Abstract
We investigated whether dietary supplementation with Aurantiochytrium sp. meal, a DHA-rich source (docosahexaenoic acid, 22: 6 n-3), fed during long-term exposure to cold-suboptimal temperature (22 °C, P1), followed by short-term exposure to higher temperatures (28 °C, P2, and 33 °C, P3), would promote oxidative damage in Nile tilapia (Oreochromis niloticus). Two supplementation levels were tested: 1.0 g 100 g−1 (D1) and 4.0 g 100 g−1 (D4). A control diet, without the additive (D0, 0 g 100 g−1), and a positive control diet supplemented with cod liver oil (CLO) were also tested. The concentrations of DHA and total n-3 PUFAs in the CLO diet were similar to those found in diets D1 and D4, respectively. The parameters analyzed included hemoglobin (Hb), the antioxidant enzymes catalase, glutathione peroxidase, total glutathione, non-protein thiols, and the oxidative markers protein carbonyl and erythrocyte DNA damage. Nile tilapia did not present differences in Hb content, regardless of diet composition, but the temperature increase (P1 to P2) led to a higher Hb content. Likewise, the temperature increases promoted alterations in all antioxidant enzymes. The dietary supplementation with 1.0 g 100 g−1 Aurantiochytrium sp. meal after P1 caused minor DNA damage in Nile tilapia, demonstrating that the additive can safely be included in winter diets, despite its high DHA concentration.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and material
The data from the study will be available through the corresponding author by reasonable request.
Code availability
Not applicable.
References
AOAC (1999) Official methods of analysis of the AOAC international, 17th edn. Association of Official Analytical Chemists, Gaithersburg, MD
Abdel-Tawwab M, Ahmad MH, Khattab YAE, Shalaby AME (2010) Effect of dietary protein level, initial body weight, and their interaction on the growth, feed utilization, and physiological alterations of Nile tilapia, Oreochromis niloticus (L.). Aquaculture 298:267–274. https://doi.org/10.1016/j.aquaculture.2009.10.027
Abele D, Puntarulo S (2004) Formation ofreactive species and induction ofantioxidant defence systems in polar and temperate marine invertebrates and fish. Comp Biochem Physiol C 138:405–415. https://doi.org/10.1016/j.cbpb.2004.05.013
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. https://doi.org/10.1016/S0076-6879(84)05016-3
Austin B and Austin DA (1993) Bacterial Fish Pathogens Disease in Farmed and Wild Fish. 2nd Edn. Ellis Horwood, London, pp 376. ISBN: 0–13–059494–6
Bagnyukova TV, Lushchak OV, Lushchak SKB, VI, (2007) Oxidative stress and antioxidant defense responses by goldfish tissues to acute change of temperature from 3 to 23°C. J Therm Biol 32:227–234. https://doi.org/10.1016/j.jtherbio.2007.01.004
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. https://doi.org/10.1016/0003-2697(76)90527-3
Bhattacharyya A, Chattopadhyay R, Mitra S, Crowe SE (2014) Oxidative stress: An essential factor in the pathogenesis of gastrointestinal mucosal diseases. Physiol Rev 94:329–354. https://doi.org/10.1152/physrev.00040.2012
Bowden TJ, Thompson KD, Morgan AL, Gratacap RML, Nikoskelainen S (2007) Seasonal variation and the immune response: a fish perspective. Fish Shellfish Immun 22:695–706. https://doi.org/10.1016/j.fsi.2006.08.016
Brignol FD, Fernandes VAG, Nobrega RO, Corrêa CF, Filler K, Pettigrew J, Fracalossi DM (2018) Aurantiochytrium sp. meal as DHA source in Nile tilapia diet, part II: Body fatty acid retention and muscle fatty acid profile. Aquac Res 50:707–716. https://doi.org/10.1111/are.13906
