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The Effect of Lactococcus lactis subsp. lactis PTCC 1403 on the Growth Performance, Digestive Enzymes Activity, Antioxidative Status, Immune Response, and Disease Resistance of Rainbow Trout (Oncorhynchus mykiss)

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Abstract

The effect of Lactococcus lactis subsp. lactis strain PTCC 1403 as a potential probiotic was investigated on the growth, hematobiochemical, immune responses, and resistance to Yersinia ruckeri infection in rainbow trout. A total of 240 fish were distributed into 12 fiberglass tanks representing four groups (× 3 replicates). Each tank was stocked with 20 fish (average initial weight: 11.81 ± 0.32 g) and fed L. lactis subsp. lactis PTCC 1403 at 0 (control, T0), 1 × 109 (T1), 2 × 109 (T2), and 3 × 109 (T3) CFU/g feed for 8 weeks. The results showed enhanced protein efficiency ratio and reduced feed conversion ratio in the fish-fed T2 diet. Further, fish-fed T2 and T3 diets showed a significantly higher survival rate than the control (p < 0.05). Trypsin, lipase, and protease activities were increased in fish-fed L. lactis subsp. lactis PTCC 1403 compared to the control (p < 0.05). Fish fed with a T2 diet showed significantly (p < 0.05) lower glucose content than other groups. The blood lysozyme activity and IgM showed significantly (p < 0.05) higher values in fish-fed T2 and T3 diets than in other groups. The antioxidative responses were increased in fish-fed T2 and T3 diets (p < 0.05). After 7 days post-Y. ruckeri challenge, the cumulative mortality rate showed the lowest value in fish fed with T1 and T2 diets, while the highest value was recorded in the control group. In conclusion, the results revealed beneficial effects of L. lactis subsp. lactis PTCC 1403 on the feed efficiency, immune response, and resistance to Y. ruckeri infection in rainbow trout.

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Data Availability

Data available on request due to privacy/ethical restrictions (The data that support the findings of this study are available on request from the corresponding author. The data are not publicly available due to privacy or ethical restrictions).

References

  1. Dawood MAO, El Basuini MF, Zaineldin AI, Yilmaz S, Hasan MT, Ahmadifar E et al (2021) Antiparasitic and antibacterial functionality of essential oils: an alternative approach for sustainable aquaculture. Pathogens 10:185. https://doi.org/10.3390/pathogens10020185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Mohammadian T, Nasirpour M, Tabandeh MR, Heidary AA, Ghanei-Motlagh R, Hosseini SS (2019) Administrations of autochthonous probiotics altered juvenile rainbow trout Oncorhynchus mykiss health status, growth performance and resistance to Lactococcus garvieae, an experimental infection. Fish Shellfish Immunol 86:269–279. https://doi.org/10.1016/j.fsi.2018.11.052

    Article  CAS  PubMed  Google Scholar 

  3. Kakoolaki S, Akbary P, Zorriehzahra MJ, Salehi H, Sepahdari A, Afsharnasab M et al (2016) Camellia sinensis supplemented diet enhances the innate non-specific responses, haematological parameters and growth performance in Mugil cephalus against Photobacterium damselae. Fish Shellfish Immunol 57:379–385. https://doi.org/10.1016/j.fsi.2016.08.060

    Article  CAS  PubMed  Google Scholar 

  4. Cottrell RS, Blanchard JL, Halpern BS, Metian M, Froehlich HE (2020) Global adoption of novel aquaculture feeds could substantially reduce forage fish demand by 2030. Nat Food 1:301–308. https://doi.org/10.1038/s43016-020-0078-x

    Article  Google Scholar 

  5. Akbary P, Aminikhoei Z (2018) Effect of water-soluble polysaccharide extract from the green alga Ulva rigida on growth performance, antioxidant enzyme activity, and immune stimulation of grey mullet Mugil cephalus. J Appl Phycol 30:1345–1353. https://doi.org/10.1007/s10811-017-1299-8

    Article  CAS  Google Scholar 

  6. Akbary P, Jahanbakhshi A (2018) Growth yield, survival, carcass quality, haematological, biochemical parameters and innate immune responses in the grey mullet (Mugil cephalus Linneaus, 1758) fingerling induced by Immunogen® prebiotic. J Appl Anim Res 46:10–16. https://doi.org/10.1080/09712119.2016.1251927

