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Dietary montmorillonite improves growth, chemical composition, antioxidant system and immune-related genes of whiteleg shrimp (Litopenaeus vannamei)

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Abstract

Montmorillonite (MMT) is an aluminosilicate clay with specific properties, such as improving growth performance and enhancing immunity. The effects of MMT supplements on performance, survival rate, body composition, haemolymph parameters, relative gene expressions, and antioxidant response of whiteleg shrimp (Litopenaeus vannamei) were investigated. Five diets with MMT supplementation were formulated at 0 (Control), 10 (MMT1), 20 (MMT2), 30 (MMT3) and 40 (MMT4) g/kg representing five treatments in replicates (15 tanks). A quadratic relation existed between the growth, feed conversion ratio, lysozyme and penaeidin3a and the MMT levels (further, MMT1 and MMT2 had significantly higher levels than other groups). Phenoloxidase, alkaline phosphatase and the expression of heat shock protein (HSP70), metallothionein and glutathione had linear relations so that MMT4 had a higher value than others (P < 0.05). Weight gain also had positive correlations with feed efficiency (correlation coefficient R: 0.76), HSP70 (R: 0.55), lysozyme (R: 0.72) and penaeidin3a (R: 0.60), while it had negative relations with daily feed intake, triglycerides and malondialdehyde. Malondialdehyde also had negative correlations with the level of MMT (R: − 0.69), weight gain (R: − 0.54), phenoloxidase (R: − 0.61), HSP70 (R: − 0.65), metallothionein (R: − 0.57) and catalase (R: 0.54) and also negative, but not significant, correlations with other measured parameters. In general, the findings of this study showed that the inclusion of MMT supplements in the diet improves the growth, antioxidant system and expression of genes related to whiteleg shrimp immunity and avoids lipid peroxidation. Most of the measured parameters suggest supplementing 20 g/kg MMT in diets of whiteleg shrimp, which is economically beneficial through improved growth and FCR.

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Data availability

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

References

  • Abele D, Zenteno-Savin T & Vazquez-Medina JP (2011) Oxidative stress in aquatic ecosystems. John Wiley & Sons

  • Aebi H (1984) Methods in enzymology. 105:121–126. Elsevier

  • Afshari F, Sotoudeh E, Mozanzadeh MT, Ghasemi A (2023) Dietary mixture of short-chain fatty acids, a phytogenic agent, and a permeabiliser improved growth, antioxidant enzymes, and immunocompetence in whiteleg shrimp juveniles (Penaeus vannamei). Aquacult Int 31:847–866

    Article  CAS  Google Scholar 

  • Ahmadi-Noorbakhsh S, Mirabzadeh Ardakani E, Sadighi J, Aldavood SJ, Farajli Abbasi M, Farzad-Mohajeri S, Ghasemi A, Sharif-Paghaleh E, Hatami Z, Nikravanfard N (2021) Guideline for the Care and Use of Laboratory Animals in Iran. Lab Anim 50:303–305

    Article  Google Scholar 

  • Amparyup P, Charoensapsri W, Tassanakajon A (2013) Prophenoloxidase system and its role in shrimp immune responses against major pathogens. Fish Shellfish Immunol 34:990–1001

    Article  CAS  PubMed  Google Scholar 

  • AOAC (2000) Official methods of analysis of the AOAC International. Vol. 18. The Association

  • Aweya JJ, Zheng Z, Zheng X, Yao D, Zhang Y (2021) The expanding repertoire of immune-related molecules with antimicrobial activity in penaeid shrimps: a review. Rev Aquac 13:1907–1937

    Article  Google Scholar 

  • Bagheri D, Moradi R, Zare M, Sotoudeh E, Hoseinifar SH, Oujifard A, Esmaeili N (2023) Does dietary sodium alginate with low molecular weight affect growth, antioxidant system, and haemolymph parameters and alleviate cadmium stress in whiteleg shrimp (Litopenaeus vannamei)? Animals 13:1805

    Article  PubMed  PubMed Central  Google Scholar 

  • Banaee M, Akhlaghi M, Soltanian S, Gholamhosseini A, Heidarieh H, Fereidouni MS (2019) Acute exposure to chlorpyrifos and glyphosate induces changes in hemolymph biochemical parameters in the crayfish, Astacus leptodactylus (Eschscholtz, 1823). Comp Biochem Physiol c: Toxicol Pharmacol 222:145–155