Chandra J, Samali A, Orrenius S (2000) Triggering and modulation of apoptosis by oxidative stress. Free Radic Biol Med 29:323–333. https://doi.org/10.1016/S08915849(00)00302-6
Conover WJ, Iman RL (1981) Ranks Transformations as a Bridge Between Nonparametric and Parametric Statistics. Am Stat 35(3):124–129. https://doi.org/10.2307/268397
Corrêa CF, Nobrega RO, Block JM, Fracalossi DM (2018) Mixes of plant oils as fish oil substitutes for Nile tilapia at optimal and cold suboptimal temperature. Aquaculture 497:82–90. https://doi.org/10.1016/j.aquaculture.2018.07.034
Corrêa CF, Nobrega RO, Mattioni B, Block JM, Fracalossi DM (2017) Dietary lipid sources affect the performance of Nile tilapia at optimal and cold, suboptimal temperatures. Aquacult Nutr 23:1016–1026. https://doi.org/10.1111/anu.12469
Donaldson M, Cooke S, Patterson D, Macdonald J (2008) Cold shock and fish. J Fish Biol 73:1491–1530. https://doi.org/10.1111/j.1095-8649.2008.02061.x
Drabkin DL and Austin JH (1932) Spectrophotometric studies: I. Spectrophotometric constants for common hemoglobin derivates in human, dog, and rabbit blood. J Biol Chem 98(2):719–733.
Eissa EA, Moustafa M, Abdelaziz M, Ezzeldeen NA (2008) Yersinia ruckeri infection in cultured Nile tilapia, Oreochromis niloticus, at a semi-intensive fish farm in lower Egypt. Afr J Aquat Sci 3:283–286. https://doi.org/10.2989/AJAS.2008.33.3.13.625
Ellman G, Lysko H (1979) A precise method for the determination of whole blood and plasma sulfhydryl groups. Anal Biochem 93:98–102. https://doi.org/10.1016/s0003-2697(79)80122-0
FAO (2020) The State of World Fisheries and Aquaculture 2020 Sustainability in action. Food and Agriculture Organization of the United Nations, Rome. https://doi.org/10.4060/ca9229en
Fernandes VAG, Brignol FD, Filler K, Pettigrew J, Fracalossi DM (2018) Aurantiochytrium sp. meal as DHA source in Nile tilapia diet, part I: Growth performance and body composition. Aquac Res 50:390–399. https://doi.org/10.1111/are.13887
Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509. https://doi.org/10.1016/S0021-9258(18)64849-5
Gao YY, Xie QM, Jin L, Sun BL, Ji J, Chen F, Ma JY, Bi YZ (2012) Supplementation of xanthophylls decreased proinflammatory and increased anti-inflammatory cytokines in hens and chicks. Br J Nutr 108:1746–1755. https://doi.org/10.1017/S0007114512000025
Garrido A, Garrido F, Guerra R, Valenzuela A (1989) Ingestion of high doses of fish oil increases the susceptibility of cellular membranes to the induction ofoxidative stress. Lipids 24:833–835. https://doi.org/10.1007/BF02544593
Gęgotek A, Skrzydlewska E (2019) Biological effect of protein modifications by lipid peroxidation products. Chem Phys Lipids 221:46–52. https://doi.org/10.1016/j.chemphyslip.2019.03.011
Heise K, Puntarulo S, Nikinmaa M, Abele D, Pörtner HO (2006) Oxidative stress during stressful heat exposure and recovery in the North Sea eelpout Zoarces viviparus. L J Exp Biol 209:353–363. https://doi.org/10.1242/jeb.01977
Heise K, Puntarulo S, Pörtner HO, Abele D (2003) Production of reactive oxygen species by isolated mitochondria of the Antarctic bivalve Laternula elliptica (King and Broderip) under heat stress. Comp Biochem Physiol C 134:79–90. https://doi.org/10.1016/s1532-0456(02)00212-0
Hoeijmakers J (2001) Genome maintenance mechanisms for preventing cancer. Nat Genet 411:366–374. https://doi.org/10.1038/35077232
Huang CH, Huang MC, Hou PC (1998) Effect of dietary lipids on fatty acid composition and lipid peroxidation in sarcoplasmic reticulum of hybrid tilapia, Oreochromis niloticus×O. aureus. Comp Biochem Physiol B Biochem Mol Biol 120:331–336. https://doi.org/10.1016/S0305-0491(98)10022-6
