Abstract
Experiments were conducted to identify different ratios of Bacillus sp. SJ-10 and Lactobacillus plantarum KCCM 11322 mixtures at a concentration of 1 × 108 CFU/g diet; the effects on growth and cellular and humoral immune responses and the characteristics of disease protection in olive flounder (Paralichthys olivaceus). Flounder were divided into six groups and fed control diet D-1 (without Bacillus sp. SJ-10 and L. plantarum KCCM 11322), positive control diets D-2 (Bacillus sp. SJ-10 at 1 × 108 CFU/g feed) and D-3 (L. plantarum KCCM 11322 at 1 × 108 CFU/g feed); or treatment diets D-4 (3:1 Bacillus sp. SJ-10 and L. plantarum KCCM 11322 at 0.75 + 0.25 × 108 CFU/g feed), D-5 (1:1 Bacillus sp. SJ-10 and L. plantarum KCCM 11322 at 0.50 + 0.50 × 108 CFU/g feed), or D-6 (1:3 Bacillus sp. SJ-10 and L. plantarum KCCM 11322 at 0.25 + 0.75 × 108 CFU/g feed) for 8 weeks. Group D-4 demonstrated better growth and feed utilization (P < 0.05) compared with the controls and positive controls. Similar modulation was also observed in respiratory burst for all treatments and in the expression levels of TNF-α, IL-1β, IL-6, and IL-10 in different organs in D-4. D-4 and D-5 increased respiratory burst, superoxide dismutase, lysozyme, and myeloperoxidase activities compared with the controls, and only D-4 increased microvilli length. When challenged with 1 × 108 CFU/mL Streptococcus iniae, the fish in the D-4 and D-5 groups survived up to 14 days, whereas the fish in the other groups reached 100% mortality at 11.50 days. Collectively, a ratio-specific Bacillus sp. SJ-10 and L. plantarum KCCM 11322 mixture (3:1) was associated with elevated growth, innate immunity, and streptococcosis resistance (3:1 and 1:1) compared with the control and single probiotic diets.
Similar content being viewed by others
Data Availability
Requesting to corresponding author.
References
Hasan MT, Jang WJ, Lee S, Kim KW, Lee BJ, Han HS, Bai SC, Kong IS (2018) Effect of β-glucooligosaccharides as a new prebiotic for dietary supplementation in olive flounder (Paralichthys olivaceus) aquaculture. Aquac Res 49:1310–1319. https://doi.org/10.1111/are.13588
Lee W, Ahn G, Oh JY, Kim SM, Kang N, Kim EA, Kim KN, Jeon YJ (2016) A prebiotic effect of Ecklonia cava on the growth and mortality of olive flounder infected with pathogenic bacteria. Fish Shellfish Immunol 51:313–320. https://doi.org/10.1016/j.fsi.2016.02.030
Statistics Korea (2018) Fishery production statistics and survey on current state of aquaculture. http://www.index.go.kr/potal/main/EachDtlPageDetail.do?idx_cd=2748
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 MJ, 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 (Paralichthys olivaceus). Fish Shellfish Immunol 42:177–183. https://doi.org/10.1016/j.fsi.2014.10.035
Hasan MT, Jang WJ, Lee JM, Lee BJ, Hur SW, Lim SG, Kim KW, Han HS, Kong IS (2019) Effects of immunostimulants, prebiotics, probiotics, synbiotics, and potentially immunoreactive feed additives on olive flounder (Paralichthys olivaceus) aquaculture: a review. Rev Fish Sci Aquac 27:417–437. https://doi.org/10.1080/23308249.2019.1622510
Baeck GW, Kim JH, Gomez DK, Park SC (2006) Isolation and characterization of Streptococcus sp. from diseased flounder (Paralichthys olivaceus) in Jeju Island. J Vet Sci 7:53–58. https://doi.org/10.4142/jvs.2006.7.1.53
Facklam R, Elliott J, Shewmaker L, Reingold A (2005) Identification and characterization of sporadic isolates of Streptococcus iniae isolated from humans. J Clin Microbiol 43:933–937. https://doi.org/10.1128/JCM.43.2.933-937.2005
Food and Agricultural Organization and World Health Organization (FAO/WHO) (2001) Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. A joint FAO/WHO expert consultation report. Cordoba, Argentina, 1–4 October, pp 1–34
Pérez-Sánchez T, Ruiz-Zarzuela I, de Blas I, Balcázar JL (2014) Probiotics in aquaculture: a current assessment. Rev Aquacult 6:133–146. https://doi.org/10.1111/raq.12033