    CAS  PubMed  Google Scholar 

  • Bayne CJ, Gerwick L (2001) The acute phase response and innate immunity of fish. Dev Comp Immunol 25:725–743

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Kuang Y, Qu X, Guo S, Kang K, He C (2019) The effects and combinational effects of Bacillus subtilis and montmorillonite supplementation on performance, egg quality, oxidation status, and immune response in laying hens. Livest Sci 227:114–119

    Article  Google Scholar 

  • Chen M, Chen X-Q, Tian L-X, Liu Y-J, Niu J (2020) Beneficial impacts on growth, intestinal health, immune responses and ammonia resistance of pacific white shrimp (Litopenaeus vannamei) fed dietary synbiotic (mannan oligosaccharide and Bacillus licheniformis). Aquaculture Reports 17:100408

    Article  Google Scholar 

  • Duan Q, Li J, Gong L, Wu H, Zhang L (2013) Effects of graded levels of montmorillonite on performance, hematological parameters and bone mineralisation in weaned pigs. Asian Australas J Anim Sci 26:1614–1621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fao (2022) The Food and Agriculture Organization. The State of World Fisheries and Aquaculture 2020 Sustainability in action. Food and Agriculture Organization of the United Nations, Rome

    Google Scholar 

  • Fredrick WS, Ravichandran S (2012) Hemolymph proteins in marine crustaceans. Asian Pac J Trop Biomed 2:496–502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghaffarizadeh A, Sotoudeh E, Mozanzadeh MT, Sanati AM, Ghasemi A (2022) Supplementing dietary selenium nano-particles increased growth, antioxidant capacity and immune-related genes transcription in Pacific whiteleg shrimp (Penaeus vannamei) juveniles. Aquaculture Reports 25:101215

    Article  Google Scholar 

  • Golub EE, Boesze-Battaglia K (2007) The role of alkaline phosphatase in mineralisation. Curr Opin Orthop 18:444–448

    Article  Google Scholar 

  • Hernández-López J, Gollas-Galván T, Vargas-Albores F (1996) Activation of the prophenoloxidase system of the brown shrimp Penaeus californiensis Holmes. Comp Biochem Physiol c: Pharmacol Toxicol Endocrinol 113:61–66

    Google Scholar 

  • Hosseinpour Aghaei R, Abedian Kenari A, Yazdani Sadati MA, Esmaeili M (2018) The effect of time-dependent protein restriction on growth factors, nonspecific immunity, body composition, fatty acids and amino acids in the Siberian sturgeon (Acipenser baerii). Aquac Res 49:3033–3044

    Article  CAS  Google Scholar 

  • Hu C, Xu Y, Xia M, Xiong L, Xu Z (2007) Effects of Cu2+-exchanged montmorillonite on growth performance, microbial ecology and intestinal morphology of Nile tilapia (Oreochromis niloticus). Aquaculture 270:200–206

    Article  CAS  Google Scholar 

  • Hu C, Xu Y, Xia M, Xiong L, Xu Z (2008) Effects of Cu2+-exchanged montmorillonite on intestinal microflora, digestibility and digestive enzyme activities of Nile tilapia. Aquac Nutr 14:281–288

    Article  Google Scholar 

  • Hu M-L (1994) Methods in enzymology. 233 380–385. Elsevier

  • Huang H-T, Liao Z-H, Wu Y-S, Lin Y-J, Kang Y-S, Nan F-H (2022) Effects of Bidens alba and Plectranthus amboinicus dietary supplements on nonspecific immune responses, growth, and resistance to Vibrio alginolyticus in white leg shrimp (Penaeus vannamei). Aquaculture 546:737306

    Article  CAS  Google Scholar 

  • Jiao L, Zhang Q, Wu H, Wang C, Cao S, Feng J, Hu C (2018) Influences of copper/zinc-loaded montmorillonite on growth performance, mineral retention, intestinal morphology, mucosa antioxidant capacity, and cytokine contents in weaned piglets. Biol Trace Elem Res 185:356–363