Huang CH, Huang SL (2004) Effect of dietary vitamin E on growth, tissue lipid peroxi- dation, and liver glutathione level of juvenile hybrid tilapia, Oreochromis niloticus × O. aureus, fed oxidized oil. Aquaculture 237:381–389. https://doi.org/10.1016/j.aquaculture.2004.04.002
Ibrahim RE, El-Houseiny W, Behairy A, Abo-Elmaaty A, Al-Sagheer AA (2019) The palliative role of Eruca sativa leaves dietary supplementation against oxidative stress, immunosuppression, and growth retardation in temperature-stressed Oreochromis niloticus. J Therm Biol 84:26–35. https://doi.org/10.1016/j.jtherbio.2019.05.026
Jerônimo GT, Speck GM, Cechinel MM, Gonçalves ELT, Martins ML (2011) Seasonal variation on the ectoparasitic communities of Nile tilapia cultured in three regions in southern Brazil. Brazilian J Biol 71:365–373. https://doi.org/10.1590/S1519-69842011000300005
Joseph JD, Ackman RG (1992) Capillary column gas chromatographic method for analysis of encapsulated fish oils and fish oil ethyl esters: Collaborative study. J AOAC Int 75(3):488–506. https://doi.org/10.1093/jaoac/75.3.488
Klein RD, Borges VD, Rosa CE, Colares EP, Robaldo RB, Martinez PE, Bianchini A (2017) Effects of increasing temperature on antioxid ant defense system and oxidative stress parameters in the Antarctic fish Notothenia coriiceps and Notothenia rossii. J Therm Biol 68:110–118. https://doi.org/10.1016/j.jtherbio.2017.02.016
Levine RL, Williams JA, Stadtman ER, Shacter E (1994) Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 233:346–357. https://doi.org/10.1016/S0076-6879(94)33040-9
Liu B, Xie J, Ge XP, Xu P, Wang AM, He YJ, Zhou QL, Pan LK, Chen RL (2010) Effects of anthraquinone extract from Rheum officinale Bail on the growth performance and physiological responses of Macrobrachium rosenbergii under high temperature stress. Fish Shellfish Immunol 29:49–57. https://doi.org/10.1016/j.fsi.2010.02.018
Lu DL, Ma Q, Sun SX, Zhang H, Chen LQ, Zhang ML, Du ZY (2019) Reduced oxidative stress increases acute cold stress tolerance in zebrafish. Comp Biochem Physiol A Mol Integr Physiol 235:166–173. https://doi.org/10.1016/j.cbpa.2019.06.009
Luo SW, Cai L, Liu Y, Wang WN (2014) Functional analysis of a dietary recombinant Fatty acid binding protein 10 (FABP10) on the Epinephelus coioides in response to acute low temperature challenge Fish. Shellfish Immunol 36:475–484. https://doi.org/10.1016/j.fsi.2013.12.028
Luo S, Huang Y, Xie F, Huang X, Liu Y, Wang W, Qin Q (2015) Molecular cloning, characterization and expression analysis of PPAR gamma in the orange-spotted grouper (Epinephelus coioides) after the Vibrio alginolyticus challenge. Fish Shellfish Immunol 43:310–324. https://doi.org/10.1016/j.fsi.2015.01.003
Ma XY, Qiang J, He J, Gabriel NN, 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. https://doi.org/10.1007/s10695-015-0059-4
Malev O, Rut M, Maguire I, Tambuk A, Ferrero EA, Lorenzon S, Klobučar GRIV (2010) Genotoxic, physiological and immunological effects caused by temperature increase, air exposure or food deprivation in freshwater crayfish Astacus leptodactylus. Comp Biochem Physiol C 152:433–443. https://doi.org/10.1016/j.cbpc.2010.07.006
Miyashita T (1984) Pseudomonas fluorescens and Edwardsiella tarda Isolated from Diseased Tilapia. Fish Pathol 19:45–50. https://doi.org/10.3147/jsfp.19.45
