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Antioxidative and immunoprotective potential of Chlorella vulgaris dietary supplementation against chlorpyrifos-induced toxicity in Nile tilapia

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Abstract

This study highlighted the effects of chronic chlorpyrifos (CPF) exposure on Nile tilapia (Oreochromis niloticus) and the benefits of using dietary Chlorella vulgaris (Ch) to ameliorate CPF-induced toxicity. Genes encoding antioxidant enzymes and stress-responsive proteins in the liver as well as cytokine expression in the spleen and head kidney were evaluated in O. niloticus fed with a basal diet or diets containing 1, 2, and 3% of supplementary Ch against 15 mg/L CPF at 4 and 8 weeks. CPF-exposed groups displayed a notable induction in the hepatic expression of heat shock protein 70/hsp70, glutathione peroxidase/GPx, and glutathione synthase/GSS, while glutathione reductase/GSR was markedly decreased. The mRNA levels of interleukin 1β/IL-1β, TNF-α, transforming growth factor β1/TGFβ1, and interleukin 8/ IL-8 in the spleen and head kidney increased significantly after CPF exposure. Interestingly, Ch supplementation, particularly at levels 2 and 3%, was able to modulate the stress and immune-related genes of Nile tilapia sub-chronically exposed to CPF. These outcomes provide valuable insights regarding the toxic impact of chronic exposure to CPF in fish at the molecular level and a better understanding of the Ch dietary vital roles. Besides, our findings encourage adequate monitoring of pesticide levels owing to its impacts on fish health and human as a final consumer.

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References

  • Abdelazim AM, Saadeldin IM, Swelum AA-A, Afifi MM, Alkaladi A (2018) Oxidative stress in the muscles of the fish Nile tilapia caused by zinc oxide nanoparticles and its modulation by vitamins C and E. Oxidative Med Cell Longev 2018:1–9

    Google Scholar 

  • Abdel-Halim K, Salama A, El-Khateeb E, Bakry N (2006) Organophosphorus pollutants (OPP) in aquatic environment at Damietta governorate, Egypt: implications for monitoring and biomarker responses. Chemosphere 63:1491–1498

    CAS  PubMed  Google Scholar 

  • Abhilash P, Singh N (2009) Pesticide use and application: an Indian scenario. J Hazard Mater 165:1–12

    CAS  PubMed  Google Scholar 

  • Abu-Srea H, Risha E, Zahran E, Abdalla O (2018) (2018) Protective effects of Chlorella vulgaris dietary supplementation on growth performance, hematological and biochemical parameters in Nile tilapia (Oreochromis niloticus) exposed to chlorpyrifos. Ann Vet Anim Sci 5:1–12

  • Austin B (1998) The effects of pollution on fish health. J Appl Microbiol 85:234S–242S

    PubMed  Google Scholar 

  • Bengwayan PT, Laygo JC, Pacio AE, Poyaoan JLZ, Rebugio JF, Yuson ALL (2010) A comparative study on the antioxidant property of Chlorella (Chlorella sp.) tablet and glutathione tablet. E-Int Sci Res J 2:25–35

    Google Scholar 

  • Buono S, Langellotti AL, Martello A, Rinna F, Fogliano V (2014) Functional ingredients from microalgae. Food Funct 5:1669–1685

    CAS  PubMed  Google Scholar 

  • Caxico Vieira CAS, Vieira JS, Bastos MS, Zancanela V, Barbosa LT, Gasparino E, Del Vesco AP (2018) Expression of genes related to antioxidant activity in Nile tilapia kept under salinity stress and fed diets containing different levels of vitamin C. J Toxicol Environ Health A 81:20–30

    CAS  PubMed  Google Scholar 

  • Cerezuela R, Guardiola FA, Meseguer J, Esteban MA (2012) Enrichment of gilthead seabream (Sparus aurata L.) diet with microalgae: effects on the immune system. Fish Physiol Biochem 38:1729–1739

