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Effect of dietary supplementation with Chlorella sorokiniana meal on the growth performance, antioxidant status, and immune response of rainbow trout (Oncorhynchus mykiss)

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Abstract

The aim of the study is to investigate whether dietary Chlorella sorokiniana supplementation could improve growth performance, antioxidant status, and immune response of Oncorhynchus mykiss. Three isonitrogenous (47%) and isolipidic (16.5%) diets supplemented with 0% (Control), 5% (5% CS), and 10% C. sorokiniana meal (10% CS) were assigned to O. mykiss (three replicates per diet, 30 fish in each replicate, initial body weight 165.24 ± 0.46 g). The results indicated that O. mykiss fed with 5% CS diet had an increased feeding rate (FR), specific growth rate (SGR), and weight gain rate (WGR) compared to the control (P < 0.05). Dietary 5% or 10% C. sorokiniana supplementation significantly increased activity levels of superoxide dismutase (SOD) in the liver and catalase (CAT) in the liver and head kidney. In addition, dietary supplementation with 10% C. sorokiniana also significantly increased activity level of glutathione peroxidase (GPX) and simultaneously decreased contents of malondialdehyde (MDA) in the liver and head kidney. Furthermore, fish fed with 5% CS or 10 CS diet demonstrated increased activity level of lysozyme (LYZ), higher content of immunoglobulin M (IgM), and upregulated transcriptional expression of tumor necrosis factor α (TNF-α), interleukin 1β (IL-1β), hepcidin (HEP), and nuclear factor kappa-B (NF-κB) in the head kidney. Based on fish growth performance, antioxidant capacity, and immune response, dietary supplementation of 5% C. sorokiniana was recommended.

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Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  • Adel M, Yeganeh S, Dadar M, Sakai M, Dawood MAO (2016) Effects of dietary Spirulina platensis on growth performance, humoral and mucosal immune responses and disease resistance in juvenile great sturgeon (Huso huso Linnaeus, 1754). Fish Shellfish Immunol 56:436–444

    Article  CAS  PubMed  Google Scholar 

  • Ahmad MT, Shariff M, Md Yusoff F, Goh YM, Banerjee S (2020) Applications of microalga Chlorella vulgaris in aquaculture. Rev Aquacult 12:328–346

    Article  Google Scholar 

  • Anderson J, Asche F, Garlock T, Chu J (2017) Aquaculture: its role in the future of food. In: World Agricultural Resources and Food Security. Emerald Publishing Limited, Bingley 159–173

  • AOAC (1995) Official methods of analysis (16th ed.). Association of Official Analytical Chemests, Arlington, VA

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Cao S, Zhang P, Zou T, Fei S, Han D, Jin J, Liu H, Yang Y, Zhu X, Xie S (2018) Replacement of fishmeal by spirulina Arthrospira platensis affects growth, immune related-gene expression in gibel carp (Carassius auratus gibelio var. CAS III), and its challenge against Aeromonas hydrophila infection. Fish Shellfish Immunol 79:265–273

    Article  CAS  PubMed  Google Scholar 

  • Chen S, Zou L, Li L, Wu T (2013) The protective effect of glycyrrhetinic acid on carbon tetrachloride-induced chronic liver fibrosis in mice via upregulation of Nrf2. PLoS ONE 8:e53662

  • Chen W, Luo L, Han D, Long F, Chi Q, Hu Q (2021) Effect of dietary supplementation with filamentous microalga Tribonema ultriculosum on growth performance, fillet quality and immunity of rainbow trout Oncorhynchus mykiss. Aquacult Nutr. https://doi.org/10.1111/anu.13264

  • Chew BP, Park JS (2004) Carotenoid action on the immune response. J Nutr 134:257S-261S

    Article  CAS  PubMed  Google Scholar 

  • Chomczynski P, Sacchi N (2006) The single-step method of RNA isolation by acid guanidinium thiocyanate–phenol–chloroform extraction: twenty-something years on. Nat Protoc 1:581

  • Cuesta A, Meseguer J, Esteban MÁ (2008) The antimicrobial peptide hepcidin exerts an important role in the innate immunity against bacteria in the bony fish gilthead seabream. Mol Immunol 45:2333–2342