    Article  CAS  Google Scholar 

  7. Ringø E, Hoseinifar SH, Ghosh K, Doan HV, Beck BR, Song SK (2018) Lactic acid bacteria in finfish—an update. Front Microbiol 9:1818. https://doi.org/10.3389/fmicb.2018.01818

    Article  PubMed  PubMed Central  Google Scholar 

  8. Dawood MA, Abo-Al-Ela HG, Hasan MT (2020) Modulation of transcriptomic profile in aquatic animals: probiotics, prebiotics and synbiotics scenarios. Fish Shellfish Immunol 97:268–282. https://doi.org/10.1016/j.fsi.2019.12.054

    Article  CAS  PubMed  Google Scholar 

  9. Dawood MAO (2021) Nutritional immunity of fish intestines: important insights for sustainable aquaculture. Rev Aquacult 13:642–663. https://doi.org/10.1111/raq.12492

    Article  Google Scholar 

  10. Knipe H, Temperton B, Lange A, Bass D, Tyler CR (2021) Probiotics and competitive exclusion of pathogens in shrimp aquaculture. Rev Aquacult 13:324–352. https://doi.org/10.1111/raq.12477

    Article  Google Scholar 

  11. Zaineldin AI, Hegazi S, Koshio S, Ishikawa M, Dawood MA, Dossou S et al (2020) Singular effects of Bacillus subtilis C-3102 or Saccharomyces cerevisiae type 1 on the growth, gut morphology, immunity, and stress resistance of red sea bream (Pagrus major) Ann Anim Sci 1. https://doi.org/10.2478/aoas-2020-0075

  12. Kim D, Beck BR, Lee SM, Jeon J, Lee DW, Lee JI et al (2016) Pellet feed adsorbed with the recombinant Lactococcus lactis BFE920 expressing SiMA antigen induced strong recall vaccine effects against Streptococcus iniae infection in olive flounder (Paralichthys olivaceus). Fish Shellfish Immunol 55:374–383. https://doi.org/10.1016/j.fsi.2016.06.010

    Article  CAS  PubMed  Google Scholar 

  13. Xia Y, Lu M, Chen G, Cao J, Gao F, Wang M et al (2018) Effects of dietary Lactobacillus rhamnosus JCM1136 and Lactococcus lactis subsp. lactis JCM5805 on the growth, intestinal microbiota, morphology, immune response and disease resistance of juvenile Nile tilapia, Oreochromis niloticus. Fish Shellfish Immunol 76:368–379. https://doi.org/10.1016/j.fsi.2018.03.020

    Article  CAS  PubMed  Google Scholar 

  14. Hasan MT, Jang WJ, Tak JY, Lee BJ, Kim KW, Hur SW et al (2018) Effects of Lactococcus lactis subsp. lactis I2 with beta-glucooligosaccharides on growth, innate immunity and streptococcosis resistance in Olive flounder (Paralichthys olivaceus). Appl Microbiol Biotechnol 28:1433–1442. https://doi.org/10.4014/jmb.1805.05011

    Article  CAS  Google Scholar 

  15. Dawood MA, Koshio S, Ishikawa M, Yokoyama S, El Basuini MF, Hossain MS et al (2016) Effects of dietary supplementation of Lactobacillus rhamnosus or/and Lactococcus lactis on the growth, gut microbiota and immune responses of red sea bream, Pagrus major. Fish Shellfish Immunol 49:275–285. https://doi.org/10.1016/j.fsi.2015.12.047

    Article  CAS  PubMed  Google Scholar 

  16. Beck BR, Kim D, Jeon J, Lee S-M, Kim HK, Kim O-J et al (2015) The effects of combined dietary probiotics Lactococcus lactis BFE920 and Lactobacillus plantarum FGL0001 on innate immunity and disease resistance in olive flounder (Paralichthys olivaceus). Fish Shellfish Immunol 42:177–183. https://doi.org/10.1016/j.fsi.2014.10.035

    Article  CAS  PubMed  Google Scholar 

  17. Kim D, Beck BR, Heo S-B, Kim J, Kim HD, Lee S-M et al (2013) Lactococcus lactis BFE920 activates the innate immune system of olive flounder (Paralichthys olivaceus), resulting in protection against Streptococcus iniae infection and enhancing feed efficiency and weight gain in large-scale field studies. Fish Shellfish Immunol 35:1585–1590. https://doi.org/10.1016/j.fsi.2013.09.008