Hidalgo MC, Skalli A, Abellán E, Arizcun M, Cardenete G (2006) Dietary intake of probiotics and maslinic acid in juvenile dentex (Dentex dentex L.): effects on growth performance, survival and liver proteolytic activities. Aquact Nutr 12:256–266. https://doi.org/10.1111/j.1365-2095.2006.00408.x
Li Z, Bao N, Ren T, Han Y, Jiang Z, Bai Z, Hu Y, Ding J (2019) The effect of a multi-strain probiotic on growth performance, non-specific immune response, and intestinal health of juvenile turbot, Scophthalmus maximus L. Fish Physiol Biochem 45:1393–1407. https://doi.org/10.1007/s10695-019-00635-4
Suzer C, Çoban D, Kamaci HO, Saka Ş, Firat K, Otgucuoğlu Ö, Küçüksari H (2008) Lactobacillus spp. bacteria as probiotics in gilthead sea bream (Sparus aurata, L.) larvae: effects on growth performance and digestive enzyme activities. Aquaculture 280:140–145. https://doi.org/10.1016/j.aquaculture.2008.04.020
Montalban-Arques A, De Schryver P, Bossier P, Gorkiewicz G, Mulero V, Gatlin III DM, Galindo-Villegas J (2015) Selective manipulation of the gut microbiota improves immune status in vertebrates. Front Immunol 6:p.512. https://doi.org/10.3389/fimmu.2015.00512
Cha JH, Rahimnejad S, Yang SY, Kim KW, Lee KJ (2013) Evaluations of Bacillus spp. as dietary additives on growth performance, innate immunity and disease resistance of olive flounder (Paralichthys olivaceus) against Streptococcus iniae and as water additives. Aquaculture 402:50–57. https://doi.org/10.1016/j.aquaculture.2013.03.030
Harikrishnan R, Kim MC, Kim JS, Balasundaram C, Heo MS (2011a) Probiotics and herbal mixtures enhance the growth, blood constituents, and nonspecific immune response in Paralichthys olivaceus against Streptococcus parauberis. Fish Shellfish Immunol 31:310–317. https://doi.org/10.1016/j.fsi.2011.05.020
Jang WJ, Lee JM, Hasan MT, Lee BJ, Lim SG, Kong IS (2019) Effects of probiotic supplementation of a plant-based protein diet on intestinal microbial diversity, digestive enzyme activity, intestinal structure, and immunity in olive flounder (Paralichthys olivaceus). Fish Shellfish Immunol 92:719–727. https://doi.org/10.1016/j.fsi.2019.06.056
Kim D, Beck BR, Heo SB, Kim J, Kim HD, Lee SM, Kim Y, Oh SY, Lee K, Do HK, Lee KH, Holzapfel WH, Song SK (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
Jang WJ, Lee JM, Kim YR, Hasan MT, Kong IS (2018) Complete genome sequence of Bacillus sp. SJ-10 (KCCM 90078) producing 400-kDa poly-γ-glutamic acid. Curr Microbiol 75:1378–1383. https://doi.org/10.1007/s00284-018-1533-x
Lee JM, Jang WJ, Hasan MT, Lee BJ, Kim KW, Lim SG, Han HS, Kong IS (2019) Characterization of a Bacillus sp. isolated from fermented food and its synbiotic effect with barley β-glucan as a biocontrol agent in the aquaculture industry. Appl Microbiol Biotechnol 103:1429–1439. https://doi.org/10.1007/s00253-018-9480-9
Jang WJ, Choi SY, Lee JM, Lee GH, Hasan MT, Kong IS (2019) Viability of Lactobacillus plantarum encapsulated with poly γ-glutamic acid produced by Bacillus sp. SJ-10 during freeze drying and in an in vitro gastrointestinal model. LWT-Food Sci Technol 112:10822. https://doi.org/10.1016/j.lwt.2019.05.120
Hasan MT, Jang WJ, Kim H, Lee BJ, Kim KW, Hur SW, Lim SG, Bai SC, Kong IS (2018) Synergistic effects of dietary Bacillus sp. SJ-10 plus β-glucooligosaccharides as a synbiotic on growth performance, innate immunity and streptococcosis resistance in olive flounder (Paralichthys olivaceus). Fish Shellfish Immunol 82:544–553. https://doi.org/10.1016/j.fsi.2018.09.002
Aly SM, Ahmed YAG, Ghareeb AAA, 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. https://doi.org/10.1016/j.fsi.2008.03.013
Lin HL, Shiu YL, Chiu CS, Huang SL, Liu CH (2017) Screening probiotic candidates for a mixture of probiotics to enhance the growth performance, immunity, and disease resistance of Asian seabass, Lates calcarifer (Bloch), against Aeromonas hydrophila. Fish Shellfish Immunol 60:474–482. https://doi.org/10.1016/j.fsi.2016.11.026