Moldogazieva NT, Mokhosoev IM, Mel’nikova TI, (2019) Oxidative Stress and Advanced Lipoxidation and Glycation End Products (ALEs and AGEs) in Aging and Age-Related Diseases. Oxid Med Cell Longev 2019:1–14. https://doi.org/10.1155/2019/3085756
Morgan R, Finnøen MH, Jutfelt F (2018) Ctmax Is Repeatable and Doesn’t Reduce Growth in Zebrafish 2018:8–7099. https://doi.org/10.1038/s41598-018-25593-4
Muratori MCS, Martins NE, Peixoto MTD, Oliveira AL, Ribeiro LP, Costa APR, Silva MCC, Leite RC (2001) Mortalidade por" septicemia dos peixes tropicais" em tilápias criadas em consorciação com suínos. Arq Bras Med Vet Zootec 53(6):658–662. https://doi.org/10.1590/S0102-09352001000600007
Naylor RL, Hardy RW, Bureau DP, Chiu A, Elliott M, Farrell AP, Nichols PD (2009) Feeding aquaculture in an era of finite resources. Proc Natl Acad Sci 106:15103–15110. https://doi.org/10.1073/pnas.0905235106
Nobrega RO, Banze JF, Batista RO, Fracalossi DM (2020) Improving winter production of Nile tilapia: What can be done? Aquac Reports 18:100453–100467. https://doi.org/10.1016/j.aqrep.2020.100453
Nobrega RO, Batista RO, Corrêa CF, Mattioni B, Filer K, Pettigrew JE, Fracalossi DM (2019) Dietary supplementation of Aurantiochytrium sp. meal, a docosahexaenoic acid source, promotes growth of Nile tilapia at a suboptimal low temperature. Aquaculture 507:500–509. https://doi.org/10.1016/j.aquaculture.2019.04.030
Nobrega RO, Corrêa CF, Mattioni B, Fracalossi DM (2017) Dietary α-linolenic for juvenile Nile tilapia at cold suboptimal temperature. Aquaculture 471:66–71. https://doi.org/10.1016/j.aquaculture.2016.12.026
NRC (2011) Nutrient requirements of fish and shrimp. National Research Council. Washington, DC: National Academic Press.
O’Fallon JV, Busboom JR, Nelson ML, Gaskins CT (2007) A direct method for fatty acid methyl ester synthesis: Application to wet meat tissues, oils, and feedstuffs. J Animal Sci 85(6):1511–1521. https://doi.org/10.2527/jas.2006-491
Panase P, Saenphet S, Saenphet K (2018) Biochemical and physiological responses of Nile tilapia, Oreochromis niloticus, Lin subjected to cold shock of water temperature. Aquac Reports 11:17–23. https://doi.org/10.1016/j.aqrep.2018.05.005
Pandey S, Parvez S, Sayeed I, Haque R, Bin-Hafeez B, Raisuddin S (2003) Biomarkers of oxidative stress: a comparative study on river Yamuna fish Wallago attu (Bland Schn.). Scie Total Environm 309:105–115. https://doi.org/10.1016/S0048-9697(03)00006-8
Pimolrat P, Whangchai N, Chitmanat C, Promya J, Lebel L (2013) Survey of climate-related risks to tilapia pond farms in northern Thailand. Int J Geosci 4:54–59. https://doi.org/10.4236/ijg.2013.45b009
Popma TJ and Lovshin LL (1995) Worldwide Prospects for Commercial Production of Tilapia. Research and Development Series no. 41, Aurburn, Department of Fisheries and Allied Aquacultures, Auburn University, AL, USA
Qiang J, Yang H, Wang H, Kpundeh MD, Xu P (2013) Interacting effects of water temperature and dietary protein level on hematological parameters in Nile tilapia juveniles, Oreochromis niloticus (L.) and mortality under Streptococcus iniae infection. Fish Shellfish Immunol 34:8–16. https://doi.org/10.1016/j.fsi.2012.09.003
Qiu J, Wang WN, Wang LJ, Liu YF, Wang AL (2011) Oxidative stress, DNA damage and osmolality in the Pacific white shrimp, Litopenaeus vannamei exposed to acute low temperature stress. Comp Biochem Physiol C Toxicol Pharmacol 154:36–41. https://doi.org/10.1016/j.cbpc.2011.02.007
Rady AAR, Csengeri I, Matkovics B (1990) Phospholipid fatty acid composition and lipid peroxi- dation in some tissues of carp acclimation to different environmental temperature. Aquacuitura Hungarica (Szarvas) VI:161–170.
