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Moringa oleifera alleviated oxidative stress, physiological and molecular disruption induced by acute thermal stress in grass carp, Ctenopharyngodon idella

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Abstract

The present study was designed to investigate the protective effect of dietary Moringa oleifera leaf meal (MLM) supplementation against high temperature-induced stress in grass carp (Ctenopharyngodon idella). A total of 180 apparent healthy juvenile grass carp (15.48 g ± 0.054) were divided into three groups in triplicate (20 fish in each replicate). Fish were fed with diets containing 0, 1, and 5% MLM for 60 days and then subjected to a high-temperature challenge for 48 h (32–33 °C). The results revealed that feeding fish with 1 and 5% MLM resulted in a significant increase in weight gain and specific growth rate compared to the control. In addition, feed conversion ratio was significantly reduced in groups fed with MLM. No significant difference was reported in the serum cortisol level among different experimental groups before heat stress while serum glucose level significantly decreased in fish fed with 5% MLM. Serum alanine transaminase, aspartate transaminase, and alkaline phosphatase significantly decreased in fish fed with 1 and 5% MLM before and after heat stress. Hepatic lipid peroxidation significantly decreased in fish fed with MLM for 60 days. A non-significant increase in hepatic reduced glutathione level was reported in fish fed with 1 and 5% MLM before heat stress. Catalase and superoxide dismutase activities increased significantly in the liver of fish fed with 5% MLM. No significant change was observed in the expression profile of heat shock protein (hsp) 70 and 90 before heat stress. Meanwhile, after heat stress, up to a fivefold increase was recorded in mRNA level of hsp 70 and fourfold increase in the expression level of hsp 90 in the liver of the control fish which were not fed with MLM-supplemented diets. Fish fed with 1 and 5% MLM showed a significant decrease in the expression of hsp 70 and a non-significant decrease in the expression of hsp 90. Results of the present study suggest that supplementing the diet of grass carp with 5% MLM could improve growth and physiological performance and provide resistance against high temperature-induced stress.

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The data presented in this study are available on request from the corresponding author.

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References

  • Basu N, Todgham A, Ackerman P, Bibeau M, Nakano K, Schulte P, Iwama GK (2002) Heat shock protein genes and their functional significance in fish. Gene 295:173–183

    Article  CAS  Google Scholar 

  • Beutler E, Duron O, Kelly BM (1963) An improved method for the detection of blood glutathione. J Lab Clin Med 61:882–888

    CAS  Google Scholar 

  • Brand MD (2010) The sites and topology of mitochondrial superoxide production. Exp Gerontol 45:466–472

    Article  CAS  Google Scholar 

  • Burtis CA, Ashwood ER (1994) Tietz textbook of clinical chemistry. American Association for Clinical Chemistry, USA

    Google Scholar 

  • Cao S, Mo P, Xiao Y, Chen Y, Shi Y, Hu Y, Tang J, Qu F, Luo M, Ai X (2021) Dietary supplementation with fermented plant meal enhances growth, antioxidant capacity and expression of TOR signaling pathway genes in gibel carp (Carassius auratus gibelio var. CAS V). Aquacult Rep 19:100559

    Google Scholar 

  • Carrasco GA, Van de Kar LD (2003) Neuroendocrine pharmacology of stress. Eur J Pharmacol 463:235–272

    Article  CAS  Google Scholar 

  • Dawood MA, Eweedah NM, El-Sharawy ME, Awad SS, Van Doan H, Paray BA (2020) Dietary white button mushroom improved the growth, immunity, antioxidative status and resistance against heat stress in Nile tilapia (Oreochromis niloticus). Aquaculture 523:735229

    Article  CAS  Google Scholar 

  • Dawood MA, Noreldin AE, Sewilam H (2022) Blood biochemical variables, antioxidative status, and histological features of intestinal, gill, and liver tissues of African catfish (Clarias gariepinus) exposed to high salinity and high-temperature stress. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-022-19702-0,1-13

    Article  Google Scholar 

  • Faheem M, Khaliq S, Mustafa N, Rani S, Lone KP (2020) Dietary Moringa oleifera leaf meal induce growth, innate immunity and cytokine expression in grass carp, Ctenopharyngodon idella. Aquacult Nutr 26:1164–1172