    CAS  PubMed  Google Scholar 

  • Chen D, Zhang Z, Yao H, Cao Y, Xing H, Xu S (2014) Pro-and anti-inflammatory cytokine expression in immune organs of the common carp exposed to atrazine and chlorpyrifos. Pestic Biochem Physiol 114:8–15

    CAS  PubMed  Google Scholar 

  • Cheng D, Wan Z, Zhang X, Li J, Li H, Wang C (2017) Dietary Chlorella vulgaris ameliorates altered immunomodulatory functions in cyclophosphamide-induced immunosuppressive mice. Nutrients 9:708

    PubMed Central  Google Scholar 

  • Chou N-T, Cheng C-F, Wu H-C, Lai C-P, Lin L-T, Pan I, Ko C-H (2012) Chlorella sorokiniana-induced activation and maturation of human monocyte-derived dendritic cells through NF-κB and PI3K/MAPK pathways. Evid Based Complement Alternat Med 2012:1–12

    Google Scholar 

  • Chu W-L (2012) Biotechnological applications of microalgae. J IeJSME 6:S24–S37

    Google Scholar 

  • Dang W, Hu Y-h, Zhang M, Sun L (2010) Identification and molecular analysis of a stress-inducible Hsp70 from Sciaenops ocellatus. Fish Shellfish Immunol 29:600–607

    CAS  PubMed  Google Scholar 

  • Díaz-Resendiz KJG, Toledo-Ibarra GA, Girón-Pérez MI (2015) Modulation of immune response by organophosphorus pesticides: fishes as a potential model in immunotoxicology. J Immunol Res 2015:1–10

    Google Scholar 

  • Eder KJ, Clifford MA, Hedrick RP, Köhler H-R, Werner I (2008) Expression of immune-regulatory genes in juvenile Chinook salmon following exposure to pesticides and infectious hematopoietic necrosis virus (IHNV). Fish Shellfish Immunol 25:508–516

    CAS  PubMed  Google Scholar 

  • Eder KJ, Leutenegger CM, Köhler H-R, Werner I (2009) Effects of neurotoxic insecticides on heat-shock proteins and cytokine transcription in Chinook salmon (Oncorhynchus tshawytscha). Ecotoxicol Environ Saf 72:182–190

    CAS  PubMed  Google Scholar 

  • El-Sayed A-FM (2017) Tilapia Co-culture in Egypt. Tilapia in Intensive Co-culture 1, 211

  • Galal AA, Reda RM, Mohamed AA-R (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

    CAS  PubMed  Google Scholar 

  • Goel A, Dani V, Dhawan D (2005) Protective effects of zinc on lipid peroxidation, antioxidant enzymes and hepatic histoarchitecture in chlorpyrifos-induced toxicity. Chem Biol Interact 156:131–140

    CAS  PubMed  Google Scholar 

  • Hasan MR (2010) On-farm feeding and feed management in aquaculture. J FAO Aquac Newsl 48

  • Ismail M (2004) Phytoplankton and heavy metal contamination in the marine environment. In: Phang SM, Brown M, eds. Biomonitoring in tropical coastal ecosystems, Kuala Lumpur: University of Malaya Maritime Research Centre (UMMrec)

  • Jaffer NS, Rabee AM, Al-Chalabi SM (2017) Biochemical and hematological parameters and histological alterations in fish Cyprinus carpio L. as biomarkers for water pollution with chlorpyrifos. Hum Ecol Risk Assess 23:605–616

    CAS  Google Scholar 

  • Jin Y, Liu Z, Peng T, Fu Z (2015) The toxicity of chlorpyrifos on the early life stage of zebrafish: a survey on the endpoints at development, locomotor behavior, oxidative stress and immunotoxicity. Fish Shellfish Immunol 43:405–414

    CAS  PubMed  Google Scholar 

  • Joseph B, Raj SJ (2011) Impact of pesticide toxicity on selected biomarkers in fishes. Int J Zool Res 7:212–222

