Abstract
Bacterial infections have been associated with immune dysfunction and oxidative stress in cultured fish species while essential elements could boost immunity and exhibit antioxidant properties in fish. This study was therefore aimed at determining the effects of pre-treatment with waterborne selenium on humoral immunity and redox status of Clarias gariepinus experimentally challenged with Serratia marcescens. Juveniles C. gariepinus were pre-treated with 50 µg/L selenium for 14 days after which they were challenged with 5 × 103 CFU/mL of S. marcescens via oral gavage for 24 or 48 h. The control fish were not pre-treated with selenium and not challenged with bacteria. Thereafter, fish were sacrificed, blood collected into EDTA bottles for the determination of plasma nitric oxide levels and respiratory burst, and the liver excised for the determination of reduced glutathione, lipid peroxidation, and activities of catalase, superoxide dismutase, and glutathione peroxidase. Fish that were pre-treated with selenium prior to bacterial challenge (Sel + Bact) had decreased levels of nitric oxide and lipid peroxidation but a significant increase in the levels of reduced glutathione (at 48-h post-infection period only) compared to the fish challenged with bacteria without prior selenium pre-treatment (Bact). The respiratory burst and catalase activity decreased significantly in the Sel + Bact group especially at 48-h post-infection period while the activity of glutathione peroxidase increased significantly in the Sel + Bact group (at 24-h post-infection period only) compared to the Bact group. The results from this study showed that infection with S. marcescens is capable of disrupting the immune system and redox homeostasis in C. gariepinus, while pre-treatment with selenium has the ability to improve the physiological status of fish that were challenged with bacteria probably through its antioxidant properties.
Highlight
The pre-treatment of Clarias gariepinus to waterborne selenium for 14 days improved the redox homeostasis and innate immunity of fish that were experimentally challenged with the bacterium, Serratia marcescens.
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All data sets, on which the conclusions of the manuscript rely on, are present in the “Results” section in the manuscript.
References
Adeyemi JA (2014) Oxidative stress and antioxidant enzymes activities in the African catfish, Clarias gariepinus experimentally challenged with Escherichia coli and Vibrio fischeri. Fish Physiol Biochem 40:347–354
Adeyemi JA, Ogunlowo KO, Oyedara OO (2013) Bacterial microflora in the gut, gill and skin of African catfish, Clarias gariepinus (Burchell, 1822) collected from earthen ponds in Oke-Baale, Osogbo. Nigeria NISEB J 13:40–43
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126
Ampofo JA, Clerk G (2010) Diversity of bacteria contaminant in tissue of a fish cultured in organic waste fertilized ponds. Open Fish Sci J 3:142–146
Anderson DP, Siwicki AK (1995) Basic haematology and serology for fish health programs. In Shariff M, Arthur JR, Subasinghe RP (eds.) Diseases in Asian aquaculture ii. Fish health section. Manila: Asian Fish Soc 85–202
Araujo JM, Fortes-Silva R, Pola CC, Yamamoto FY, Gatlin DM, Gomes CL (2021) Delivery of selenium using chitosan nanoparticles: Synthesis, characterization, and antioxidant and growth effects in Nile tilapia (Orechromis niloticus). PLoS ONE 16:e0251786
Baldissera MD, Souza CF, Val AL, Baldisserotto B (2020) Involvement of purinergic signaling in the Amazon fish Pterygoplichthys pardalis subjected to handling stress: Relationship with immune response. Aquaculture 514:734481
Baya AM, Toranzo AE, Lupiani B, Santos Y, Hetrick FM (1992) Serratia marcescens: a potential pathogen for fish. J Fish Dis 15:15–26
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287
Biller-Takahashi JD, Takahashi LS, Mingatto FE, Urbinati EC (2015) The immune system is limited by oxidative stress: dietary selenium promotes optimal antioxidative status and greatest immune defense in pacu Piaractus mesopotamicus. Fish Shellfish Immunol 47:360–367
