Skip to main content
Log in

Inclusion of Pediococcus acidilactici as probiotic candidate in diets for beluga (Huso huso) modifies biochemical parameters and improves immune functions

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

Administration of probiotic candidates in fish has generally been shown as a useful strategy to improve growth performance, survival, digestive enzyme activity, and gut microbiota. Unfortunately, the sero-immunological responses of different fish to different probiotic candidates are poorly understood. The present study assessed the effect of Pediococcus acidilactici as a probiotic on the biochemical and immunological parameters of beluga. Fish (248.32 ± 10.21 g) were fed a control diet (without P. acidilactici( and three different doses of P. acidilactici-supplemented diets (107, 108, and 109 CFUg−1 diets) for 8 weeks. On week 8, blood and serum were sampled. Dose-dependent increase of immunological parameters (respiratory burst activity, lysozyme content, serum antibacterial activity, and total immunoglobulin) and biochemical parameters (total protein and albumin levels) was observed. However, alanine aminotransferase (ALT) and aspartate aminotransferase (AST) were significantly increased in the juvenile beluga fed by 109 CFUg−1 P. acidilactici-supplemented diet compared to the other groups. Based on the results of this evaluation, it is reasonable to conclude that the inclusion of P. acidilactici as probiotic in diets for juvenile beluga improves the sero-immunological parameters of the fish and should be considered by farmers as a strategy to improve fish health.

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
Fig. 4

Similar content being viewed by others

References

  • Abd El-Rhman AMA, Khattab YAE, Shalaby AME (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. https://doi.org/10.1016/j.fsi.2009.03.020

    Article  PubMed  Google Scholar 

  • Akrami R, Hajimoradloo A, Matinfar A, Abedian Kinari A (2009) Effect of dietary prebiotic inulin on growth performance, intestinal microflora, body composition and hematological parameters of juvenile beluga, Huso huso (Linnaeus, 1758). J World Aquacult Soci 40:771–779. https://doi.org/10.1111/j.1749-7345.2009.00297.x

    Article  Google Scholar 

  • 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 40:642–1652. https://doi.org/10.1111/j.1365-2109.2009.02265.x

    Article  CAS  Google Scholar 

  • Al-Dohail MA, Hashim R, Aliyu-Paiko M (2011) Evaluating the use of Lactobacillus acidophilus as a biocontrol agent against common pathogenic bacteria and the effects on the haematology parameters and histopathology in African catfish Clarias gariepinus juveniles. Aquac Res 42:196–209. https://doi.org/10.1111/j.1365-2109.2010.02606.x

    Article  CAS  Google Scholar 

  • Aly SM, Mohamed MF, John G (2008a) Effect of probiotics on the survival, growth and challenge infection in Tilapia nilotica (Oreochromis niloticus). Aquacult Res 39:647–656. https://doi.org/10.1111/j.1365-2109.2008.01932.x

    Article  CAS  Google Scholar 

  • Aly SM, Ahmed YA, Aziz AAG, Mohamed MF (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. https://doi.org/10.1016/j.fsi.2008.03.013

    Article  PubMed  CAS  Google Scholar 

  • Amar CE, Kiron V, Satoh S, Okamoto N, Watanabe T (2000) Effect of dietary β-carotene on the immune response of rainbow trout Oncorhynchus mykiss. Fisher Sci 66:1068–1075. https://doi.org/10.1046/j.1444-2906.2000.00170.x

    Article  CAS  Google Scholar 

  • Anastasiadou S, Papagianni M, Filiousis G, 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. https://doi.org/10.1016/j.biortech.2007.11.015

    Article  PubMed  CAS  Google Scholar 

  • Askarian F, Kousha A, Salma W, Ringø E (2011) The effect of lactic acid bacteria administration on growth, digestive enzyme activity and gut microbiota in Persian sturgeon (Acipenser persicus) and beluga (Huso huso) fry. Aquacult Nut 17:488–497. https://doi.org/10.1111/j.1365-2095.2010.00826.x

    Article  Google Scholar 

  • Aubin J, Gatesoupe FJ, Labbé L, Lebrun L (2005) Trial of probiotics to prevent the vertebral column compression syndrome in rainbow trout (Oncorhynchus mykiss Walbaum). Aquac Res 367:58–767. https://doi.org/10.1111/j.1365-2109.2005.01280.x