Rady AA (1993) Environmental temperature shift induced adaptive changes of carp (Cyprinus carpio L.) erythrocyte plasma membrane in vivo. Comp Biochem Physiol A Physiol 105:513–518. https://doi.org/10.1016/0300-9629(93)90427-6
Rasband WS (2018) ImageJ, U. S. National Institutes of Health, Bethesda, Maryland, USA, https://imagej.nih.gov/ij/.
Rastogi A, Clark CW, Conlin SM, Brown SE, Timme-Laragy AR (2019) Redox Biol 26:101–235. https://doi.org/10.1016/j.redox.2019.101235
Rossi A, Bacchetta C, Cazenave J (2017) Effect of thermal stress on metabolic and oxidative stress biomarkers of Hoplosternum littorale (Teleostei, Callichthyidae). Ecol Indic 79:361–370. https://doi.org/10.1016/j.ecolind.2017.04.042
Shi G-C, Dong X-H, Chen G, Tan B-P, Yang Q-H, Chi S-Y, Liu H-Y (2015) Physiological responses and HSP70 mRNA expression of GIFT strain of Nile tilapia (Oreochromis niloticus) under cold stress. Aquac Res 46:658–668. https://doi.org/10.1111/are.12212
Sies H (1997) Oxidative stress: oxidants and antioxidants. Exp Physiol 82(2):291–295. https://doi.org/10.1113/expphysiol.1997.sp004024
Singh NP, McCoy MT, Tice RR, Schneider EL (1988) A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res 175:184–191. https://doi.org/10.1016/0014-4827(88)90265-0
Sokolova IM, Lannig G (2008) Interactive effects of metal pollution and temperature on metabolism in aquatic ectotherms: implications of global climate change. Clim Res 37:181–201. https://doi.org/10.3354/cr00764
Sollid J, Nilsson GE (2006) Plasticity of respiratory structures adaptive remodeling of fish gills induced by ambient oxygen and temperature. Respir Physiol Neurobiol 154:241–251. https://doi.org/10.1016/j.resp.2006.02.006
Souza PC, Bonilla-Rodriguez GO (2007) Fish hemoglobins. Braz J Med Biol Res 4(6):769–778. https://doi.org/10.1590/S0100-879X2007000600004
Starke PE, Oliver CN, Stadtman ER (1987) Modification of hepatic proteins in rats exposed to high oxygen concentration. FASEB J 1:36–39. https://doi.org/10.1096/fasebj.1.1.2886388
Tietze F (1969) Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal Biochem 27(3):502–522. https://doi.org/10.1016/0003-2697(69)90064-5
Turchini GM, Torstensen BE, Ng WK (2009) Fish oil replacement in finfish nutrition. Rev Aquac 1:10–57. https://doi.org/10.1111/j.1753-5131.2008.01001.x
Vinagre C, Madeira D, Narciso L, Cabral HN, Diniz M (2012) Effect of temperature on oxidative stress in fish: lipid peroxidation and catalase activity in the muscle of juvenile seabass, Dicentrarchus labrax. Ecol Indic 23:274–279. https://doi.org/10.1016/j.ecolind.2012.04.009
Ways P, Hanahan DJ (1964) Characterization and quantification of red cell lipids in normal man. J Lipid Res 5:318–328. https://doi.org/10.1016/S0022-2275(20)40200-7
Weber TE, Bosworth BG (2005) Effects of 28 day exposure to cold temperature or feed restriction on growth, body composition, and expression of genes related to muscle growth and metabolism in channel catfish. Aquaculture 246:483–492. https://doi.org/10.1016/j.aquaculture.2005.02.032
Wendel A (1981) Glutathione Peroxidase. Methods Enzymol 77:325–333. https://doi.org/10.1016/S0076-6879(81)77046-0
Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 77:591–625. https://doi.org/10.1152/physrev.1997.77.3.591