    Article  CAS  Google Scholar 

  • Faheem M, Zahid Z, Ferreira NG (2021) Toxicity assessment of dibutyl phthalate in grass carp: an integrated biomarker approach. Pak Vet J 41:365–371

    CAS  Google Scholar 

  • Ferreira PMP, Farias DF, Oliveira JTdA, Carvalho AdFU (2008) Moringa oleifera: bioactive compounds and nutritional potential. Rev Nutr 21:431–437

    Article  CAS  Google Scholar 

  • García-Beltrán JM, Mansour AT, Alsaqufi AS, Ali HM, Esteban MÁ (2020) Effects of aqueous and ethanolic leaf extracts from drumstick tree (Moringa oleifera) on gilthead seabream (Sparus aurata L.) leucocytes, and their cytotoxic, antitumor, bactericidal and antioxidant activities. Fish Shellfish Immunol 106:44–55

    Article  Google Scholar 

  • Gbadamosi OK, Fasakin AE, Adebayo OT (2016) Hepatoprotective and stress-reducing effects of dietary Moringa oleifera extract against Aeromonas hydrophila infections and transportation-induced stress in Nile tilapia, Oreochromis niloticus (Linnaeus 1757) fingerlings. Int J Environ Agri Res 2:121–128

    Google Scholar 

  • Gopalakrishnan L, Doriya K, Kumar DS (2016) Moringa oleifera: a review on nutritive importance and its medicinal application. Food Sci Hum Wellness 5:49–56

    Article  Google Scholar 

  • Heise K, Puntarulo S, Nikinmaa M, Abele D, Pörtner H-O (2006) Oxidative stress during stressful heat exposure and recovery in the North Sea eelpout Zoarces viviparus L. J Exp Biol 209:353–363

    Article  CAS  Google Scholar 

  • Henry RJ (1964) Clinical chemistry: principles and techniques. Harper and Row, New York

    Google Scholar 

  • Herrera M, Mancera JM, Costas B (2019) The use of dietary additives in fish stress mitigation: comparative endocrine and physiological responses. Front Endocrinol (lausanne) 10:447

    Article  Google Scholar 

  • Hisam EEA, Rofiee MS, Khalid A, Jalaluddin AF, Yusof MIM, Idris MH, Ramli S, James RJ, Yoeng WJ, Kek TL (2018) Combined extract of Moringa oleifera and Centella asiatica modulates oxidative stress and senescence in hydrogen peroxide-induced human dermal fibroblasts. Turk J Biol 42:33–44

    Article  Google Scholar 

  • Hoseini SM, Gupta SK, Yousefi M, Kulikov EV, Drukovsky SG, Petrov AK, Mirghaed AT, Hoseinifar SH, Van Doan H (2022) Mitigation of transportation stress in common carp, Cyprinus carpio, by dietary administration of turmeric. Aquaculture 546:737380

    Article  CAS  Google Scholar 

  • Kaur M, Atif AM, Rehman H, Raisuddin S (2005) Heat stress-induced alterations of antioxidants in the freshwater fish Channa punctata Bloch. J Fish Biol 67:1653–1665

    Article  CAS  Google Scholar 

  • Kausar R, Salim M (2006) Effect of water temperature on the growth performance and feed conversion ratio of Labeo rohita. Pak Vet J 26:105–108

    Google Scholar 

  • Khalil F, Korni FM (2017) Evaluation of Moringa oleifera leaves and their aqueous extract in improving growth, immunity and mitigating effect of stress on common carp (Cyprinus carpio) fingerlings. Aquat Sci Eng 32:170–177

  • Khan MS, Qureshi NA, Jabeen F, Asghar MS, Shakeel M, Fakhar-e-Alam M (2017) Eco-friendly synthesis of silver nanoparticles through economical methods and assessment of toxicity through oxidative stress analysis in the Labeo rohita. Biol Trace Elem Res 176:416–428

    Article  CAS  Google Scholar 

  • Latif M, Faheem M, Asmatullal (2020) Study of oxidative stress and histo-biochemical biomarkers of diethyl phthalate induced toxicity in a cultureable fish, Labeo rohita. Pak Vet J 40(2):202–208