    Article  CAS  PubMed  Google Scholar 

  • Karimi M, Mousavi SM, Zolgharnain H, Zakeri M (2020) Dietary montmorillonite as growth promoter and immunomodulator in rainbow trout (Oncorhynchus mykiss). Chemosphere 252:126459

    Article  CAS  PubMed  Google Scholar 

  • Licona-Jain A, Campa-Córdova Á, Luna-González A, Racotta IS, Tello M, Angulo C (2020) Dietary supplementation of marine yeast Yarrowia lipolytica modulates immune response in Litopenaeus vannamei. Fish Shellfish Immunol 105:469–476

    Article  CAS  PubMed  Google Scholar 

  • Lin C, Yan P, Lou Z, Shi X, Zhao Q, Li E (2022) Effects of histamine on the neuroendocrine-immune regulatory network in the pacific white shrimp. Litopenaeus Vannamei Aquaculture 554:738156

    Article  CAS  Google Scholar 

  • Luna-González A, Almaraz-Salas JC, Fierro-Coronado JA, Del Carmen F-M, González-Ocampo HA, Peraza-Gómez V (2012) The prebiotic inulin increases the phenoloxidase activity and reduces the prevalence of WSSV in whiteleg shrimp (Litopenaeus vannamei) cultured under laboratory conditions. Aquaculture 362:28–32

    Article  Google Scholar 

  • Matés JM, Pérez-Gómez C, De Castro IN (1999) Antioxidant enzymes and human diseases. Clin Biochem 32:595–603

    Article  PubMed  Google Scholar 

  • Ng W-K, Mong M-L, Abdul-Hamid A-A (2023) Dietary montmorillonite clay improved Penaeus vannamei survival from acute hepatopancreatic necrosis disease and modulated stomach microbiota. Anim Feed Sci Technol 297:115581

    Article  CAS  Google Scholar 

  • NRC. National Research Council, Nutrient requirements of fish and shrimp (2011) The National Academies Press. National academies press, Washington DC

    Google Scholar 

  • Palm HW, Berchtold E, Gille B, Knaus U, Wenzel LC, Baßmann B (2022) Growth and welfare of African catfish (Clarias gariepinus Burchell, 1822) under dietary supplementation with mixed-layer clay mineral montmorillonite-illite/muscovite in commercial aquaculture. Aquaculture Journal 2:227–245

    Article  Google Scholar 

  • Pourmozaffar S, Hajimoradloo A, Miandare HK (2017) Dietary effect of apple cider vinegar and propionic acid on immune related transcriptional responses and growth performance in white shrimp, Litopenaeus vannamei. Fish Shellfish Immunol 60:65–71

    Article  CAS  PubMed  Google Scholar 

  • Qu X, Chen J, He C, Chi F, Johnston S (2018) Effects of modified montmorillonite adsorbent on performance, egg quality, serum biochemistry, oxidation status, and immune response of laying hens in late production. Livest Sci 210:15–20

    Article  Google Scholar 

  • Reilly CA, Aust SD (1999) Measurement of lipid peroxidation. Current Protocols in Toxicology https://doi.org/10.1002/0471140856.tx0204s00

  • Requena JR, Fu M-X, Ahmed MU, Jenkins AJ, Lyons TJ, Thorpe SR (1996) Lipoxidation products as biomarkers of oxidative damage to proteins during lipid peroxidation reactions. Nephrol Dial Transplant 11:48–53

    Article  CAS  PubMed  Google Scholar 

  • Roberts R, Agius C, Saliba C, Bossier P, Sung Y (2010) Heat shock proteins (chaperones) in fish and shellfish and their potential role in relation to fish health: a review. J Fish Dis 33:789–801

    Article  CAS  PubMed  Google Scholar 

  • Sánchez A, Pascual C, Sánchez A, Vargas-Albores F, Le Moullac G, Rosas C (2001) Hemolymph metabolic variables and immune response in Litopenaeus setiferus adult males: the effect of acclimation. Aquaculture 198:13–28

    Article  Google Scholar 

  • Sapcharoen P, Rengpipat S (2013) Effects of the probiotic Bacillus subtilis (BP 11 and BS 11) on the growth and survival of Pacific white shrimp, Litopenaeus vannamei. Aquac Nutr 19:946–954

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Shearer KD (1994) Factors affecting the proximate composition of cultured fishes with emphasis on salmonids. Aquaculture 119:63–88