    Article  CAS  PubMed  Google Scholar 

  18. Feng J, Chang X, Zhang Y, Yan X, Zhang J, Nie G (2019) Effects of Lactococcus lactis from Cyprinus carpio L. as probiotics on growth performance, innate immune response and disease resistance against Aeromonas hydrophila. Fish Shellfish Immunol 93:73–81. https://doi.org/10.1016/j.fsi.2019.07.028

    Article  CAS  PubMed  Google Scholar 

  19. Yao J-Y, Yuan X-M, Xu Y, Yin W-L, Lin L-Y, Pan X-Y et al (2016) Live recombinant Lactococcus lactis vaccine expressing immobilization antigen (i-Ag) for protection against Ichthyophthirius multifiliis in goldfish. Fish Shellfish Immunol 58:302–308. https://doi.org/10.1016/j.fsi.2016.09.037

    Article  CAS  PubMed  Google Scholar 

  20. Dini P, Mottaghian P, Ataie Amarloie O, Farhoodi M (2012) Comparison of the antagonistic effects of Lactococcus lactis PTCC 1403 and isolated vaginal lactobacilli against uterine and udder pathogens of dairy cows. Int J Probiotics Prebiotics 74

  21. Ghasemzadeh J, Shekooh Saljughi Z, Akbary P, Hasani M (2018) Effects of dietary probiotic, Lactococcus lactis “subspecies PTCC 1403” on the growth parameters and survival rate of grey mullet (Mugil cephalus L.) against Lactococcus garvieae bacteria. J Anim Environ 10:367–374. http://www.aejournal.ir/article_87689.html?lang=en

  22. Barghaman H, Yeganeh S, Keramat Amirkolaie A (2019) Effect of probiotic Lactococcus lactis (PTCC 1403) and chitin on blood and serum biochemical parameters and intestine bacteria of common carp (Cyprinus carpio). ISFJ 28:143–156. http://isfj.ir/article-1-2258-en.html

  23. Adel M, Dawood MA, Shafiei S, Sakhaie F, Shekarabi SPH (2020) Dietary Polygonum minus extract ameliorated the growth performance, humoral immune parameters, immune-related gene expression and resistance against Yersinia ruckeri in rainbow trout (Oncorhynchus mykiss). Aquaculture 519:734738. https://doi.org/10.1016/j.aquaculture.2019.734738

    Article  CAS  Google Scholar 

  24. Andani HRR, 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 28:728–734. https://doi.org/10.1111/j.1439-0426.2012.01974.x

    Article  Google Scholar 

  25. Merrifield DL, Dimitroglou A, Bradley G, Baker RTM, Davies SJ (2010) Probiotic applications for rainbow trout (Oncorhynchus mykiss Walbaum) I. Effects on growth performance, feed utilization, intestinal microbiota and related health criteria. Aquacult Nutr 16:504–510. https://doi.org/10.1111/j.1365-2095.2009.00689.x

    Article  CAS  Google Scholar 

  26. Adel M, Yeganeh S, Dawood M, Safari R, Radhakrishnan S (2017) Effects of Pediococcus pentosaceus supplementation on growth performance, intestinal microflora and disease resistance of white shrimp, Litopenaeus vannamei. Aquacult Nutr 23:1401–1409. https://doi.org/10.1111/anu.12515

    Article  CAS  Google Scholar 

  27. Safari R, Adel M, Lazado CC, Caipang CMA, Dadar M (2016) Host-derived probiotics Enterococcus casseliflavus improves resistance against Streptococcus iniae infection in rainbow trout (Oncorhynchus mykiss) via immunomodulation. Fish Shellfish Immunol 52:198–205. https://doi.org/10.1016/j.fsi.2016.03.020

    Article  CAS  PubMed  Google Scholar 

  28. Rodriguez-Estrada U, Satoh S, Haga Y, Fushimi H, Sweetman J (2013) Effects of inactivated Enterococcus faecalis and mannan oligosaccharide and their combination on growth, immunity, and disease protection in rainbow trout. N Am J Aquac 75:416–428. https://doi.org/10.1080/15222055.2013.799620

    Article  Google Scholar 

  29. Eaton AD, Clesceri LS, Rice EW, Greenberg AE, Franson MAH (2005) Standard methods for the examination of water and wastewater.  American public health association 1015