Thy HTT, Tri NN, Quy OM, Fotedar R, Kannika K, Unajak S, Areechon N (2017) Effects of the dietary supplementation of mixed probiotic spores of Bacillus amyloliquefaciens 54A, and Bacillus pumilus 47B on growth, innate immunity and stress responses of striped catfish (Pangasianodon hypophthalmus). Fish Shellfish Immunol 60:391–399. https://doi.org/10.1016/j.fsi.2016.11.016
Harikrishnan R, Balasundaram C, Heo MS (2010) Effect of probiotics enriched diet on Paralichthys olivaceus infected with lymphocystis disease virus (LCDV). Fish Shellfish Immunol 29:868–874. https://doi.org/10.1016/j.fsi.2010.07.031
Harikrishnan R, Kim MC, Kim JS, Balasundaram C, Heo MS (2011b) Immunomodulatory effect of probiotics enriched diets on Uronema marinum infected olive flounder. Fish Shellfish Immunol 30:964–971. https://doi.org/10.1016/j.fsi.2011.01.030
Nicholson WL, Setlow P (1990) Sporulation, germination and outgrowth. In: Harwood CR, Cutting SM (eds) Molecular biological methods for Bacillus. John Wiley and Sons, Chichester, England, pp 391–450
Park Y, Moniruzzaman M, Lee S, Hong J, Won S, Lee JM, Yun H, Kim KW, Ko D, Bai SC (2016) Comparison of the effects of dietary single and multi-probiotics on growth, non-specific immune responses and disease resistance in starry flounder, Platichthys stellatus. Fish Shellfish Immunol 59:351–357. https://doi.org/10.1016/j.fsi.2016.11.006
Hasan MT, Jang WJ, Tak JY, Lee BJ, Kim KW, Hur SW, Han HS, Kim BS, Huh MD, Kim SK, Kong IS (2018) Effects of Lactococcus lactis subsp. lactis I2 with β-glucooligosaccharides on growth, innate immunity and streptococcosis resistance in olive flounder (Paralichthys olivaceus). J Microbiol Biotechnol 28:1433–1442. https://doi.org/10.4014/jmb.1805.05011
Heo WS, Kim YR, Kim EY, Bai SC, Kong IS (2013) Effects of dietary probiotic, Lactococcus lactis subsp. lactis I2, supplementation on the growth and immune response of olive flounder (Paralichthys olivaceus). Aquaculture 376:20–24. https://doi.org/10.1016/j.aquaculture.2012.11.009
AOAC (Association of Official Analytical Chemists), (1995) Official Methods of Analysis, sixteenth. Arlington, Virginia
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. https://doi.org/10.1007/s00253-015-6702-2
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. Asian Fisheries Society, Manila, Philippines, Philippines Fish Health Section, pp 185–202
Hultmark D, Steiner H, Rasmuson T, Boman HG (1980) Insect immunity. Purification and properties of three inducible bactericidal proteins from hemolymph of immunized pupae of Hyalophora cecropia. Eur J Biochem 106:7–16. https://doi.org/10.1111/j.1432-1033.1980.tb05991.x
Quade MJ, Roth JA (1997) A rapid, direct assay to measure degranulation of bovine neutrophil primary granules. Vet Immunol Immunopathol 58:239–248. https://doi.org/10.1016/S0165-2427(97)00048-2
Wu ZQ, Jiang C, Ling F, Wang GX (2015) Effects of dietary supplementation of intestinal autochthonous bacteria on the innate immunity and disease resistance of grass carp (Ctenopharyngodon idellus). Aquaculture 438:105–114. https://doi.org/10.1016/j.aquaculture.2014.12.041
Zhang CN, Li XF, Xu WN, Zhang DD, Lu KL, Wang LN, Tian HY, Liu WB (2015) Combined effects of dietary fructooligosaccharide and Bacillus licheniformis on growth performance, body composition, intestinal enzymes activities and gut histology of triangular bream (Megalobrama terminalis). Aquacult Nutr 21:755–766. https://doi.org/10.1111/anu.12200
Hasan MT, Jang WJ, Lee BJ, Kim KW, Hur SW, Lim SG, Bai SC, Kong IS (2019) Heat-killed Bacillus sp. SJ-10 probiotic acts as a growth and humoral innate immunity response enhancer in olive flounder (Paralichthys olivaceus). Fish Shellfish Immunol 88:424–431. https://doi.org/10.1016/j.fsi.2019.03.018