    Article  CAS  Google Scholar 

  • Shi X, Liang Y, Li Y, Zhang P, Yang Z, Liu H (2022) Dietary supplementation of montmorillonite promotes growth and intestinal health in turbot (Scophthalmus maximus). Anim Feed Sci Technol 283:115176

    Article  CAS  Google Scholar 

  • Song J, Li Li Y, Hong HuC (2013) Effects of copper-exchanged montmorillonite, as alternative to antibiotic, on diarrhea, intestinal permeability and proinflammatory cytokine of weanling pigs. Appl Clay Sci 77:52–55

    Article  ADS  Google Scholar 

  • Sotoudeh E, Esmaeili M (2022) Effects of Biotronic® Top3, a feed additive containing organic acids, cinnamaldehyde and a permeabilising complex on growth, digestive enzyme activities, immunity, antioxidant system and gene expression of barramundi (Lates calcarifer). Aquaculture Reports 24:101152

    Article  Google Scholar 

  • Tharaka K, Gunathilaka BE, Veille A, Kim M-G, Shin J, Lim H, Jeong J-B, Meallet V, Lee K-J (2020) Algae-clay powder (sea lettuce, Ulva lactuca and red algae, Solieria chordalis in exfoliated micronised montmorillonite) supplementation in a fish meal-reduced diet for olive flounder (Paralichthys olivaceus). Aquac Rep 18:100498

    Article  Google Scholar 

  • Thirumoorthy N, Kumar KM, Sundar AS, Panayappan L, Chatterjee M (2007) Metallothionein: an overview. World J Gastroenterol: WJG 13:993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang H, Wu P, Liu J, Yang S, Ruan B, Rehman S, Liu L & Zhu N (2020) The regulatory mechanism of Chryseobacterium sp. resistance mediated by montmorillonite upon cadmium stress. Chemosphere 240:124851

  • Wang Q, Zhan X, Wang B, Wang F, Zhou Y, Xu S, Li X, Tang L, Jin Q, Li W (2022) Modified montmorillonite improved growth performance of broilers by modulating intestinal microbiota and enhancing intestinal barriers, anti-inflammatory response, and antioxidative capacity. Antioxidants 11:1799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y-C, Chang P-S, Chen H-Y (2007) Tissue expressions of nine genes important to immune defence of the Pacific white shrimp Litopenaeus vannamei. Fish Shellfish Immunol 23:1161–1177

    Article  PubMed  Google Scholar 

  • Zhang X, Li M, Tao X, Yang Y, Sun P, Jin M, Zhou Q, Jiao L (2022) Effects of dietary montmorillonite supplementation on the growth performance, antioxidant capacity, intestinal barrier and microbiota composition in Marsupenaeus japonicus. Aquac 557:738330

    Article  CAS  Google Scholar 

  • Zhao H, Mao X, Yu B, He J, Zheng P, Yu J, Luo J, Wang Q, Chen D (2017) Excess of dietary montmorillonite impairs growth performance, liver function, and antioxidant capacity in starter pigs. J Anim Sci 95:2943–2951

    CAS  PubMed  Google Scholar 

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Acknowledgements

The authors express their gratitude to all individuals who provided valuable assistance in animal farming, laboratory work, and technical aspects.

Funding

This research was funded by the Persian Gulf University.

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Contributions

F.P.: statistical analysis, resources, research, investigation. E.S.: resources, research, investigation, ideas, supervision, revision. D.B.: research, laboratory works, investigation, validation, revision. A.G.: research, investigation, resources. N.E.: writing, validation, ideas, revision.

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Correspondence to Ebrahim Sotoudeh.

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According to the regulations governing animal research in Iran (Ahmadi-Noorbakhsh et al. 2021), this study strictly adheres to the ethical guidelines outlined in the Declaration of Helsinki (1975) and the Society for Neuroscience Animal Care and Use guidelines (1998). These regulations and guidelines ensure the ethical treatment and welfare of the animals involved in research.

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Pourjam, F., Sotoudeh, E., Bagheri, D. et al. Dietary montmorillonite improves growth, chemical composition, antioxidant system and immune-related genes of whiteleg shrimp (Litopenaeus vannamei). Aquacult Int (2024). https://doi.org/10.1007/s10499-024-01442-2

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