  • Leggatt R, Brauner C, Schulte P, Iwama G (2007) Effects of acclimation and incubation temperature on the glutathione antioxidant system in killifish and RTH-149 cells. Comp Biochem Physiol Part A Mol Integr Physiol 146:317–326

    Article  CAS  Google Scholar 

  • Liu F, Qu YK, Wang A-M, Yu Y-B, Yang W-P, Lv F, Nie Q (2019) Effects of carotenoids on the growth performance, biochemical parameters, immune responses and disease resistance of yellow catfish (Pelteobagrus fulvidraco) under high-temperature stress. Aquaculture 503:293–303

    Article  CAS  Google Scholar 

  • Lu Y, Wu Z, Song Z, Xiao P, Liu Y, Zhang P, You F (2016) Insight into the heat resistance of fish via blood: effects of heat stress on metabolism, oxidative stress and antioxidant response of olive flounder Paralichthys olivaceus and turbot Scophthalmus maximus. Fish Shellfish Immunol 58:125–135

    Article  CAS  Google Scholar 

  • Luck H (1974) Catalase In Method of Enzymatic Analysis, Bergmayer, M.V., Ed. Verlag Chemic/Academic Press: New York, USA, p. 885

  • Ma X, Qiang J, He J, Gabriel N, Xu P (2015) Changes in the physiological parameters, fatty acid metabolism, and SCD activity and expression in juvenile GIFT tilapia (Oreochromis niloticus) reared at three different temperatures. Fish Physiol Biochem 41:937–950

    Article  CAS  Google Scholar 

  • Mansour AT-E, Goda AA, Omar EA, Khalil HS, Esteban MÁ (2017) Dietary supplementation of organic selenium improves growth, survival, antioxidant and immune status of meagre, Argyrosomus regius, juveniles. Fish Shellfish Immunol 68:516–524

    Article  CAS  Google Scholar 

  • Mansour AT, Espinosa C, García-Beltrán JM, Miao L, Ceballos Francisco DC, Alsaqufi AS, Esteban M (2020a) Dietary supplementation of drumstick tree, Moringa oleifera, improves mucosal immune response in skin and gills of seabream, Sparus aurata, and attenuates the effect of hydrogen peroxide exposure. Fish Physiol Biochem 46:981–996

    Article  CAS  Google Scholar 

  • Mansour AT, El-Feky MM, El-Beltagi HS, Sallam AE (2020b) Synergism of dietary co-supplementation with lutein and bile salts improved the growth performance, carotenoid content, antioxidant capacity, lipid metabolism, and lipase activity of the marbled spinefoot rabbitfish Siganus Rivulatus. Animals 10:1643

    Article  Google Scholar 

  • Mansour AT, Fayed WM, Elkhayat BK, Omar EA, Zaki MA, Nour A-AM, Morshedy SA (2021) Extract dietary supplementation affects growth performance, hematological and physiological status of European seabass. Ann Anim Sci 21:1043–1060

    Article  CAS  Google Scholar 

  • Misra H, Fridovich I (1972) The role of superoxide anion in the autooxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247:3170–3175

    Article  CAS  Google Scholar 

  • Murray R, Kaplan A (1984) Aspartate aminotransferase; CV Mosby Company pp. 1105–1108

  • Pandit NP, Bhandari RK, Kobayashi Y, Nakamura M (2015) High temperature-induced sterility in the female Nile tilapia, Oreochromis niloticus. Gen Comp Endocrinol 213:110–117

    Article  CAS  Google Scholar 

  • Pérez-Gálvez A, Viera I, Roca M (2020) Carotenoids and Chlorophylls as Antioxidants. Antioxidants 9:505

    Article  Google Scholar 

  • Qiang J, Bao WJ, Tao FY, He J, Li XH, Xu P, Sun LY (2017) The expression profiles of miRNA–mRNA of early response in genetically improved farmed tilapia (Oreochromis niloticus) liver by acute heat stress. Sci Rep 7:8705