    Article  Google Scholar 

  • Balcázar JL, de Blas I, Ruiz-Zarzuela I, Vendrell D, Calvo AC, Márquez I, Gironés O, Muzquiz JL (2007) Changes in intestinal microbiota and humoral immune response following probiotic administration in brown trout (Salmo trutta). British J Nutri 97:522–527. https://doi.org/10.1017/S0007114507432986

    Article  CAS  Google Scholar 

  • Binaii M, Ghiasi M, Farabi SMV, Pourgholam R, Fazli H, Safari R, Alavi SE, Taghavi MJ, Bankehsaz Z (2014) Biochemical and hemato-immunological parameters in juvenile beluga (Huso huso) following the diet supplemented with nettle (Urtica dioica). Fish Shellfish Immunol 36:46–51. https://doi.org/10.1016/j.fsi.2013.10.001

    Article  PubMed  CAS  Google Scholar 

  • Castex M, Lemaire P, Wabete N, Chim L (2010) Effect of probiotic Pediococcus acidilactici on antioxidant defenses and oxidative stress of Litopenaeus stylirostris under Vibrio nigripulchritudo challenge. Fish Shellfish Immunol 28:622–631. https://doi.org/10.1016/j.fsi.2009.12.024

    Article  PubMed  CAS  Google Scholar 

  • Ellis AE (1990) In: Stolen JS, Fletcher TC, Anderson DP, Robertson BS, Van Muisvinkel WR (eds) Lysozyme assay in techniques in fish immunology. Fair Haven, USA

    Google Scholar 

  • Ellis AE (1999) Immunity to bacteria in fish. Fish Shellfish Immunol 9:291–308

    Article  Google Scholar 

  • Falahatkar B, Soltani M, Abtahi B, Kalbassi R, Pourkazemi M (2006) Effects of dietary vitamin C supplementation on performance, tissue chemical composition and alkaline phosphatase activity in great sturgeon (Huso huso). J Appl Ichthyol 22:283–286. https://doi.org/10.1111/j.1439-0426.2007.00969.x

    Article  Google Scholar 

  • FAO/WHO/OIE (2006) Expert consultation on antimicrobial use in aquaculture and antimicrobial resistance. Republic of South Korea, Seoul

    Google Scholar 

  • Faramarzi M, Jafaryan H, Patimar R, Iranshahi F, Boloki ML, Farahi A (2011) The effects of different concentrations of probiotic Bacillus spp. and different bioencapsulation times on growth performance and survival rate of Persian sturgeon (Acipenser persicus) larvae. World J Fish Marine Sci 3:145–150

    Google Scholar 

  • Faramarzi M, Jafaryan H, Roozbehfar R, Jafari M, Biria M (2012a) Influences of probiotic bacilli on ammonia and urea excretion in two conditions of starvation and satiation in Persian sturgeon (Acipenser persicus) larvae. Global Veterina 8:185–189

    CAS  Google Scholar 

  • Faramarzi M, Jafaryan H, Roozbehfar R, Jafari M, Rashidi Y, Biria M (2012b) Influences of probiotic bacilli via bioencapsulated daphnia magna on resistance of Persian sturgeon larvae against challenge tests. Global Veterina 8:421–425

    Google Scholar 

  • Ferguson RM, Merrifield DL, Harper GM, Rawling MD, Mustafa S, Picchietti S, Balcazar JL, Davies SJ (2010) The effect of Pediococcus acidilactici on the gut microbiota and immune status of on-growing red tilapia (Oreochromis niloticus). J Appl Microbiol 109:851–862. https://doi.org/10.1111/j.1365-2672.2010.04713.x

    Article  PubMed  CAS  Google Scholar 

  • Harikrishnan R, Balasundaram C, Heo MS (2010) Lactobacillus sakei BK19 enriched diet enhances the immunity status and disease resistance to streptococcosis infection in kelp grouper, Epinephelus bruneus. Fish Shellfish Immunol 29:1037–1043. https://doi.org/10.1016/j.fsi.2010.08.017

    Article  PubMed  CAS  Google Scholar 

  • Hosaeinifar SH, Mirvaghefi A, Amoozegar MA, Merrifield DL (2015) In vitro selection of a symbiotic and in vivo evaluation on intestinal microbiota, performance and physiological responses of rainbow trout (Oncorhynchus mikiss) fingerling. Aquac Nutr 23:111–119. https://doi.org/10.1111/anu.12373

