis of pouchitis onset with probiotic therapy: a double-blind, placebo-controlled trial. Gastroenterology 124(5):1202–1209. https://doi.org/10.1016/S0016-5085(03)00171-9
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. https://doi.org/10.1016/j.fsi.2012.12.008
Giri S, Sukumaran V, Sen S, Jena P (2014) Effects of dietary supplementation of potential probiotic Bacillus subtilis VSG1 singularly or in combination with Lactobacillus plantarum VSG3 or/and Pseudomonas aeruginosa VSG2 on the growth, immunity and disease resistance of Labeo rohita. Aquac Nutr 20(2):163–171. https://doi.org/10.1111/anu.12062
Goetz FW, Planas JV, MacKenzie S (2004) Tumor necrosis factors. Dev Comp Immunol 28(5):487–497. https://doi.org/10.1016/j.dci.2003.09.008
Goldberg S, Doyle R, Rosenberg M (1990) Mechanism of enhancement of microbial cell hydrophobicity by cationic polymers. J Bacteriol 172(10):5650–5654
Gueimonde M, Salminen S (2006) New methods for selecting and evaluating probiotics. Dig Liver Dis 38(2):S242–S247. https://doi.org/10.1016/S1590-8658(07)60003-6
Holland J, Gould C, Jones C, Noble L, Secombes C (2003) The expression of immune-regulatory genes in rainbow trout, Oncorhynchus mykiss, during a natural outbreak of proliferative kidney disease (PKD). Parasitology 126(7):95–102. https://doi.org/10.1017/S0031182003003767
Jin L, Ho Y, Abdullah N, Ali M, Jalaludin S (1996) Antagonistic effects of intestinal Lactobacillus isolates on pathogens of chicken. Lett Appl Microbiol 23(2):67–71. https://doi.org/10.1111/j.1472-765X.1996.tb00032.x
Kader MA, Koshio S, Ishikawa M, Yokoyama S, Bulbul M (2010) Supplemental effects of some crude ingredients in improving nutritive values of low fishmeal diets for red sea bream, Pagrus major. Aquaculture 308(3–4):136–144. https://doi.org/10.1016/j.aquaculture.2010.07.037
Kaushik JK, Kumar A, Duary RK, Mohanty AK, Grover S, Batish VK (2009) Functional and probiotic attributes of an indigenous isolate of Lactobacillus plantarum. PLoS One 4(12):8099–8109. https://doi.org/10.1371/journal.pone.0008099
Kim DH, Austin B (2006) Cytokine expression in leucocytes and gut cells of rainbow trout, Oncorhynchus mykiss Walbaum, induced by probiotics. Vet Immunol Immunopathol 114(3–4):297–304. https://doi.org/10.1016/j.vetimm.2006.08.015
Kumar R, Mukherjee SC, Prasad KP, Pal AK (2006) Evaluation of Bacillus subtilis as a probiotic to Indian major carp Labeo rohita (Ham.). Aquac Res 37(12):1215–1221. https://doi.org/10.1111/j.1365-2109.2006.01551.x
Lähteinen T, Malinen E, Koort JM, Mertaniemi-Hannus U, Hankimo T, Karikoski N, Pakkanen S, Laine H, Sillanpää H, Söderholm H (2010) Probiotic properties of Lactobacillus isolates originating from porcine intestine and feces. Anaerobe 16(3):293–300. https://doi.org/10.1016/j.anaerobe.2009.08.002
Lee YK, Puong KY (2002) Competition for adhesion between probiotics and human gastrointestinal pathogens in the presence of carbohydrate. Br J Nutr 88(1):101–108. https://doi.org/10.1079/BJN2002635
Liu Y, Chen SL, Meng L, Zhang YX (2007) Cloning, characterization and expression analysis of a novel CXC chemokine from turbot (Scophthalmus maximus). Fish Shellfish Immunol 23(4):711–720. https://doi.org/10.1016/j.fsi.2007.01.008
Liu W, Ren P, He S, Xu L, Yang Y, Gu Z, Zhou Z (2013) Comparison of adhesive gut bacteria composition, immunity, and disease resistance in juvenile hybrid tilapia fed two different Lactobacillus strains. Fish Shellfish Immunol 35(1):54–62. https://doi.org/10.1016/j.fsi.2013.04.010
Low C, Wadsworth S, Burrells C, Secombes C (2003) Expression of immune genes in turbot (Scophthalmus maximus) fed a nucleotide-supplemented diet. Aquaculture 221(1–4):23–40. https://doi.org/10.1016/S0044-8486(03)00022-X
Maragkoudakis PA, Zoumpopoulou G, Miaris C, Kalantzopoulos G, Pot B, Tsakalidou E (2006) Probiotic potential of Lactobacillus strains isolated from dairy products. Int Dairy J 16(3):189–199. https://doi.org/10.1016/j.idairyj.2005.02.009