    Article  CAS  PubMed  Google Scholar 

  • Dawood MAO, Koshio S, Esteban MÁ (2018) Beneficial roles of feed additives as immunostimulants in aquaculture: a review. Rev Aquacult 10:950–974

    Article  Google Scholar 

  • de-Bashan LE, Trejo A, Huss VAR, Hernandez J-P, Bashan Y (2008) Chlorella sorokiniana UTEX 2805, a heat and intense, sunlight-tolerant microalga with potential for removing ammonium from wastewater. Bioresour Technol 99:4980-4989

  • Del Rio D, Stewart AJ, Pellegrini N (2005) A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress. Nutr Metab Cardiovasc 15:316–328

    Article  Google Scholar 

  • Deng Y-P, Jiang W-D, Liu Y, Jiang J, Kuang S-Y, Tang L, Wu P, Zhang Y-A, Feng L, Zhou X-Q (2014) Differential growth performance, intestinal antioxidant status and relative expression of Nrf2 and its target genes in young grass carp (Ctenopharyngodon idella) fed with graded levels of leucine. Aquaculture 434:66–73

    Article  Google Scholar 

  • El-Habashi N, Fadl SE, Farag HF, Gad DM, Elsadany AY, El Gohary MS (2019) Effect of using Spirulina and Chlorella as feed additives for elevating immunity status of Nile tilapia experimentally infected with Aeromonas hydrophila. Aquacult Res 50:2769–2781

    Article  CAS  Google Scholar 

  • Ellis A (1990) Lysozyme assays. In: Stolen JS, Fletcher TC, Anderson DP, Roberson BS, Van Muiswinkel WB (eds) Techniques in fish immunology. SOS Publications, Fair Haven, New Jersey, pp 101–103

    Google Scholar 

  • Galal AAA, Reda RM, Abdel-Rahman Mohamed A (2018) Influences of Chlorella vulgaris dietary supplementation on growth performance, hematology, immune response and disease resistance in Oreochromis niloticus exposed to sub-lethal concentrations of penoxsulam herbicide. Fish Shellfish Immunol 77:445–456

    Article  CAS  PubMed  Google Scholar 

  • Hayden MS, Ghosh S (2011) NF-κB in immunobiology. Cell Res 21:223–244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi M, Msangi S, Batka M, Vannuccini S, Dey MM, Anderson JL (2015) Fish to 2030: the role and opportunity for aquaculture. Aquacult Econ Manag 19:282–300

  • Kumar K, Banerjee D, Das D (2014a) Carbon dioxide sequestration from industrial flue gas by Chlorella sorokiniana. Bioresour Technol 152:225–233

    Article  CAS  PubMed  Google Scholar 

  • Kumar K, Dasgupta CN, Das D (2014b) Cell growth kinetics of Chlorella sorokiniana and nutritional values of its biomass. Bioresour Technol 167:358–366

    Article  CAS  PubMed  Google Scholar 

  • Løvoll M, Fischer U, Mathisen GS, Bøgwald J, Ototake M, Dalmo RA (2007) The C3 subtypes are differentially regulated after immunostimulation in rainbow trout, but head kidney macrophages do not contribute to C3 transcription. Vet Immunol Immunopathol 117:284–295

    Article  PubMed  CAS  Google Scholar 

  • Lebron F, Vassallo R, Puri V, Limper AH (2003) Pneumocystis carinii cell wall β-glucans initiate macrophage inflammatory responses through NF-κB activation. J Biol Chem 278:25001–25008

    Article  CAS  PubMed  Google Scholar 

  • Li T, Zheng Y, Yu L, Chen S (2014) Mixotrophic cultivation of a Chlorella sorokiniana strain for enhanced biomass and lipid production. Biomass Bioenergy 66:204–213

    Article  CAS  Google Scholar 

  • Lin PY, Tsai CT, Chuang WL, Chao YH, Pan IH, Chen YK, Lin CC, Wang BY (2017) Chlorella sorokiniana induces mitochondrial-mediated apoptosis in human non-small cell lung cancer cells and inhibits xenograft tumor growth in vivo. BMC Complement Altern Med 17:88