Kim J, Lee KW, Jeong HS, Ansary MWR, Kim HS, Kim T, Kwon MG, Cho SH (2019) Oral administration effect of yacon, ginger and blueberry on the growth, body composition and plasma chemistry of juvenile olive flounder (Paralichthys olivaceus) and immunity test against Streptococcus iniae compared to a commercial probiotic, Lactobacillus fermentum. Aquacult Rep 15:100212. https://doi.org/10.1016/j.aqrep.2019.100212
Sukhavachana S, Poompuang S, Onming S, Luengnaruemitchai A (2019) Heritability estimates and selection response for resistance to Streptococcus agalactiae in red tilapia Oreochromis spp. Aquaculture 502:384–390. https://doi.org/10.1016/j.aquaculture.2018.12.075
Amend DF (1981) Potency testing of fish vaccines. In: Anderson DP, Hennessen W (eds) Fish biologics: serodiagnostics and vaccines. S. Karger, Basel, pp 447–454
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. https://doi.org/10.1016/j.fsi.2008.03.011
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
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
Akter MN, Hashim R, Sutriana A, Siti Azizah MN, Asaduzzaman M (2019) Effect of Lactobacillus acidophilus supplementation on growth performances, digestive enzyme activities and gut histomorphology of striped catfish (Pangasianodon hypophthalmus Sauvage, 1878) juveniles. Aquac Res 50:786–797. https://doi.org/10.1111/are.13938
Tan HY, Chen SW, Hu SY (2019) Improvements in the growth performance, immunity, disease resistance, and gut microbiota by the probiotic Rummeliibacillus stabekisii in Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol 92:265–275. https://doi.org/10.1016/j.fsi.2019.06.027
Giannenas I, Karamaligas I, Margaroni M, Pappas I, Mayer E, Encarnação P, Karagouni E (2015) Effect of dietary incorporation of a multi-strain probiotic on growth performance and health status in rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 41:119–128. https://doi.org/10.1007/s10695-014-0010-0
Xie JJ, Liu QQ, Liao S, Fang HH, Yin P, Xie SW, Tian LX, Liu YJ, Niu J (2019) Effects of dietary mixed probiotics on growth, non-specific immunity, intestinal morphology and microbiota of juvenile pacific white shrimp, Litopenaeus vannamei. Fish Shellfish Immunol 90:456–465. https://doi.org/10.1016/j.fsi.2019.04.301
Giri SS, Sukumaran V, Sen SS, Jena PK (2014) Effects of dietary supplementation of potential probiotic Bacillus subtilis VSG 1 singularly or in combination with Lactobacillus plantarum VSG3 or/and Pseudomonas aeruginosa VSG2 on the growth, immunity and disease resistance of Labeo rohita. Aquacult Nutr 20:163–171. https://doi.org/10.1111/anu.12062
Zhang C, Zhang J, Fan W, Huang M, Liu M (2019) Effects of dietary Lactobacillus delbrueckii on growth performance, body composition, digestive and absorptive capacity, and gene expression of common carp (Cyprinus carpio Huanghe var). Aquacult Nutr 25:166–175. https://doi.org/10.1111/anu.12840
Adorian TJ, Jamali H, Farsani HG, Darvishi P, Hasanpour S, Bagheri T, Roozbehfar R (2019) Effects of probiotic bacteria Bacillus on growth performance, digestive enzyme activity, and hematological parameters of Asian sea bass, Lates calcarifer (Bloch). Probiotics Antimicrob Proteins 11:248–255. https://doi.org/10.1007/s12602-018-9393-z
Seenivasan C, Radhakrishnan S, Muralisankar T, Bhavan PS (2016) Effects of probiotics on survival, growth and digestive enzymes activities in freshwater prawn Macrobrachium rosenbergii (De Man 1879). Proc Zool Soc 69:62–60. https://doi.org/10.1007/s12595-014-0123-6
Dobaño C, Moncunill G (2018) Naturally acquired immunity (NAI). In: Kremsner P, Krisna S (eds) Encyclopedia of Malaria. Springer, New York, pp 1–15
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
Reece J, Urry LA, Meyers N, Cain ML, Wasserman SA, Minorsky PV, Jackson RB, Cooke BN (2015) Campbell Biology, 10th edn. Pearson, Boston
Wang Y, Branicky R, Noë A, Hekimi S (2018) Superoxide dismutases: dual roles in controlling ROS damage and regulating ROS signaling. J Cell Biol 217:1915–1928. https://doi.org/10.1083/jcb.201708007