Biller-Takahashi JD, Takahashi LS, Saita MV, Gimbo RY, Urbinati EC (2013) Leukocytes respiratory burst activity as indicator of innate immunity of pacu Piaractus mesopotamicus. Braz J Biol 73:425–429
Biller-Takahashi JD, Urbinati EC (2014) Fish immunology. The modification and manipulation of the innate immune system: Brazilian studies. An Acad Bras Cienc 86:1483–1495
Bradford M (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
Cai J, Quagrainie K, Hishamunda N (2017) Social and economic performance of tilapia farming in Africa. FAO Fisheries and Aquaculture Circular (C1130)
Campos-Perez JJ, Ward M, Grabowski PS, Ellis AE, Secombes CJ (2000) The gills are an important site of iNOS expression in rainbow trout Oncorhynchus mykiss after challenge with the Gram-positive pathogen Renibacterium salmoninarum. Immunology 99:153–161
Cazcarro I, López-Morales CA, Duchin F (2019) The global economic costs of substituting dietary protein from fish with meat, grains and legumes, and dairy. J Ind Ecol 23:1159–1171
Chan X, Chang CY, Hong K, Tee KK, Yin W, Chan K (2013) Insights of biosurfactant producing Serratia marcescens strain W2.3 isolated from diseased tilapia fish: a draft genome analysis. Gut Pathog 5:29. https://doi.org/10.1186/1757-4749-5-29
Chen H, Li J, Yan L, Cao J, Li D, Huang G, Shi W, Dong W, Zha J, Ying G, Zhong H, Wang Z, Huang Y, Luo Y, Xie L (2020) Subchronic effects of dietary selenium yeast and selenite on growth performance and the immune and antioxidant systems in Nile tilapia Oreochromis niloticus. Fish Shellfish Immunol 97:283–293
Day BJ (2009) Catalase and glutathione peroxidase mimics. Biochem Pharmacol 77:285–296
de Faria CFP, Martinez CBD, Takahashi LS, de Mello MMM, Martins TP, Urbinati EC (2021) Modulation of the innate immune response, antioxidant system and oxidative stress during acute and chronic stress in pacu (Piaractus mesopotamicus). Fish Physiol Biochem 47:895–905
Dharmaratnam A, Kumar R, Basheer VS, Sood N, Swaminathan TR, Jena JL (2017) Isolation and characterization of virulent Serratia marcescens associated with a disease outbreak in farmed ornamental fish, Poecilia reticulata in Kerala, India. Indian J Fish 64:71–79
Durigon EG, Kunz DF, Peixoto NC, Uczay J, Lazzari R (2019) Diet selenium improves the antioxidant defense system of juveniles Nile tilapia (Oreochromis niloticus L.). Braz J Biol 79:527–532
Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–77
El-Shebly AA (2006) Evaluation of growth performance, production and nutritive value of the African catfish, Clarias gariepinus cultured in earthen ponds. Egypt Aquat Biol Fish 10:55–67
Esterbauer H, Cheeseman KH (1990) Determination of aldehydic lipid peroxidation products: malonaldehyde and 4-hydroxynoneal. Methods Enzymol 186:407–421
FAO (2016) The state of world fisheries and aquaculture: contributing to food security and nutrition for all. FAO, Rome, p 200
FAO (2018) The state of world fisheries and aquaculture: meeting the sustainable development goals. http://www.fao.org/3/i9540en/i9540en.pdf. Accessed Sept 2021
Gopalakrishnan S, Chen F, Thilagam H, Qiao K, Xu W, Wang K (2011) Modulation and interaction of immune-associated parameters with antioxidant in the immunocytes of crab Scylla paramamosain challenged with lipopolysaccharides. Evid-Based Complementary Altern Med 2011:824962. https://doi.org/10.1155/2011/824962
Guevara-Guzman R, Emson PC, Kendrick KM (1994) Modulation of in vivo striatal transmitter release by nitric oxide and cyclic GMP. J Neurochem 62:807–810
Hafeman DG, Sunde RA, Hoekstra WG (1974) Effect of dietary selenium on erythrocyte and liver glutathione peroxidase in the rat. J Nutr 104:580–587
Hoseinifar SH, Yousefi S, Van Doan H, Ashouri G, Gioacchini G, Maradonna F, Carnevali O (2021) Oxidative stress and antioxidant defense in fish: the implications of probiotic, prebiotic, and synbiotics. Rev Fish Sci Aquac 29:198–217
Hsu PC, Guo YL (2002) Antioxidant nutrients and lead toxicity. Toxicology 180:33–44