    CAS  Google Scholar 

  • Khalil SR, Reda RM, Awad A (2017) Efficacy of Spirulina platensis diet supplements on disease resistance and immune-related gene expression in Cyprinus carpio L. exposed to herbicide atrazine. Fish Shellfish Immunol 67:119–128

    CAS  PubMed  Google Scholar 

  • Kumar H, Kawai T, Akira S (2011) Pathogen recognition by the innate immune system. Int Rev Immunol 30:16–34

    CAS  PubMed  Google Scholar 

  • Kumar M, Jeon J, Choi J, Kim S-R (2018) Rapid and efficient genetic transformation of the green microalga Chlorella vulgaris. J Appl Phycol 30:1735–1745

    CAS  Google Scholar 

  • Kurade MB, Kim JR, Govindwar SP, Jeon B-H (2016) Insights into microalgae mediated biodegradation of diazinon by Chlorella vulgaris: microalgal tolerance to xenobiotic pollutants and metabolism. J Algal Res 20:126–134

    Google Scholar 

  • Li X, Liu L, Zhang Y, Fang Q, Li Y, Li Y (2013) Toxic effects of chlorpyrifos on lysozyme activities, the contents of complement C3 and IgM, and IgM and complement C3 expressions in common carp (Cyprinus carpio L.). Chemosphere 93:428–433

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Nguyen TTT, Nguyen HT, Wang P-C, Chen S-C (2017) Identification and expression analysis of two pro-inflammatory cytokines, TNF-α and IL-8, in cobia (Rachycentron canadum L.) in response to Streptococcus dysgalactiae infection. Fish Shellfish Immunol 67:159–171

    CAS  PubMed  Google Scholar 

  • NRC (2011) Nutrient requirements of fish and shrimp. National academies press

  • Oruç EÖ (2010) Oxidative stress, steroid hormone concentrations and acetylcholinesterase activity in Oreochromis niloticus exposed to chlorpyrifos. Pestic Biochem Physiol 96:160–166

    Google Scholar 

  • Oruc E (2012) Oxidative stress responses and recovery patterns in the liver of Oreochromis niloticus exposed to chlorpyrifos-ethyl. Bull Environ Contam Toxicol 88:678–684

    CAS  PubMed  Google Scholar 

  • Oruc EO, Sevgiler Y, Uner N (2004) Tissue-specific oxidative stress responses in fish exposed to 2, 4-D and azinphosmethyl. Comp Biochem Physiol C Toxicol Pharmacol 137:43–51

    PubMed  Google Scholar 

  • Panahi Y, Darvishi B, Jowzi N, Beiraghdar F, Sahebkar A (2016) Chlorella vulgaris: a multifunctional dietary supplement with diverse medicinal properties. Curr Pharm Des 22:164–173

    PubMed  Google Scholar 

  • Polinski M, Bridle A, Nowak B (2013) Temperature-induced transcription of inflammatory mediators and the influence of Hsp70 following LPS stimulation of southern bluefin tuna peripheral blood leukocytes and kidney homogenates. Fish Shellfish Immunol 34:1147–1157

    CAS  PubMed  Google Scholar 

  • Priyadarshani I, Rath B (2012) Commercial and industrial applications of micro algae–a review. J Algal Biomass Util 3:89–100

    Google Scholar 

  • Racke KD (1993) Environmental fate of chlorpyrifos, Rev. Environ. Contam. Toxicol. Springer, pp. 1-150

  • Radhakrishnan S, Bhavan PS, Seenivasan C, Shanthi R, Muralisankar T (2014) Replacement of fishmeal with Spirulina platensis, Chlorella vulgaris and Azolla pinnata on non-enzymatic and enzymatic antioxidant activities of Macrobrachium rosenbergii. J Basic Appl Zool 67:25–33