  30. Heydarnejad MS, Purser GJ (2009) Agonistic acts as possible indicator of food anticipatory activity (FAA) in rainbow trout (Oncorhynchus mykiss). Iranian Journal of Veterinary Research, Shiraz University, Vol. 10, No. 2, Ser. No. 27. 137–145. https://www.sid.ir/en/journal/ViewPaper.aspx?id=141226

  31. Adel M, Lazado CC, Safari R, Yeganeh S, Zorriehzahra MJ (2017) Aqualase®, a yeast-based in-feed probiotic, modulates intestinal microbiota, immunity and growth of rainbow trout Oncorhynchus mykiss. Aquacult Res 48:1815–1826. https://doi.org/10.1111/are.13019

    Article  CAS  Google Scholar 

  32. Lazado CC, Caipang CMA, Kiron V (2012) Enzymes from the gut bacteria of Atlantic cod, Gadus morhua and their influence on intestinal enzyme activity. Aquacult Nutr 18:423–431. https://doi.org/10.1111/j.1365-2095.2011.00928.x

    Article  CAS  Google Scholar 

  33. Hummel BCW (1959) A modified spectrophotometric determination of chymotrypsin, trypsin, and thrombin. Can J Biochem Physiol 37:1393–1399. https://doi.org/10.1139/o59-157

    Article  CAS  PubMed  Google Scholar 

  34. Robyt J, Whelan W (1968) The α-amylases. Starch and its derivatives. Academic Press, London. Chapman & Hall, London, pp 477–497

    Google Scholar 

  35. Furné M, Hidalgo MC, López A, García-Gallego M, Morales AE, Domezain A et al (2005) Digestive enzyme activities in Adriatic sturgeon Acipenser naccarii and rainbow trout Oncorhynchus mykiss. A comparative study. Aquaculture 250:391–398. https://doi.org/10.1016/j.aquaculture.2005.05.017

    Article  CAS  Google Scholar 

  36. Saeidi asl MR, Adel M, Caipang CMA, Dawood MAO (2017) Immunological responses and disease resistance of rainbow trout (Oncorhynchus mykiss) juveniles following dietary administration of stinging nettle (Urtica dioica). Fish Shellfish Immunol 71:230–238. https://doi.org/10.1016/j.fsi.2017.10.016

    Article  CAS  Google Scholar 

  37. Blaxhall PC, Daisley KW (1973) Routine haematological methods for use with fish blood. J Fish Biol 5:771–781. https://doi.org/10.1111/j.1095-8649.1973.tb04510.x

    Article  Google Scholar 

  38. Klinger RC, Blazer VS, Echevarria CJA (1996) Effects of dietary lipid on the hematology of channel catfish, Ictalurus punctatus. Aquaculture 147:225–233. https://doi.org/10.1016/S0044-8486(96)01410-X

    Article  CAS  Google Scholar 

  39. Mohebbi A, Nematollahi A, Dorcheh EE, Asad FG (2012) Influence of dietary garlic (Allium sativum) on the antioxidative status of rainbow trout (Oncorhynchus mykiss). Aquacult Res 43:1184–1193. https://doi.org/10.1111/j.1365-2109.2011.02922.x

    Article  CAS  Google Scholar 

  40. Siwicki A, Anderson D (2000) Nonspecific defense mechanisms assay in fish: II. Potential killing activity of neutrophils and macrophages, lysozyme activity in serum and organs and total immunoglobulin level in serum. Olsztyn, Poland: FAO project GCP/INT/JPA, IFI p 105–112

  41. Ellis A, Stolen J, Fletcher T, Anderson D, Robertson B, Van Muiswinkel W (1990) Lysozyme assay in techniques in fish immunology. Technique in Fish Immunology

  42. M. Monte M, Urquhart K, Secombes CJ, Collet B, (2016) Individual monitoring of immune responses in rainbow trout after cohabitation and intraperitoneal injection challenge with Yersinia ruckeri. Fish Shellfish Immunol 55:469–478. https://doi.org/10.1016/j.fsi.2016.05.041

    Article  CAS  Google Scholar 

  43. Ahmadifar E, Dawood MA, Moghadam MS, Shahrestanaki AH, Van Doan H, Saad AH et al (2020) The effect of Pediococcus acidilactici MA 18/5M on immune responses and mRNA levels of growth, antioxidant and immune-related genes in zebrafish (Danio rerio). Aquacult Rep 17:100374. https://doi.org/10.1016/j.aqrep.2020.100374