Standen BT, Rawling MD, Davies SJ, Castex M, Foey A, Gioacchini G, Carnevali O, Merrifield DL (2013) Probiotic Pediococcus acidilactici modulates both localised intestinal-and peripheral-immunity in tilapia (Oreochromis niloticus). Fish Shellfish Immunol 35:1097–1104. https://doi.org/10.1016/j.fsi.2013.07.018
Alejo A, Tafalla C (2011) Chemokines in teleost fish species. Dev Comp Immunol 35:1215–1222. https://doi.org/10.1016/j.dci.2011.03.011
Scheller J, Chalaris A, Schmidt-Arras D, Rose-John S (2011) The pro-and anti-inflammatory properties of the cytokine interleukin-6. BBA- Mol Cell Res 1813:878–888. https://doi.org/10.1016/j.bbamcr.2011.01.034
Akhter N, Wu B, Memon AM, Mohsin M (2015) Probiotics and prebiotics associated with aquaculture: a review. Fish Shellfish Immunol 45:733–741. https://doi.org/10.1016/j.fsi.2015.05.038
Kabat AM, Srinivasan N, Maloy KJ (2014) Modulation of immune development and function by intestinal microbiota. Trends Immunol 35:507–517. https://doi.org/10.1016/j.it.2014.07.010
Lyer SS, Cheng G (2012) Role of interleukin 10 transcriptional regulation in inflammation and autoimmune disease. Crit Rev Immunol 32:23–63. https://doi.org/10.1615/CritRevImmunol.v32.i1.30
Dawood MAO, Abu-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
Avella MA, Gioacchini G, Decamp O, Makridis P, Bracciatelli C, Carnevali O (2010) Application of multi-species of Bacillus in sea bream larviculture. Aquaculture 305:12–19. https://doi.org/10.1016/j.aquaculture.2010.03.029
Dawood MA, Koshio S, Ishikawa M, Yokoyama S, El Basuini MF, Hossain MS, Nhu TH, Dossou S, Moss AS (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
de Roos NM, Katan MB (2000) Effects of probiotic bacteria on diarrhea, lipid metabolism, and carcinogenesis: a review of papers published between 1988 and 1998. Am J Clin Nutr 71:405–411. https://doi.org/10.1093/ajcn/71.2.405
Collet B (2014) Innate immune responses of salmonid fish to viral infections. Dev Comp Immunol 43:160–173. https://doi.org/10.1016/j.dci.2013.08.017
Matur E, Eraslan E (2012) The impact of probiotics on the gastrointestinal physiology. In: Brzozowski T (ed), New advances in the basic and clinical gastroenterology, pp 51−74
Wang L, Zhou H, He R, Xu W, Mai K, He G (2016) Effects of soybean meal fermentation by Lactobacillus plantarum P8 on growth, immune responses, and intestinal morphology in juvenile turbot (Scophthalmus maximus L.). Aquaculture 464:87–94. https://doi.org/10.1016/j.aquaculture.2016.06.026
Park Y, Kim H, Won S, Hamidoghli A, Hasan MT, Kong IS, Bai SC (2019) Effects of two dietary probiotics (Bacillus subtilis or licheniformis) with two prebiotics (mannan or fructo oligosaccharide) in Japanese eel, Anguilla japonica. Aquacult Nutr 26:316–327. https://doi.org/10.1111/anu.12993
Funding
This research work was financially supported by the grant (R2021016) from the National Institute of Fisheries Science, Republic of Korea.
Author information
Authors and Affiliations
Contributions
First 2 authors contributed equally in this research.
Corresponding authors
Ethics declarations
Ethics Approval
All research activities were conducted according to “Animal Ethics Regulation-554” issued by “Pukyong National University, Busan, Republic of Korea”, which are in accordance with the guidelines for the care and use of laboratory animals described by the US National Institutes of Health.
Consent to Participate
All authors approved.
Consent for Publication
All authors approved.
Conflict of Interest
The authors declare that they have no conflicts of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Hasan, M.T., Jang, W.J., Lee, BJ. et al. Dietary Supplementation of Bacillus sp. SJ-10 and Lactobacillus plantarum KCCM 11322 Combinations Enhance Growth and Cellular and Humoral Immunity in Olive Flounder (Paralichthys olivaceus). Probiotics & Antimicro. Prot. 13, 1277–1291 (2021). https://doi.org/10.1007/s12602-021-09749-9
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12602-021-09749-9