    Article  Google Scholar 

  • Rufchaei R, Nedaei S, Hoseinifar SH, Hassanpour S, Golshan M, Sayad Bourani M (2021) Improved growth performance, serum and mucosal immunity, haematology and antioxidant capacity in pikeperch (Sander lucioperca) using dietary water hyacinth (Eichhornia crassipes) leaf powder. Aquacult Res 52:2194–2204

    Article  CAS  Google Scholar 

  • Sallam AE, Mansour AT, Alsaqufi AS, Salem MES, El-Feky MM (2020) Growth performance, anti-oxidative status, innate immunity, and ammonia stress resistance of Siganus rivulatus fed diet supplemented with zinc and zinc nanoparticles. Aquacult Rep 18:100410

    Google Scholar 

  • Schreck CB (1996) Immunomodulation: endogenous factors. In The Fish Immune System, Organism, Pathogen and Environment, Iwama G, Nakanishi T. Eds. Academic Press: San Diego, 1996; pp. 311–337

  • Sung YY, MacRae TH, Sorgeloos P, Bossier P (2011) Stress response for disease control in aquaculture. Rev Aquacult 3:120–137

    Article  Google Scholar 

  • Teixeira CP, Barros MM, Pezzato LE, Fernandes J, Ademir C, Koch JFA, Padovani CR (2012) Growth performance of Nile tilapia, Oreochromis niloticus, fed diets containing levels of pyridoxine and haematological response under heat stress. Aquacult Res 43:1081–1088

    Article  CAS  Google Scholar 

  • Ullahkhan S, Shahab S, Fani MI, Wahid A, Hassan M, Khan A (2021) Climate and weather condition of Balochistan province, Pakistan. Int J Econ Environ Geol 12:65–71

    Google Scholar 

  • Vergara-Jimenez M, Almatrafi MM, Fernandez ML (2017) Bioactive components in Moringa oleifera leaves protect against chronic disease. Antioxidants 6:91

    Article  Google Scholar 

  • Wen H, Feng L, Jiang W, Liu Y, Jiang J, Li S, Tang L, Zhang Y, Kuang S, Zhou X (2014) Dietary tryptophan modulates intestinal immune response, barrier function, antioxidant status and gene expression of TOR and Nrf2 in young grass carp (Ctenopharyngodon idella). Fish Shellfish Immunol 40:275–287

    Article  CAS  Google Scholar 

  • Wenger C, Kaplan A, Rubaltelli F, Hammerman C (1984) Alkaline phosphatase. Clin Chem. The C.V. Mosby Co. St Louis. Toronto. Princeton, pp 1094–1098

  • Young AJ, Lowe GL (2018) Carotenoids-Antioxidant Properties. Antioxidant 7:28

    Article  Google Scholar 

  • Yousefi M, Ghafarifarsani H, Hoseinifar SH, Rashidian G, Van Doan H (2021) Effects of dietary marjoram, Origanum majorana extract on growth performance, hematological, antioxidant, humoral and mucosal immune responses, and resistance of common carp, Cyprinus carpio against Aeromonas hydrophila. Fish Shellfish Immunol 108:127–133

    Article  CAS  Google Scholar 

  • Zhang C-N, Tian H-Y, Li X-F, Zhu J, Cai D-S, Xu C, Wang F, Zhang D-D, Liu W-B (2014) The effects of fructooligosaccharide on the immune response, antioxidant capability and HSP70 and HSP90 expressions in blunt snout bream (Megalobrama amblycephala Yih) under high heat stress. Aquaculture 433:458–466

    Article  CAS  Google Scholar 

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Conceptualization, MF and SK; methodology, MF; validation, ATM; formal analysis, MF, ATM; resources, SK; visualization, ATM; writing—original draft preparation, MF, RZA; writing—review and editing, ATM. All the authors reviewed and approved the final manuscript.

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Correspondence to Mehwish Faheem.

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The study was conducted in accordance with the Declaration of Helsinki and approved by the Departmental Board of Studies of Government College University (Zool-7–932/21).

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Faheem, M., Khaliq, S., Abbas, R.Z. et al. Moringa oleifera alleviated oxidative stress, physiological and molecular disruption induced by acute thermal stress in grass carp, Ctenopharyngodon idella. Fish Physiol Biochem 48, 1463–1473 (2022). https://doi.org/10.1007/s10695-022-01147-4

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