Zhou J, Wang L, Xin Y, Wang WN, He WY, Wang AL, Liu Y (2010) Effect of temperature on antioxidant enzyme gene expression and stress protein response in white shrimp, Litopenaeus vannamei. J Therm Biol 35:284–289. https://doi.org/10.1016/j.jtherbio.2010.06.004
Acknowledgements
The authors would like to thank Alltech Inc. (USA) for funding this study and to the Coordination of Superior Level Staff Improvement (CAPES-Brazil) for granting scholarships to Renata O. Nobrega, Rosana O. Batista, and Bruna Mattioni, and to the National Council for Scientific and Technological Development (CNPq-Brazil) through a fellowship granted to Débora M. Fracalossi. The authors thank Nicoluzzi Rações Ltda (Penha, Santa Catarina, Brazil) and Kabsa Exportadora S.A. (Porto Alegre, Rio Grande do Sul, Brazil) for donating ingredients for the elaboration of the experimental diets. Thanks are also due to Dr. Maria do Carmo Gominho Rosa and Dr. Pitágoras Augusto Piana for assisting with the statistical analyses.
Funding
This work was funded by Alltech Inc. and by the Coordination of Superior Level Staff Improvement (CAPES-Brazil) through scholarships to the authors Renata O. Nobrega, Rosana O. Batista, and Bruna Mattioni, and by the National Council for Scientific and Technological Development (CNPq-Brazil) through a fellowship to Débora M. Fracalossi.
Author information
Authors and Affiliations
Contributions
Renata Oselame Nobrega—investigation; methodology; conceptualization; data curation; formal analysis; visualization; writing—original draft; writing—review and editing.
Alcir Luiz Dafre—supervision; methodology; conceptualization; data curation; formal analysis writing: review and editing.
Camila Fernandes Corrêa—supervision; methodology; conceptualization; data curation; writing: review and editing.
Bruna Mattioni—supervision; methodology; conceptualization; data curation; writing: review and editing.
Rosana Oliveira Batista—investigation; conceptualization; methodology; visualization.
James E. Pettigrew—conceptualization; data curation; visualization; writing—review and editing.
Débora Machado Fracalossi—supervision; funding acquisition; methodology; project administration; writing: review and editing.
Corresponding author
Ethics declarations
Ethics approval
Fish management followed the protocol n° 5665210917, approved by the Ethics Committee of Animal Use of the Federal University of Santa Catarina (CEUA, UFSC, Brazil).
Conflict of interest
The feed additive used in this study was produced and sold by Alltech Inc. (USA) for use in aquaculture diets under the tradename ALL‐G‐RICH™. We understand the issue of conflict of interest and declare: this study was funded by Alltech through a joint research alliance between Alltech and the Universidade Federal de Santa Catarina (UFSC, Brazil). James E. Pettigrew is a consultant of Alltech through a committee containing both Alltech staff and UFSC staff, where the research project was developed and approved.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Nobrega, R.O., Dafre, A.L., Corrêa, C.F. et al. Oxidative damage in Nile tilapia, Oreochromis niloticus, is mainly induced by water temperature variation rather than Aurantiochytrium sp. meal dietary supplementation. Fish Physiol Biochem 48, 85–99 (2022). https://doi.org/10.1007/s10695-021-01025-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-021-01025-5