Skip to main content
Log in

Immune modulation, disease resistance and growth performance of Indian farmed carp, Labeo rohita (Hamilton), in response to dietary consortium of putative lactic acid bacteria

  • Published:
Aquaculture International Aims and scope Submit manuscript

Abstract

Probiotic effect of a consortium of putative lactic acid bacteria on Labeo rohita was investigated with emphasis on growth performance, immune response, and disease resistance against Aeromonas hydrophila. Fish were fed either a lactic acid bacteria-supplemented diet or a control diet for a period of 30 days. At the end of the experiment, probiotic fed group showed a significant improvement in weight gain percentage, specific growth rate, and feed conversion ratio along with increased respiratory burst activity of blood phagocytes and serum antiprotease activity level. Quantitative real-time PCR showed significant upregulation of IL-10 gene in kidney, intestine, and liver of probiotic-treated group, whereas TNF-α gene was significantly upregulated only in liver and intestine. HSP70 gene was significantly upregulated in intestine but downregulated in liver on day 15. Challenge with Aeromonas hydrophila on day 30 of probiotic feeding showed a significant increase in survival percentage of treated (93.33 %) over the control group (33.33 %). Further challenge after 20 and 40 days of withdrawal of probiotic showed higher survival percentage (60 and 40 %, respectively) in withdrawn group compared to control although difference was statistically insignificant. The consortium of putative probionts may serve simultaneously as an immunomodulating feed additive useful for disease protection and growth enhancer in eco-friendly freshwater aquaculture practices. However, feeding at regular interval with probiotic supplemented diet is suggested for a prolonged immunity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aly SM, Abdel-Galil Ahmed Y, Abdel-Aziz Ghareeb A, Mohamed MF (2008) 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

    Article  CAS  PubMed  Google Scholar 

  • Anderson DP, Siwicki AK (1995) Basic hematology and serology for fish health programs. In: Shariff M, Arthur JR, Subasinghe RP (eds) Diseases in Asian aquaculture II. Fish health section. Asian Fisheries Society, Manila, pp 185–202

    Google Scholar 

  • Balcazar JL, de Blas I, Ruiz-Zarzuela I, Vendrell D, Calvo AC, Marquez I, Girones O, Muzquiz JL (2007) Changes in intestinal microbiota and humoral immune response following probiotic administration in brown trout (Salmo trutta). Br J Nutr 97:522–527

    Article  CAS  PubMed  Google Scholar 

  • Beck BR, Kim D, Jeon J, Lee SM, Kim HK, Kim OJ, Lee JI, Suh BS, Do HK, Lee KH, Holzapfel WH, Hwang JY, Kwon MG, Song SK (2015) The effects of combined dietary probiotics Lactococcus lactis BFE920 and Lactobacillus plantarum FGL0001 on innate immunity and disease resistance in olive flounder (Paralicthys olivaceus). Fish Shellfish Immunol 42:177–183

    Article  CAS  PubMed  Google Scholar 

  • Choudhury D, Pal AK, Sahu NP, Kumar S, Das SS, Mukherjee SC (2005) Dietary yeast RNA supplementation reduces mortality by Aeromonas hydrophila in rohu (Labeo rohita L.) juveniles. Fish Shellfish Immunol 19:281–291

    Article  CAS  PubMed  Google Scholar 

  • Daugard M, Rohde M, Jaattela M (2007) The heat shock protein 70 family: highly homologous 24 proteins with overlapping and distinct functions. FEBS Lett 581:3702–3710

    Article  Google Scholar 

  • Dimitroglou A, Merrifield DL, Carnevali O, Picchietti S, Avella M, Daniels C, Guroy D, Davies SJ (2011) Microbial manipulations to improve fish health and production—a Mediterranean perspective. Fish Shellfish Immunol 30:1–16

    Article  CAS  PubMed  Google Scholar 

  • Ellis AE (1990) Serum antiproteases in fish. In: Stolen JS, Fletcher TC, Anderson DP, Roberson BS, van Muiswinkel WB (eds) Techniques in fish immunology. SOS Publications, Fair Haven, NJ, pp 95–99

    Google Scholar 

  • Eslamloo K, Akhavan SR, Henry MA (2013) Effects of dietary administration of Bacillus probiotics on the non-specific immune responses of tinfoil barb, Barbonymus schwanenfeldii (Actinopterygii: Cypriniformes: Cyprinidae). Acta Icthyol Piscat 43:211–218

    Article  Google Scholar 

  • Food and Agriculture Organization of the United Nations (FAO) (2001) Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. In the joint FAO/WHO expert consultation report on evaluation of health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria (October 2001)

  • Geng X, Dong X-H, Tan B-P, Yang Q-H, Chi S-Y, Liu H-Y, Liu X-Q (2012) Effects of dietary probiotic on the growth performance, non-specific immunity and disease resistance of cobia, Rachycentron canadum. Aquac Nutr 18:46–55