Marin ML, Tejada-Simon MV, Lee JH, Murtha J, Ustunol Z, Pestka JJ (1998) Stimulation of cytokine production in clonal macrophage and T-cell models by Streptococcus thermophilus: comparison with Bifidobacterium sp. and Lactobacillus bulgaricus. J Food Prot 61(7):859–864. https://doi.org/10.4315/0362-028X-61.7.859
Matsuzaki T, Chin J (2000) Modulating immune responses with probiotic bacteria. Immunol Cell Biol 78(1):67–73. https://doi.org/10.1046/j.1440-1711.2000.00887.x
Merrifield DL, Dimitroglou A, Foey A, Davies SJ, Baker RT, Bøgwald J, Castex M, Ringø E (2010) The current status and future focus of probiotic and prebiotic applications for salmonids. Aquaculture 302(1–2):1–18. https://doi.org/10.1016/j.aquaculture.2010.02.007
Midolo P, Lambert J, Hull R, Luo F, Grayson M (1995) In vitro inhibition of Helicobacter pylori NCTC 11637 by organic acids and lactic acid bacteria. J Appl Bacteriol 79(4):475–479. https://doi.org/10.1111/j.1365-2672.1995.tb03164.x
Miettinen M, Vuopio-Varkila J, Varkila K (1996) Production of human tumor necrosis factor alpha, interleukin-6, and interleukin-10 is induced by lactic acid bacteria. Infect Immun 64(12):5403–5405
Mohammadian T, Alishahi M, Tabandeh MR, Ghorbanpoor M, Gharibi D, Tollabi M, Rohanizade S (2016) Probiotic effects of Lactobacillus plantarum and L. delbrueckii ssp. bulguricus on some immune-related parameters in Barbus grypus. Aquac Int 24(1):225–242. https://doi.org/10.1007/s10499-015-9921-8
Mohammadian T, Alishahi M, Tabandeh MR, Ghorbanpoor M, Gharibi D (2017) Effect of Lactobacillus plantarum and Lactobacillus delbrueckii subsp. bulgaricus on growth performance, gut microbial flora and digestive enzymes activities in Tor grypus (Karaman, 1971). Iran J Fish Sci 16(1):296–317
Moreno MF, Sarantinopoulos P, Tsakalidou E, De Vuyst L (2006) The role and application of enterococci in food and health. Int J Food Microbiol 106(1):1–24. https://doi.org/10.1016/j.ijfoodmicro.2005.06.026
Nayak S (2010) Probiotics and immunity: a fish perspective. Fish Shellfish Immunol 29(1):2–14. https://doi.org/10.1016/j.fsi.2010.02.017
Nikoskelainen S, Salminen S, Bylund G, Ouwehand AC (2001) Characterization of the properties of human-and dairy-derived probiotics for prevention of infectious diseases in fish. Appl Environ Microbiol 67(6):2430–2435. https://doi.org/10.1128/AEM.67.6.2430-2435.2001
Niku-Paavola ML, Laitila A, Mattila-Sandholm T, Haikara A (1999) New types of antimicrobial compounds produced by Lactobacillus plantarum. J Appl Microbiol 86(1):29–35. https://doi.org/10.1046/j.1365-2672.1999.00632.x
Olayinka AS, Afolabi OO (2013) Evaluation of the effects of Lactobacillus acidophilus on the haematological parameters of Clarias gariepinus. Int J Res Fish Aquac 3(2):38–41
Otero MC, Ocaña VS, Nader-Macías ME (2004) Bacterial surface characteristics applied to selection of probiotic microorganisms. In: Spencer JFT, Ragout de Spencer AL (eds) Public health microbiology: methods and protocols. Humana Press Inc., Totowa, pp 435–440
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(1–4):241–254. https://doi.org/10.1016/j.aquaculture.2004.09.032
Panigrahi A, Kiron V, Satoh S, Hirono I, Kobayashi T, Sugita H, Puangkaew J, Aoki T (2007) Immune modulation and expression of cytokine genes in rainbow trout Oncorhynchus mykiss upon probiotic feeding. Dev Comp Immunol 31(4):372–382. https://doi.org/10.1016/j.dci.2006.07.004
Panigrahi A, Viswanath K, Satoh S (2011) Real-time quantification of the immune gene expression in rainbow trout fed different forms of probiotic bacteria Lactobacillus rhamnosus. Aquac Res 42(7):906–917. https://doi.org/10.1111/j.1365-2109.2010.02633.x
Pérez-Sánchez T, Balcázar JL, Merrifield DL, Carnevali O, Gioacchini G, de Blas I, 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(2):196–201. https://doi.org/10.1016/j.fsi.2011.05.005