    Article  Google Scholar 

  44. Dawood MA, Koshio SJA (2016) Recent advances in the role of probiotics and prebiotics in carp aquaculture: a review. Aquaculture 454:243–251. https://doi.org/10.1016/j.aquaculture.2015.12.033

    Article  CAS  Google Scholar 

  45. Dawood MA, Koshio S, Ishikawa M, El-Sabagh M, Esteban MA, Zaineldin AI (2016) Probiotics as an environment-friendly approach to enhance red sea bream, Pagrus major growth, immune response and oxidative status. Fish Shellfish Immunol 57:170–178. https://doi.org/10.1016/j.fsi.2016.08.038

    Article  CAS  PubMed  Google Scholar 

  46. Ringø E (2020) Probiotics in shellfish aquaculture. Aquacult Fisheries 5:1–27. https://doi.org/10.1016/j.aaf.2019.12.001

    Article  Google Scholar 

  47. Dawood MA, Magouz FI, Salem MF, Abdel-Daim HA (2019) Modulation of digestive enzyme activity, blood health, oxidative responses and growth-related gene expression in GIFT by heat-killed Lactobacillus plantarum (L-137). Aquaculture 505:127–136. https://doi.org/10.1016/j.aquaculture.2019.02.053

    Article  CAS  Google Scholar 

  48. Melo-Bolívar JF, Ruiz Pardo RY, Hume ME, Villamil Díaz LM (2021) Multistrain probiotics use in main commercially cultured freshwater fish: a systematic review of evidence. Rev Aquacult. https://doi.org/10.1111/raq.12543

    Article  Google Scholar 

  49. Paray BA, El-Basuini MF, Alagawany M, Albeshr MF, Farah MA, Dawood MAO (2021) Yucca schidigera usage for healthy aquatic animals: potential roles for sustainability. Animals 11:93. https://doi.org/10.3390/ani11010093

    Article  PubMed Central  Google Scholar 

  50. Jannathulla R, Dayal JS, Vasanthakumar D, Ambasankar K, Panigrahi A, Muralidhar M (2019) Apparent digestibility coefficients of fungal fermented plant proteins in two different penaeid shrimps—a comparative study. Aquacult Res 50:1491–1500. https://doi.org/10.1111/are.14024

    Article  CAS  Google Scholar 

  51. Dawood MA, Koshio S (2020) Application of fermentation strategy in aquafeed for sustainable aquaculture. Rev Aquacult 12:987–1002. https://doi.org/10.1111/raq.12368

    Article  Google Scholar 

  52. Waché Y, Auffray F, Gatesoupe F-J, Zambonino J, Gayet V, Labbé L et al (2006) Cross effects of the strain of dietary Saccharomyces cerevisiae and rearing conditions on the onset of intestinal microbiota and digestive enzymes in rainbow trout, Onchorhynchus mykiss, fry. Aquaculture 258:470–478. https://doi.org/10.1016/j.aquaculture.2006.04.002

    Article  Google Scholar 

  53. Dawood MA, Koshio S, El-Sabagh M, Billah MM, Zaineldin AI, Zayed MM et al (2017) Changes in the growth, humoral and mucosal immune responses following β-glucan and vitamin C administration in red sea bream, Pagrus major. Aquaculture 470:214–222. https://doi.org/10.1016/j.aquaculture.2016.12.036

    Article  CAS  Google Scholar 

  54. Dawood M, Koshio S, Ishikawa M, Yokoyama S, El Basuini M, Hossain M et al (2017) Dietary supplementation of β-glucan improves growth performance, the innate immune response and stress resistance of red sea bream, Pagrus major. Aquacult Nutr 23:148–159. https://doi.org/10.1111/anu.12376

    Article  CAS  Google Scholar 

  55. Ghiasi M, Binaii M, Naghavi A, Rostami HK, Nori H, Amerizadeh A (2018) 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. https://doi.org/10.1007/s10695-018-0497-x

    Article  CAS  PubMed  Google Scholar 

  56. Dawood MA, Koshio S, Esteban MÁ (2018) Beneficial roles of feed additives as immunostimulants in aquaculture: a review. Rev Aquacult 10:950–974. https://doi.org/10.1111/raq.12209