    CAS  Google Scholar 

  • Rahimnejad S, Lee SM, Park HG, Choi J (2017) Effects of dietary inclusion of Chlorella vulgaris on growth, blood biochemical parameters, and antioxidant enzyme activity in olive flounder, Paralichthys olivaceus. J World Aquacult Soc 48:103–112

    CAS  Google Scholar 

  • Reyes-Becerril M, López-Medina T, Ascencio-Valle F, Esteban MÁ (2011) Immune response of gilthead seabream (Sparus aurata) following experimental infection with Aeromonas hydrophila. Fish Shellfish Immunol 31:564–570

    CAS  PubMed  Google Scholar 

  • Ruiz-Marin A, Mendoza-Espinosa LG, Stephenson T (2010) Growth and nutrient removal in free and immobilized green algae in batch and semi-continuous cultures treating real wastewater. J Bioresour Technol 101:58–64

    CAS  Google Scholar 

  • Said TO (2007) Determination of persistent organic pollutants in sediment and fish of the western coast of Alexandria, Egypt. Chem Ecol 23:289–302

    CAS  Google Scholar 

  • Sandahl JF, Baldwin DH, Jenkins JJ, Scholz NL (2005) Comparative thresholds for acetylcholinesterase inhibition and behavioral impairment in coho salmon exposed to chlorpyrifos. Environ Toxicol Chem 24:136–145

    CAS  PubMed  Google Scholar 

  • Sharbidre AA, Metkari V, Patode P (2011) Effect of methyl parathion and chlorpyrifos on certain biomarkers in various tissues of guppy fish, Poecilia reticulata. Pestic Biochem Physiol 101:132–141

    CAS  Google Scholar 

  • Sigamani S, Ramamurthy D, Natarajan H (2016) A review on potential biotechnological applications of microalgae. J Appl Pharm Sci 6:179–184

    CAS  Google Scholar 

  • Soliman NF, Yacout DM (2016) Aquaculture in Egypt: status, constraints and potentials. Aquac Int 24:1201–1227

    Google Scholar 

  • Srikanth K, Pereira E, Duarte A, Ahmad I (2013) Glutathione and its dependent enzymes’ modulatory responses to toxic metals and metalloids in fish—a review. Environ Sci Pollut Res 20:2133–2149

    CAS  Google Scholar 

  • Tkachenko H, Kurhaluk N, Grudniewska J (2014) Oxidative stress biomarkers in different tissues of rainbow trout (Oncorhynchus mykiss) exposed to disinfectant-CIP formulated with peracetic acid and hydrogen peroxide. Arch Pol Fish 22:207–219

    CAS  Google Scholar 

  • U.S.EPA (2000) Reregistration eligibility science for chlorpyrifos: fate and environmental risk assessment chapter. United States Environmental Protection Agency. Office of Prevention Pesticides and Toxic Substances, Washington, DC

    Google Scholar 

  • Varasteh S, Braber S, Akbari P, Garssen J, Fink-Gremmels J (2015) Differences in susceptibility to heat stress along the chicken intestine and the protective effects of galacto-oligosaccharides. PLoS One 10:e0138975

    PubMed  PubMed Central  Google Scholar 

  • Venero JA, Davis DA, Rouse DB (2007) Variable feed allowance with constant protein input for the pacific white shrimp Litopenaeus vannamei reared under semi-intensive conditions in tanks and ponds. J Aquac 269:490–503

    CAS  Google Scholar 

  • Wang T, Gorgoglione B, Maehr T, Holland JW, Vecino JLG, Wadsworth S, Secombes CJ (2011a) Fish suppressors of cytokine signaling (SOCS): gene discovery, modulation of expression and function. J Signal Transduct 2011:1–20

    Google Scholar 

  • Wang X, Xing H, Li X, Xu S, Wang X (2011b) Effects of atrazine and chlorpyrifos on the mRNA levels of IL-1 and IFN-γ2b in immune organs of common carp. Fish Shellfish Immunol 31:126–133