    Article  CAS  Google Scholar 

  • Ghosh S, Sinha A, Sahu C (2007) Isolation of putative probionts from the intestines of Indian major carps. Isr J Aquac Bamid 59:127–132

    Google Scholar 

  • Gioacchini G, Giorgini E, Olivotto I, Maradonna F, Merrifield DL, Carnevali O (2014) The influence of probiotics on zebra fish Danio rerio innate immunity and hepatic stress. Zebrafish 11:98–106

    Article  PubMed  Google Scholar 

  • Giri SS, Sukumaran V, Sen SS, Jena PK (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 20:163–171

    Article  CAS  Google Scholar 

  • He S, Liu W, Zhou Z, Mao W, Ren P, Marubashi T, Ringo E (2011) Evaluation of probiotic strain Bacillus subtilis C-3102 as a feed supplement for koi carp (Cyprinus carpio). J Aquac Res Development. doi:10.4172/2155-9546.S1-005

    Google Scholar 

  • He S, Zhang Y, Xu L, Yang Y, Marubashi T, Zhou Z, Yao B (2013) Effects of dietary Bacillus subtilis C-3102 on the production, intestinal cytokine expression and autochthonous bacteria of hybrid tilapia Oreochromis niloticus ♀ × Oreochromis aureus ♂. Aquaculture 412-413:125–130

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kumari J, Swain T, Sahoo PK (2003) Dietary bovine lactoferrin induces changes in immunity level and disease resistance in Asian catfish Clarias batrachus. Vet Immunol Immunopathol 94:1–9

    Article  CAS  PubMed  Google Scholar 

  • Lavasani S, Dzhambazov B, Nouri M, Fak F, Buske S, Molin G, Thorlacius H, Alenfall J, Jeppsson B, Westrom B (2010) A novel probiotic mixture exerts a therapeutic effect on experimental autoimmune encephalomyelitis mediated by IL-10 producing regulatory T cells. PLoS One 5:e9009. doi:10.1371/journal.pone.0009009

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu W, Ren P, He S, Xu L, Yang Y, 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 35:54–62

    Article  PubMed  Google Scholar 

  • Livak KJ, Schmittgen DT (2001) Analysis of relative gene expression data using real time quantitative PCR and the 2-ΔΔC T method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Maji UJ, Mohanty S, Mahapatra AS, Maiti NK (2016) Diversity and probiotic potentials of putative lactic acid bacteria for application in freshwater aquaculture. Turk J Fish Aquat Sci 16:805–818

    Article  Google Scholar 

  • Medina M, Izquierdo M, Ennahar S, Sanz Y (2007) Differential immunomodulatory properties of Bifidobacterium logum strains: relevance to probiotic selection and clinical applications. Clin Exp Immunol 150:531–538

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mirlohi M, Soleimanian-Zad S, Dokhani S, Sheikh-Zeinodin M, Abghary A (2009) Investigation of acid and bile tolerance of native Lactobacilli isolated from fecal samples and commercial probiotics by growth and survival studies. Iran J Biotech 7:233–240

    Google Scholar 

  • Mohapatra S, Chakraborty T, Prusty AK, Das P, Paniprasad K, Mohanta KN (2012) Use of different microbial probiotics in the diet of rohu, Labeo rohita fingerlings: effects on growth, nutrient digestibility and retention, digestive enzyme activities and intestinal microflora. Aquac Nutr 18:1–11

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • O’Shea EF, O’Connor PM, Raftis EJ, O’Toole PW, Stanton C, Cotter PD, Ross RP, Hill C (2011) Production of multiple bacteriocins from a single locus by gastrointestinal strains of Lactobacillus salivarius. J Bacteriol 193:6973–6982

    Article  PubMed  PubMed Central  Google Scholar 

  • Pagnini C, Saeed R, Bamias G, Arseneau KO, Pizarro TT, Cominelli F (2010) Probiotics promote gut health through stimulation of epithelial innate immunity. Proc Natl Acad Sci U S A 107:454–459

    Article  CAS  PubMed  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 243:241–254

    Article  Google Scholar 

  • Panigrahi A, Kiron V, Satoh S, Hirono H, 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 31:372–382

    Article  CAS  PubMed  Google Scholar 

  • Parthasarthy R, 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

    Google Scholar 

  • Perez-Sanchez T, Balcazar 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 31:196–201

    Article  CAS  PubMed  Google Scholar 

  • Picchietti S, Fausto AM, Randelli E, Carnevali O, Taddei AR, Buonocore F, Scapigliati G, Abelli L (2009) Early treatment with Lactobacillus delbruekii 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

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Reyes-Becerril M, Tovar-Ramírez D, Ascencio-Valle F, Civera-Cerecedo R, Gracia-Lopez V, Barbosa-Solomieu V, Esteban MA (2011) Effects of dietary supplementation with probiotic live yeast Debaryomyces hansenii on the immune and antioxidant systems of leopard grouper Mycteroperca rosacea infected with Aeromonas hydrophila. Aquac Res 42:1676–1686