    Article  CAS  Google Scholar 

  • Hoseinifar SH, Ringø E, Shenavar Masouleh A, Esteban MA (2014) Probiotic, prebiotic and synbiotic supplements in sturgeon aquaculture: a review. Rev Aquac 6:1–14. https://doi.org/10.1111/raq.12082

    Article  Google Scholar 

  • Iwashita MKP, Nakandakare IB, Terhune JS, Wood T, Ranzani-Paiva MJT (2015) Dietary supplementation with Bacillus subtilis, Saccharomyces cerevisiae and Aspergillus oryzae enhance immunity and disease resistance against Aeromonas hydrophila and Streptococcus iniae infection in juvenile tilapia Oreochromis niloticus. Fish Shellfish Immunol 43:60–66. https://doi.org/10.1016/j.fsi.2014.12.008

    Article  PubMed  CAS  Google Scholar 

  • Kamgar M, Ghane M (2014) Studies on Bacillus subtilis, as potential probiotics, on the hematological and biochemical parameters of rainbow trout, Oncorhynchus mykiss (Walbaum). J Appl Environ Microbiol 2:203–207. https://doi.org/10.12691/jaem-2-5-1

    Article  Google Scholar 

  • Kamgar M, Pourgholam R, Ghiasi M, Ghane M (2013) Studies on Bacillus subtilis, as potential probiotics, on the biochemical parameters of rainbow trout, Oncorhynchus mykiss (Walbaum) to challenge infections. Adv Stud Biol 5:37–50

    Article  Google Scholar 

  • Kruger NJ (1994) The Bradford method for protein quantitation. Basic Protein and Peptide Protocols. Springer, Berlin

    Google Scholar 

  • Kumar R, Mukherjee SC, Ranjan R, Nayak SK (2008) Enhanced innate immune parameters in Labeo rohita (Ham.) following oral administration of Bacillus subtilis. Fish Shellfish Immunol 24:168–172. https://doi.org/10.1016/j.fsi.2007.10.008

    Article  PubMed  CAS  Google Scholar 

  • Liu CH, Chiu CH, Wang SW, Cheng W (2012) Dietary administration of the probiotic, Bacillus subtilis E20, enhaces the growth, innate immune responses, and disease resistance of the grouper, Epinephelus coioides. Fish Shellfish Immunol 33:699–706. https://doi.org/10.1016/j.fsi.2012.06.012

    Article  PubMed  CAS  Google Scholar 

  • Marcu A, Marcu A, Nichita I, Herman V, Pascu C, Costinar L, Cotarcă L (2010) Studies in the first outbreak of vibriosis associated with pasteurelosis at siberian sturgeon (Acipenser baerii) in the south-west region of Romania preliminary report. Anim Sci Biotechnol 43:36–39

    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 17:73–79. https://doi.org/10.1111/j.1365-2095.2009.00712.x

    Article  CAS  Google Scholar 

  • Mohapatra S, Chakraborty T, Kumar V, DeBoeck G, Mohanta KN (2013) Aquaculture and stress management: a review of probiotic intervention. Anim Physiol Anim Nutr 97:405–430. https://doi.org/10.1111/j.1439-0396.2012.01301.x

    Article  CAS  Google Scholar 

  • Nayak SK (2010) Probiotics and immunity: a fish perspective. Fish Shellfish Immunol 29:2–14. https://doi.org/10.1016/j.fsi.2010.02.017

    Article  PubMed  CAS  Google Scholar 

  • Nayak SK, Swain P, Mukherjee SC (2007) Effect of dietary supplementation of probiotic and vitamin C on the immune response of Indian major carp, Labeo rohita (Ham.). Fish Shellfish Immunol 23:892–896. https://doi.org/10.1016/j.fsi.2007.02.008

    Article  PubMed  CAS  Google Scholar 

  • Neissi A, Rafiee G, Nematollahi M, Safari O (2013) The effect of Pediococcus acidilactici bacteria used as probiotic supplement on the growth and non-specific immune responses of green terror, Aequidens rivulatus. Fish Shellfish Immunol 35:1976–1980. https://doi.org/10.1016/j.fsi.2013.09.036