  • Liu J, Chen F (2014) Biology and industrial applications of Chlorella: advances and prospects. In: Posten C, Feng Chen S (eds) Microalgae biotechnology. Advances in Biochemical Engineering/Biotechnology. Springer, Berlin, 1–35

  • Liu X, Steele JC, Meng XZ (2017) Usage, residue, and human health risk of antibiotics in Chinese aquaculture: a review. Environ Pollut 223:161–169

    Article  CAS  PubMed  Google Scholar 

  • Low C, Wadsworth S, Burrells C, Secombes CJ (2003) Expression of immune genes in turbot (Scophthalmus maximus) fed a nucleotide-supplemented diet. Aquaculture 221:23–40

    Article  CAS  Google Scholar 

  • Meena DK, Das P, Kumar S, Mandal SC, Prusty AK, Singh SK, Akhtar MS, Behera BK, Kumar K, Pal AK, Mukherjee SC (2013) Beta-glucan: an ideal immunostimulant in aquaculture (a review). Fish Physiol Biochem 39:431–457

    Article  CAS  PubMed  Google Scholar 

  • Mulero V, Meseguer J (1998) Functional characterisation of a macrophage-activating factor produced by leucocytes of gilthead seabream (Sparus aurata L.). Fish Shellfish Immunol 8:143–156

    Article  Google Scholar 

  • Nakagawa H, Montgomery W (2007) Algae. In: Gatlin DI, Nakagawa H, Sato M (eds) Dietary supplements for the health and quality of cultured fish. Cabi International, Cambridge, pp 133–167

    Chapter  Google Scholar 

  • Parra D, Reyes-Lopez FE, Tort L (2015) Mucosal immunity and B cells in teleosts: effect of vaccination and stress. Front Immunol 6:354–354

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res 29:e45–e45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pulz O, Gross W (2004) Valuable products from biotechnology of microalgae. Appl Microbiol Biot 65:635–648

    Article  CAS  Google Scholar 

  • Radhakrishnan S, Saravana Bhavan P, Seenivasan C, Muralisankar T (2015) Effect of dietary replacement of fishmeal with Chlorella vulgaris on growth performance, energy utilization and digestive enzymes in Macrobrachium rosenbergii postlarvae. Int J Fish Aquac 7:62–70

    Google Scholar 

  • Rauta PR, Nayak B, Das S (2012) Immune system and immune responses in fish and their role in comparative immunity study: a model for higher organisms. Immunol Lett 148:23–33

    Article  CAS  PubMed  Google Scholar 

  • Roca FJ, Mulero I, López-Muñoz A, Sepulcre MP, Renshaw SA, Meseguer J, Mulero V (2008) Evolution of the inflammatory response in vertebrates: fish TNF-α is a powerful activator of endothelial cells but hardly activates phagocytes. J Immunol 181:5071–5081

    Article  CAS  PubMed  Google Scholar 

  • Saurabh S, Sahoo PK (2008) Lysozyme: an important defence molecule of fish innate immune system. Aquacult Res 39:223–239

    Article  CAS  Google Scholar 

  • Sies H, Berndt C, Jones DP (2017) Oxidative stress. Annu Rev Biochem 86:715–748

    Article  CAS  PubMed  Google Scholar 

  • Sithranga Boopathy N, Kathiresan K (2013) Anticancer agents derived from marine algae. In: Domínguez H (ed) Functional ingredients from algae for foods and nutraceuticals. Woodhead Publishing, Cambridge, 307–337

  • Sørensen M, Gong Y, Bjarnason F, Vasanth GK, Dahle D, Huntley M, Kiron V (2017) Nannochloropsis oceania-derived defatted meal as an alternative to fishmeal in Atlantic salmon feeds. PLoS ONE 12 :e0179907

  • Spolaore P, Joannis-Cassan C, Duran E, Isambert A (2006) Commercial applications of microalgae. J Biosci Bio Eng 101:87–96