Jayawardena R, Sooriyaarachchi P, Chourdakis M, Jeewandra C, Ranasinghe P (2020) Enhancing immunity in viral infections, with special emphasis on COVID-19: a review. Diabetes Metab Syndr 14:367–382
Kotob MH, Menanteau-Ledouble S, Kumar G, Abdelzaher M, El-Matbouli M (2016) The impact of co-infections on fish: a review. Vet Res 47:98. https://doi.org/10.1186/s13567-016-0383-4
Li X, Liu H, Li D, Lei H, Wei X, Schlenk D, Mu J, Chen H, Yan B, Xie L (2021) Dietary seleno-l-methionine causes alterations in neurotransmitters, ultrastructure of the brain, and behaviors in Zebrafish (Danio rerio). Environ Sci Technol 55:11894–11905
Pacitti D, Wang T, Page MM, Martin SA, Sweetman J, Feldmann J, Secombes CJ (2013) Characterization of cytosolic glutathione peroxidase and phospholipid-hydroperoxide glutathione peroxidase genes in rainbow trout (Oncorhynchus mykiss) and their modulation by in vitro selenium exposure. Aquat Toxicol 130–131:97–111
Pathak ND, Lal B (2010) Seasonality in expression and distribution of nitric oxide synthase isoforms in the testis of the catfish, Clarias batrachus: role of nitric oxide in testosterone production. Comp Biochem Physiol C 151:286–293
Pecora F, Persico F, Argentiero A, Neglia C, Esposito S (2020) The role of micronutrients in support of the immune response against viral infections. Nutrients 12:3198. https://doi.org/10.3390/nu12103198
Raida MK, Buchmann K (2009) Innate immune response in rainbow trout (Oncorhynchus mykiss) against primary and secondary infections with Yersinia ruckeri O1. Dev Comp Immunol 33:35–45
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
Rodríguez I, Novoa B, Figueras A (2008) Immune response of zebrafish (Danio rerio) against a newly isolated bacterial pathogen Aeromonas hydrophila. Fish Shellfish Immunol 25:239–249
Roy D, Pal S, Ray SD, Homechaudhuri S (2019) Evaluating oxidative stress in Labeo rohita, infected asymptomatically with native and invasive Aeromonads using biochemical indices. Proc Natl Acad Sci India Sect B Biol Sci 89:973–978
Sarkar B, Bhattacharjee S, Daware A, Tribedi P, Krishnani KK, Minhas PS (2015) Selenium nanoparticles for stress-resilient fish and livestock. Nanoscale Res Lett 10:371. https://doi.org/10.1186/s11671-015-1073-2
Souza CDF, Baldissera MD, Verdi CM, Santos RCV, Da Rocha MIU, Veiga MLD, Silva AS, Baldisserotto B (2019) Oxidative stress and antioxidant responses in Nile tilapia Oreochromis niloticus experimentally infected by Providencia rettgeri. Microb Pathog 131:164–169
Wang C, Lovell RT, Klesius PH (1997) Response to Edwardsiella ictaluri challenge by channel catfish fed organic and inorganic sources of selenium. J Aquat Anim Health 9:172–179
Xie L, Wu X, Chen H, Dong W, Cazan AM, Klerks PL (2016) A low level of dietary selenium has both beneficial and toxic effects and is protective against Cd-toxicity in the least killifish Heterandria formosa. Chemosphere 161:358–364
Zhao H, Luo Y, Wu Z, Zhou Y, Guo D, Wang H, Chen X (2019) Hepatic lipid metabolism and oxidative stress responses of grass carp (Ctenopharyngodon idella) fed diets of two different lipid levels against Aeromonas hydrophila infection. Aquaculture 509:149–158
Acknowledgements
The authors are grateful to Samuel Dorcas, Okhamafe Benedicta, and Kolawole Oluwaseun for the help with fish handling.
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JAA and COA were involved in the design of the experiment. JAA, GAO, and OSB were involved in data acquisition and analyses. JAA, GAO, and OSB were involved in writing the draft of the manuscript. JAA and COA were involved in writing the final draft of the manuscript.
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Adeyemi, J.A., Ogunwole, G.A., Bamidele, O.S. et al. Effects of pre-treatment with waterborne selenium on redox homeostasis and humoral innate immune parameters in African catfish, Clarias gariepinus (Burchell, 1822), experimentally challenged with Serratia marcescens. Fish Physiol Biochem 48, 409–418 (2022). https://doi.org/10.1007/s10695-022-01059-3
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DOI: https://doi.org/10.1007/s10695-022-01059-3