    Article  PubMed  CAS  Google Scholar 

  • Nikoskelainen S, Ouwehand A, 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. https://doi.org/10.1016/S1050-4648(03)00023-8

    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 butyricum CB2. J Fish Dis 31:679–686. https://doi.org/10.1111/j.1365-2761.2008.00955.x

    Article  PubMed  CAS  Google Scholar 

  • 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. https://doi.org/10.1016/j.dci.2006.07.004

    Article  PubMed  CAS  Google Scholar 

  • Pascual P, Pedrajas JR, Toribio F, López-Barea J, Peinado J (2003) Effect of food deprivation on oxidative stress biomarkers in fish (Sparus aurata). Chemico Biological Intera 145:191–199. https://doi.org/10.1016/S0009-2797(03)00002-4

    Article  CAS  Google Scholar 

  • Paulsen SM, Engstad RE, Robertsen B (2001) Enhanced lysozyme production in Atlantic salmon (Salmo salar L.) macrophages treated with yeast b-glucan and bacterial lipopolysaccharide. Fish Shellfish Immunol. 11:23–37

    Article  PubMed  CAS  Google Scholar 

  • Peters TJ (1995) All about albumin: biochemistry, genetics, and medical applications. Academic Press, New York

    Google Scholar 

  • Rajikkannu M, Natarajan N, Santhanam P, Deivasigamani B, Ilamathi J, Janani S (2015) Effect of probiotics on the haematological parameters of Indian major carp (Labeo rohita). Int J Fisher Aquat Stua 2:105–109

    Google Scholar 

  • Rao YV, Das BK, Jyotyrmayee P, Chakrabarti R (2006) Effect of Achyranthes aspera on the immunity and survival of Labeo rohita infected with Aeromonas hydrophila. Fish Shellfish Immunol 20:263–273. https://doi.org/10.1016/j.fsi.2005.04.006

    Article  Google Scholar 

  • Rusev V, Rusenova N, Simeonov R, Stratev D (2016) Staphylococcus warneri and Shewanella putrefaciens co-infection in Siberian Sturgeon (Acipenser baerii) and hybrid Sturgeon (Huso huso x Acipenser baerii). J Microbiol Exp 3(1):00078. https://doi.org/10.15406/jmen.2016.03.00078

    Article  Google Scholar 

  • Safari O, Mehraban Sang Atash M (2013) Study on the effects of probiotic, Pediococcus acidilactici in the diet on some biological indices of Oscar Astronauts ocellatus. Int Res J Appl Basic Sci 4:3458–3464

    CAS  Google Scholar 

  • Safari R, Adel M, Ghiasi M, Saeidi Asl MR, Khalili E (2015) First isolation and identification of Vibrio vulnificus (biotype 2) from cultured sturgeon (Huso huso) in Iran. Caspian J Environ Sci 13:27–285

    Google Scholar 

  • Salaghi Z, Imanpuor M, Taghizadeh V (2013) Effect of different levels of probiotic primalac on growth performance and survival rate of Persian sturgeon (Acipenser persicus). Global Veterina 11:238–242

    Google Scholar 

  • Salinas I, Cuesta A, Esteban MA, Meseguer J (2005) Dietary administration of Lactobacillus delbrüeckii and Bacillus subtilis, single or combined, on gilthead seabream cellular innate immune responses. Fish Shellfish Immunol 19:67–77. https://doi.org/10.1016/j.fsi.2004.11.007

    Article  PubMed  CAS  Google Scholar 

  • Sharifuzzaman SM, Austin B (2009) Influence of probiotic feeding duration on disease resistance and immune parameters in rainbow trout. Fish Shellfish Immunol 27:440–445. https://doi.org/10.1016/j.fsi.2009.06.010

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Siwicki AK, Anderson DP, Rumsey GL (1994) Dietary intake of immunostimulants by rainbow trout affects non-specific immunity and protection against furunculosis. Vet Immunol Immunopathol 41:125–139. https://doi.org/10.1016/0165-2427(94)90062-0

    Article  PubMed  CAS  Google Scholar 

  • Soltani M, Shenavar Masouleh A, Ahmadi M, Pourkazemi M, Taherimirghaed A (2015) Antibacterial activity, antibiotic susceptibility and probiotic use of lactic acid bacteria (LAB) in Persian sturgeon (Acipenser persicus). Iranian J Aqua Anim Health 2:54–65