    CAS  PubMed  Google Scholar 

  • Woo S, Yum S, Kim D-W, Park H-S (2009) Transcripts level responses in a marine medaka (Oryzias javanicus) exposed to organophosphorus pesticide. Comp Biochem Physiol C Toxicol Pharmacol 149:427–432

    PubMed  Google Scholar 

  • Woo S, Won H, Lee A, Yum S (2012) Oxidative stress and gene expression in diverse tissues of Oryzias javanicus exposed to 17β-estradiol. Mol Cell Toxicol 8:263–269

    CAS  Google Scholar 

  • Xing H, Li S, Wang X, Gao X, Xu S, Wang X (2013) Effects of atrazine and chlorpyrifos on the mRNA levels of HSP70 and HSC70 in the liver, brain, kidney and gill of common carp (Cyprinus carpio L.). Chemosphere 90:910–916

    CAS  PubMed  Google Scholar 

  • Xing H, Wang Z, Wu H, Zhao X, Liu T, Li S, Xu S (2015) Assessment of pesticide residues and gene expression in common carp exposed to atrazine and chlorpyrifos: health risk assessments. Ecotoxicol Environ Saf 113:491–498

    CAS  PubMed  Google Scholar 

  • Xiong J-Q, Kurade MB, Abou-Shanab RAI, Ji M-K, Choi J, Kim JO, Jeon B-H (2016) Biodegradation of carbamazepine using freshwater microalgae Chlamydomonas mexicana and Scenedesmus obliquus and the determination of its metabolic fate. Bioresour Technol 205:183–190

    CAS  PubMed  Google Scholar 

  • Xu W, Jilong L, Houjuan X, Shiwen X (2011) Review of toxicology of atrazine and chlorpyrifos on fish. J Northeast Agric Univ (English edition) 18:88–92

    Google Scholar 

  • Yilmaz S (2019) Effects of dietary blackberry syrup supplement on growth performance, antioxidant, and immunological responses, and resistance of Nile tilapia, Oreochromis niloticus to Plesiomonas shigelloides. J Fish Shellfish Immunol 84:1125–1133

    CAS  Google Scholar 

  • Yonar ME, Yonar SM, Ural MŞ, Silici S, Düşükcan M (2012) Protective role of propolis in chlorpyrifos-induced changes in the haematological parameters and the oxidative/antioxidative status of Cyprinus carpio carpio. Food Chem Toxicol 50:2703–2708

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Zahran E, Risha E, Awadin W, Palić D (2018) Acute exposure to chlorpyrifos induces reversible changes in health parameters of Nile tilapia (Oreochromis niloticus). Aquat Toxicol 197:47–59

    CAS  PubMed  Google Scholar 

  • Zahran E, Awadin W, Risha E, Khaled AA, Wang T (2019) Dietary supplementation of Chlorella vulgaris ameliorates chronic sodium arsenite toxicity in Nile tilapia Oreochromis niloticus as revealed by histopathological, biochemical and immune gene expression analysis. Fish Sci 85:199–215

    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

    Google Scholar 

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Acknowledgments

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors. The study was supported in kind by Mansoura University Faculty of Veterinary Medicine and Head of the Clinical Division of Fish Medicine, Dept. for Farm Animals and Vet. Public Health, University of Veterinary Medicine, Vienna. The authors are very grateful to Prof. Dr. Ikuo Hirono and Prof. Dr. Hidehiro Kondo, Laboratory of genome science, Tokyo University of Marine Science and Technology Japan, for providing qPCR reagents and Kits for this study.

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Zahran, E., Elbahnaswy, S., Risha, E. et al. Antioxidative and immunoprotective potential of Chlorella vulgaris dietary supplementation against chlorpyrifos-induced toxicity in Nile tilapia. Fish Physiol Biochem 46, 1549–1560 (2020). https://doi.org/10.1007/s10695-020-00814-8

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