Pérez-Sánchez T, Ruiz-Zarzuela I, Blas I, Balcázar JL (2014) Probiotics in aquaculture: a current assessment. Rev Aquac 6(3):133–146. https://doi.org/10.1111/raq.12033
Pfaffl MW (2007) qPCR 2007 event: Proceedings. In: Abstracts of the 3rd International qPCR Symposium. Technical University Munich (TUM), Munich
Prasad J, Gill H, Smart J, Gopal PK (1998) Selection and characterisation of Lactobacillus and Bifidobacterium strains for use as probiotics. Int Dairy J 8(12):993–1002. https://doi.org/10.1016/S0958-6946(99)00024-2
Rangavajhyala N, Shahani K, Sridevi G, Srikumaran S (1997) Nonlipopolysaccharide components of Lactobacillus addophilus stimulate (s) the production of interleukin-1α and tumor necrosis factor-α by murine macrophages. Nutr Cancer 28(2):130–134. https://doi.org/10.1080/01635589709514564
Ringø E, Gatesoupe FJ (1998) Lactic acid bacteria in fish: a review. Aquaculture 160(3–4):177–203. https://doi.org/10.1016/S0044-8486(97)00299-8
Rollo A, Sulpizio R, Nardi M, Silvi S, Orpianesi C, Caggiano M, Cresci A, Carnevali O (2006) Live microbial feed supplement in aquaculture for improvement of stress tolerance. Fish Physiol Biochem 32(2):167–177. https://doi.org/10.1007/s10695-006-0009-2
Román L, Real F, Padilla D, El Aamri F, Déniz S, Grasso V, Acosta F (2013) Cytokine expression in head-kidney leucocytes of European sea bass (Dicentrarchus labrax L.) after incubation with the probiotic Vagococcus fluvialis L-21. Fish Shellfish Immunol 35(4):1329–1332. https://doi.org/10.1016/j.fsi.2013.07.036
Sahoo P, Mukherjee S, Sahoo S (1998) Aeromonas hydrophila versus Edwardsiella tarda: a pathoanatomical study in Clarias batrachus. J Aquacult 6:57–66
Secombes C, Wang T, Hong S, Peddie S, Crampe M, Laing K, Cunningham C, Zou J (2001) Cytokines and innate immunity of fish. Dev Comp Immunol 25(8–9):713–723. https://doi.org/10.1016/S0145-305X(01)00032-5
Stoskopf M (1993) Clinical pathology in fish medicine. WB Saunders Company, Hartcourt Brace Jovanourah Inc., Philadelphia
Sumeri I, Arike L, Stekolštšikova J, Uusna R, Adamberg S, Adamberg K, Paalme T (2010) Effect of stress pretreatment on survival of probiotic bacteria in gastrointestinal tract simulator. Appl Microbiol Biotechnol 86(6):1925–1931. https://doi.org/10.1007/s00253-009-2429-2
Tovar-Ramírez D, Mazurais D, Gatesoupe J, Quazuguel P, Cahu C, Zambonino-Infante J (2010) Dietary probiotic live yeast modulates antioxidant enzyme activities and gene expression of sea bass (Dicentrarchus labrax) larvae. Aquaculture 300(1–4):142–147. https://doi.org/10.1016/j.aquaculture.2009.12.015
Wang YB, Han JZ (2007) The role of probiotic cell wall hydrophobicity in bioremediation of aquaculture. Aquaculture 269(1–4):349–354. https://doi.org/10.1016/j.aquaculture.2007.04.010
Zhang H, Liu L, Yangling H, Zhong S, Liu H, Han T, Xie Y (2013) Isolation and partial characterization of a bacteriocin produced by Lactobacillus plantarum BM-1 isolated from a traditionally fermented Chinese meat product. Microbiol Immunol 57:746–755. https://doi.org/10.1111/1348-0421.12091
Zou J, Peddie S, Scapigliati G, Zhang Y, Bols N, Ellis A, Secombes C (2003) Functional characterisation of the recombinant tumor necrosis factors in rainbow trout, Oncorhynchus mykiss. Dev Comp Immunol 27(9):813–822. https://doi.org/10.1016/S0145-305X(03)00077-6
Funding
This work was funded by a grant from Shahid Chamran University of Ahvaz Research Council (Grant Nos. 27176, 1393.3.2).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
All institutional and national guidelines for the care and use of laboratory animals were followed.
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Mohammadian, T., Alishahi, M., Tabandeh, M.R. et al. Effects of autochthonous probiotics, isolated from Tor grypus (Karaman, 1971) intestine and Lactobacillus casei (PTCC 1608) on expression of immune-related genes. Aquacult Int 27, 239–260 (2019). https://doi.org/10.1007/s10499-018-0320-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10499-018-0320-9