    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. https://doi.org/10.1016/j.fsi.2013.07.018

    Article  PubMed  CAS  Google Scholar 

  • Sun YZ, Yang HL, Ma RL, Lin WY (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 Immunol 29:803–809. https://doi.org/10.1016/j.fsi.2010.07.018

    Article  PubMed  Google Scholar 

  • Vaglio A, Landriscina C (1999) Changes in liver enzyme activity in the teleost Sparus aurata in response to cadmium intoxication. Ecotoxicol Environ Saf 43:111–116. https://doi.org/10.1006/eesa.1999.1778

    Article  PubMed  CAS  Google Scholar 

  • Valcarce DG, Pardo MÁ, Riesco MF, Cruz Z, Robles V (2015) Effect of diet supplementation with a commercial probiotic containing Pediococcus acidilactici (Lindner, 1887) on the expression of five quality markers in zebrafish (Danio rerio Hamilton, 1822) testis. J Appl Ichthyol 31:18–21. https://doi.org/10.1111/jai.12731

    Article  CAS  Google Scholar 

  • Vázquez JA, González MP, Murad MA (2005) Effects of lactic acid bacteria cultures on pathogenic microbiota from fish. Aquaculture 245:149–161. https://doi.org/10.1016/j.aquaculture.2004.12.008

    Article  Google Scholar 

  • Verschuere L, Rombaut G, Sorgeloos P, Verstraete W (2000) Probiotic bacteria as biological control agents in aquaculture. Microbiol Mole Biol Rev 64:655–671. https://doi.org/10.1128/MMBR.64.4.655-671.2000

    Article  CAS  Google Scholar 

  • Villamil L, Figueras A, Planas M, Novoa B (2010) Pediococcus acidilactici in the culture of turbot (Psetta maxima) larvae: administration pathways. Aquaculture 307:83–88. https://doi.org/10.1016/j.aquaculture.2010.07.004

    Article  Google Scholar 

  • Wang YB, Tian ZQ, Yao JT, Li W (2008) Effect of probiotics, Enterococcus faecium, on tilapia (Oreochromis niloticus) growth performance and immune response. Aquaculture 277:203–207. https://doi.org/10.1016/j.aquaculture.2008.03.007

    Article  Google Scholar 

  • Wang GX, Liu YL, Li FY, Gao HT, Lei Y, Liu XL (2010) Immunostimulatory activities of Bacillus simplex DR-834 to carp (Cyprinus carpio). Fish Shellfish Immunol 29:378–387. https://doi.org/10.1016/j.fsi.2010.08.017

    Article  PubMed  CAS  Google Scholar 

  • Wiegertjes GF, Stet RJM, Parmentier HK, Van Muiswinkel W (1996) Immunogenetics of disease resistance in fish; a comparable approach. Dev Comp Immunol 20:365–381. https://doi.org/10.1016/S0145-305X(96)00032-8

    Article  PubMed  CAS  Google Scholar 

  • Zar JH (1994) Biostatistical analysis. Prentice-Hall Inc., Englewood Cliffs

    Google Scholar 

  • Zare A, Azari-Takami G, Taridashti F, Khara H (2017) The effects of Pediococcus acidilactici as a probiotic on growth performance and survival rate of great sturgeon, Huso huso (Linnaeus, 1758). Iranian J Fisher Sci 16:150–161

    Google Scholar 

  • Zhao F, Cao J, Liu Q (2009) Study on pathology and etiology of hemorrhagic septicemia in Acipenser baerii. Acta Hydrobiol Sinica 33:316–323. https://doi.org/10.3724/SP.J.1035.2009.00316

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors wish to thank Dr. Esmaeli Mola and the staff of Shahid Rajaei propagation and cultivation center of sturgeon fish for their kind help during the experiment.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Maryam Ghiasi.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ghiasi, M., Binaii, M., Naghavi, A. et al. Inclusion of Pediococcus acidilactici as probiotic candidate in diets for beluga (Huso huso) modifies biochemical parameters and improves immune functions. Fish Physiol Biochem 44, 1099–1107 (2018). https://doi.org/10.1007/s10695-018-0497-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-018-0497-x

Keywords

Navigation