    Article  Google Scholar 

  57. Firouzbakhsh F, Noori F, Khalesi MK, Jani-Khalili K (2011) Effects of a probiotic, protexin, on the growth performance and hematological parameters in the Oscar (Astronotus ocellatus) fingerlings. Fish Physiol Biochem 37:833–842. https://doi.org/10.1007/s10695-011-9481-4

    Article  CAS  PubMed  Google Scholar 

  58. Cao Y, Liu H, Qin N, Ren X, Zhu B, Xia X (2020) Impact of food additives on the composition and function of gut microbiota: A review. Trends Food Sci Technol 99:295–310. https://doi.org/10.1016/j.tifs.2020.03.006

    Article  CAS  Google Scholar 

  59. Irianto A, Austin B (2002) Use of probiotics to control furunculosis in rainbow trout, Oncorhynchus mykiss (Walbaum). J Fish Dis 25:333–342. https://doi.org/10.1046/j.1365-2761.2002.00375.x

    Article  CAS  Google Scholar 

  60. Ahmed OM, Mahmoud AM, Abdel-Moneim A, Ashour MB (2012) Antidiabetic effects of hesperidin and naringin in type 2 diabetic rats. Diabetol Croat 41:53–67

    Google Scholar 

  61. Ansari BA, Kumar K (1988) Cypermethrin toxicity: effect on the carbohydrate metabolism of the Indian catfish, Heteropneustes fossilis. Sci Total Environ 72:161–166. https://doi.org/10.1016/0048-9697(88)90014-9

    Article  CAS  PubMed  Google Scholar 

  62. Lieke T, Meinelt T, Hoseinifar SH, Pan B, Straus DL, Steinberg CEW (2020) Sustainable aquaculture requires environmental-friendly treatment strategies for fish diseases. Rev Aquacult 12:943–965. https://doi.org/10.1111/raq.12365

    Article  Google Scholar 

  63. Ji L, Sun G, Li J, Wang Y, Du Y, Li X et al (2017) Effect of dietary β-glucan on growth, survival and regulation of immune processes in rainbow trout (Oncorhynchus mykiss) infected by Aeromonas salmonicida. Fish Shellfish Immunol 64:56–67. https://doi.org/10.1016/j.fsi.2017.03.015

    Article  CAS  PubMed  Google Scholar 

  64. Engstad RE, Robertsen B, Frivold E (1992) Yeast glucan induces increase in lysozyme and complement-mediated haemolytic activity in Atlantic salmon blood. Fish Shellfish Immunol 2:287–297. https://doi.org/10.1016/S1050-4648(06)80033-1

    Article  Google Scholar 

  65. Saurabh S, Sahoo P (2008) Lysozyme: an important defence molecule of fish innate immune system. Aquacult Res 39:223–239. https://doi.org/10.1111/j.1365-2109.2007.01883.x

    Article  CAS  Google Scholar 

  66. El-Boshy ME, El-Ashram AM, AbdelHamid FM, Gadalla HA (2010) Immunomodulatory effect of dietary Saccharomyces cerevisiae, β-glucan and laminaran in mercuric chloride treated Nile tilapia (Oreochromis niloticus) and experimentally infected with Aeromonas hydrophila. Fish Shellfish Immunol 28:802–808. https://doi.org/10.1016/j.fsi.2010.01.017

    Article  CAS  PubMed  Google Scholar 

  67. Gobi N, Vaseeharan B, Chen J-C, Rekha R, Vijayakumar S, Anjugam M et al (2018) Dietary supplementation of probiotic Bacillus licheniformis Dahb1 improves growth performance, mucus and serum immune parameters, antioxidant enzyme activity as well as resistance against Aeromonas hydrophila in tilapia Oreochromis mossambicus. Fish Shellfish Immunol 74:501–508. https://doi.org/10.1016/j.fsi.2017.12.066

    Article  CAS  PubMed  Google Scholar 

  68. Guardiola FA, Porcino C, Cerezuela R, Cuesta A, Faggio C, Esteban MA (2016) Impact of date palm fruits extracts and probiotic enriched diet on antioxidant status, innate immune response and immune-related gene expression of European seabass (Dicentrarchus labrax). Fish Shellfish Immunol 52:298–308. https://doi.org/10.1016/j.fsi.2016.03.152