    Article  CAS  Google Scholar 

  • Sutherland AB, Meyer JL (2007) Effects of increased suspended sediment on growth rate and gill condition of two southern Appalachian minnows. Environ Biol Fishes 80:389–403

    Article  Google Scholar 

  • Teimouri M, Yeganeh S, Mianji GR, Najafi M, Mahjoub S (2019) The effect of Spirulina platensis meal on antioxidant gene expression, total antioxidant capacity, and lipid peroxidation of rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 45:977–986

    Article  CAS  PubMed  Google Scholar 

  • Tovar-Ramírez D, Mazurais D, Gatesoupe JF, Quazuguel P, Cahu CL, Zambonino-Infante JL (2010) Dietary probiotic live yeast modulates antioxidant enzyme activities and gene expression of sea bass (Dicentrarchus labrax) larvae. Aquaculture 300:142–147

    Article  CAS  Google Scholar 

  • Vallejos-Vidal E, Reyes-López F, Teles M, MacKenzie S (2016) The response of fish to immunostimulant diets. Fish Shellfish Immunol 56:34–69

    Article  CAS  PubMed  Google Scholar 

  • Vazirzadeh A, Dehghan F, Kazemeini R (2017) Changes in growth, blood immune parameters and expression of immune related genes in rainbow trout (Oncorhynchus mykiss) in response to diet supplemented with Ducrosia anethifolia essential oil. Fish Shellfish Immunol 69:164–172

    Article  CAS  PubMed  Google Scholar 

  • Vijayavel K, Anbuselvam C, Balasubramanian MP (2007) Antioxidant effect of the marine algae Chlorella vulgaris against naphthalene-induced oxidative stress in the albino rats. Mol Cell Biochem 303:39–44

    Article  CAS  PubMed  Google Scholar 

  • Wu M, Zhang H, Sun W, Li Y, Hu Q, Zhou H, Han D (2019) Metabolic plasticity of the starchless mutant of Chlorella sorokiniana and mechanisms underlying its enhanced lipid production revealed by comparative metabolomics analysis. Algal Res 42:101587

  • Zahran E, Risha E (2014) Modulatory role of dietary Chlorella vulgaris powder against arsenic-induced immunotoxicity and oxidative stress in Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol 41:654–662

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Swain T, Bøgwald J, Dalmo RA, Kumari J (2009) Bath immunostimulation of rainbow trout (Oncorhynchus mykiss) fry induces enhancement of inflammatory cytokine transcripts, while repeated bath induce no changes. Fish Shellfish Immunol 26:677–684

    Article  PubMed  CAS  Google Scholar 

  • Zhang Q, Qiu M, Xu W, Gao Z, Shao R, Qi Z (2014) Effects of dietary administration of Chlorella on the immune status of gibel carp, Carassius auratus gibelio. Ital J Anim Sci 13:3168

    Article  Google Scholar 

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Acknowledgements

We would like to thank Zhihong Ma, Tieliang Li, Guanling Xu, and Wei Xing for their help with the sample collection and technical assistance.

Funding

This work was partially supported by SDIC Biotech Investment Co., Ltd.,  the Laboratory for Marine Biology and Biotechnology, Pilot National Laboratory for Marine Science and Technology (Qingdao) (MS2019NO03), and the Doctoral Scientific Research Foundation of Henan University of Science and Technology (13480088).

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W-j C, LL, D-x H, and QH designed the experiment. W-j C, LL, F-p L, and Q-l C conducted the experiment. W-j C and QH contributed to the analysis of the data and wrote the manuscript. LL, D-x H and QH contributed to the revision.

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Correspondence to Qiang Hu.

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All procedures implemented for rainbow trout were approved by the ethics committee of the Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, Hubei, China.

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The authors declare no competing interests.

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Chen, W., Luo, L., Han, D. et al. Effect of dietary supplementation with Chlorella sorokiniana meal on the growth performance, antioxidant status, and immune response of rainbow trout (Oncorhynchus mykiss). J Appl Phycol 33, 3113–3122 (2021). https://doi.org/10.1007/s10811-021-02541-w

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  • DOI: https://doi.org/10.1007/s10811-021-02541-w

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