    Article  CAS  Google Scholar 

  • Rollo A, Sulpizi 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 32:167–177

    Article  CAS  Google Scholar 

  • Sahoo PK, Kumari J, Mishra BK (2005) Non-specific immune responses in juveniles of Indian major carps. J Appl Ichthyol 21:151–155

    Article  Google Scholar 

  • Sahoo PK, Rauta PR, Mohanty BR, Mahapatra KD, Saha JN, Rye M, Eknath AE (2011) Selection for improved resistance to Aeromonas hydrophila in Indian major carp Labeo rohita: survival and innate immune responses in first generation of resistant and susceptible lines. Fish Shellfish Immunol 31:432–438

    Article  CAS  PubMed  Google Scholar 

  • Sahu I, Das BK, Marhual N, Samanta M, Mishra BK, Eknath AE (2011) Toxicity of crude extracellular products of Aeromonas hydrophila on rohu, Labeo rohita (Ham.). Indian J Microbiol 51:515–520

    Article  PubMed  PubMed Central  Google Scholar 

  • Saini VP, Ojha ML, Gupta MC, Nair P, Sharma A, Luhar V (2014) Effect of dietary probiotic on growth performance and disease resistance in Labeo rohita (Ham.) fingerlings. Int J Fish Aquat Stud 1:07–11

    Google Scholar 

  • Salinas I, Abelli L, Bertoni F, Picchietti S, Roque A, Furones D, Cuesta A, Meseguer J, Esteban MA (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

    Article  CAS  PubMed  Google Scholar 

  • Sharifuzzaman SM, Austin B (2010) Development of protection in rainbow trout (Oncorhynchus mykiss, Walbaum) to Vibrio anguillarum following use of the probiotic Kocuria SM1. Fish Shellfish Immunol 29:212–216

    Article  CAS  PubMed  Google Scholar 

  • Son VM, Chang CC, Wu MC, Guu YK, Chiu CH, 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 26:691–698

    Article  CAS  PubMed  Google Scholar 

  • Srinu B, Madhava Rao T, Mallikarjuna Reddy PV, Kondal Reddy K (2013) Evaluation of different lactic acid bacterial strains for probiotic characteristics. Vet World 6:785–788

    Article  Google Scholar 

  • Standen BT, Rawling MD, Davies SJ, Castex M, Foey A, Gioacchini G, Carnevali O, Merrifield DL (2013) Probiotic Pediococcus acidilactici modulates both localized intestinal and peripheral-immunity in tilapia (Oreochromis niloticus). Fish Shellfish Immunol 35:1097–1104

    Article  CAS  Google Scholar 

  • Standen BT, Rodiles A, Peggs DL, Davies SJ, Santos GA, Merrifield DL (2015) Modulation of the intestinal microbiota and morphology of tilapia, Oreochromis niloticus, following the application of a multi-species probiotic. Appl Microbiol Biotechnol 99:8403–8417

    Article  CAS  PubMed  Google Scholar 

  • Swain B, Basu M, Samanta M (2011) Cloning of interleukin-10 gene in the Indian major carp, Labeo rohita (Hamilton 1822) and its functional characterization following Aeromonas hydrophila infection. Indian J Fish 58:39–47

    Google Scholar 

  • Timmerman HM, Koning CJ, Mulder L, Rombouts FM, Beyen AC (2004) Monostrain, multistrain and multispecies probiotics—a comparison of functionality and efficacy. Int J Food Microbiol 96:219–233

    Article  CAS  PubMed  Google Scholar 

  • Utiswannakul P, Sangchai S, Rengpipat S (2011) Enhanced growth of black tiger shrimp Penaeus monodon by dietary supplementation with Bacillus (BP11) as a probiotic. J Aquac Res Dev 3. doi: 10.4172/2155-9546.S1-006

  • Zhang A, Guo Y, Zhang S, Fan X, Wang X, Zhou X, Yang K, Zhou H (2015) Cytokine effects and cellular signaling pathways of grass carp HSP70 in head kidney leukocytes. Fish Shellfish Immunol 46:550–556

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Financial assistance for this work from the Application of Microorganisms in Agriculture and Allied Sectors (AMAAS), National Bureau of Agriculturally Important Microorganisms (NBAIM) project of Indian Council of Agricultural Research, New Delhi, India is duly acknowledged.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sriprakash Mohanty.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Maji, U.J., Mohanty, S., Pradhan, A. et al. Immune modulation, disease resistance and growth performance of Indian farmed carp, Labeo rohita (Hamilton), in response to dietary consortium of putative lactic acid bacteria. Aquacult Int 25, 1391–1407 (2017). https://doi.org/10.1007/s10499-017-0122-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10499-017-0122-5

Keywords

Navigation