    Article  CAS  PubMed  Google Scholar 

  69. Iswarya A, Vaseeharan B, Anjugam M, Gobi N, Divya M, Faggio C (2018) β-1, 3 glucan binding protein based selenium nanowire enhances the immune status of Cyprinus carpio and protection against Aeromonas hydrophila infection. Fish Shellfish Immunol 83:61–75. https://doi.org/10.1016/j.fsi.2018.08.057

    Article  CAS  PubMed  Google Scholar 

  70. Salinas I, Díaz-Rosales P, Cuesta A, Meseguer J, Chabrillón M, Moriñigo MÁ et al (2006) Effect of heat-inactivated fish and non-fish derived probiotics on the innate immune parameters of a teleost fish (Sparus aurata L.). Vet Immunol Immunopathol 111:279–286. https://doi.org/10.1016/j.vetimm.2006.01.020

    Article  CAS  PubMed  Google Scholar 

  71. Alexander C, Sahu NP, Pal AK, Akhtar MS (2011) Haemato-immunological and stress responses of Labeo rohita (Hamilton) fingerlings: effect of rearing temperature and dietary gelatinized carbohydrate. J Anim Physiol Anim Nutr 95:653–663. https://doi.org/10.1111/j.1439-0396.2010.01096.x

    Article  CAS  Google Scholar 

  72. Magnadottir B (2010) Immunological control of fish diseases. Mar Biotechnol 12:361–379. https://doi.org/10.1007/s10126-010-9279-x

    Article  CAS  Google Scholar 

  73. Allameh SK, Ringø E, Yusoff FM, Daud HM, Ideris A (2017) Dietary supplement of Enterococcus faecalis on digestive enzyme activities, short-chain fatty acid production, immune system response and disease resistance of Javanese carp (Puntius gonionotus, Bleeker 1850). Aquacult Nutr 23:331–338. https://doi.org/10.1111/anu.12397

    Article  CAS  Google Scholar 

  74. Sun YZ, Yang HL, Ma RL, Song K, Li JS (2012) Effect of Lactococcus lactis and Enterococcus faecium on growth performance, digestive enzymes and immune response of grouper Epinephelus coioides. Aquacult Nutr 18:281–289. https://doi.org/10.1111/j.1365-2095.2011.00894.x

    Article  CAS  Google Scholar 

  75. Ray PD, Huang B-W, Tsuji Y (2012) Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 24:981–900. https://doi.org/10.1016/j.cellsig.2012.01.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Panigrahi A, Kiron V, Kobayashi T, Puangkaew J, Satoh S, Sugita H (2004) Immune responses in rainbow trout Oncorhynchus mykiss induced by a potential probiotic bacteria Lactobacillus rhamnosus JCM 1136. Vet Immunol Immunopath 102:379–388. https://doi.org/10.1016/j.vetimm.2004.08.006

    Article  CAS  Google Scholar 

  77. Lamari F, Mahdhi A, Chakroun I, Esteban MA, Mazurais D, Amina B et al (2016) Interactions between candidate probiotics and the immune and antioxidative responses of European sea bass (Dicentrarchus labrax) larvae. J Fish Dis 39:1421–1432. https://doi.org/10.1111/jfd.12479

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors would like to thank the Sari Agricultural Sciences and Natural Resources University (SANRU), for financial support of this research under contract number 03-1394-08.

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  1. Department of Fisheries, Sari Agricultural Sciences and Natural Resources University, Sari, Iran

    Sakineh Yeganeh & Ahmad Nosratimovafagh

  2. Department of Food Hygiene and Quality Control, Faculty of Veterinary Medicine, Shahrekord University, Shahrekord, Iran

    Milad Adel

  3. Department of Animal Production, Faculty of Agriculture, Kafrelsheikh University, Kafrelsheikh, 33516, Egypt

    Mahmoud A. O. Dawood

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  1. Sakineh Yeganeh
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  2. Milad Adel
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  3. Ahmad Nosratimovafagh
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  4. Mahmoud A. O. Dawood
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Correspondence to Sakineh Yeganeh.

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Yeganeh, S., Adel, M., Nosratimovafagh, A. et al. The Effect of Lactococcus lactis subsp. lactis PTCC 1403 on the Growth Performance, Digestive Enzymes Activity, Antioxidative Status, Immune Response, and Disease Resistance of Rainbow Trout (Oncorhynchus mykiss). Probiotics & Antimicro. Prot. 13, 1723–1733 (2021). https://doi.org/10.1007/s12602-021-09787-3

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