Abstract
The original objective was to explore the potential benefiting effects of three prebiotics in hybrid grouper (Epinephelus lanceolatus♂ × Epinephelus fuscoguttatus♀). Therefore, three experimental diets (basal diet + 1% fructooligosaccharide, Diet F; basal diet + 1% inulin, Diet I; basal diet + 0.3% mannan-oligosaccharide, Diet M) and one basal diet (Diet C) were prepared and a feeding trial was conducted. However, at the end of the fourth week into the feeding experiment, a water-leaking accident occurred and fishes of all groups went through an unexpected air exposure event. Surprisingly, different prebiotic-supplemented groups showed significantly different air exposure tolerance: the mortality of M group was significantly lower (P ≤ 0.05) than all the other groups. Examination of antioxidant, non-specific immunity, and stress parameters revealed that comparing to control group, M group showed significantly increased catalase (CAT), acid phosphatase (ACP), and alkaline phosphatase (AKP) activities, decreased superoxide dismutase (SOD) activity, and similar cortisol level (P ≤ 0.05). Real-time PCR experiment revealed that M group significantly increased the expression of CAT, glutathione peroxidase (GPx), and manganese superoxide dismutase (MnSOD) genes in head kidney (P ≤ 0.05). Overall, M exhibited the best anti-air exposure/antioxidative stress effects among the three prebiotics and could be considered a promising feed additive to relieve air exposure/oxidative stress in hybrid grouper culture.
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References
Abu-Elala NM, Younis NA, AbuBakr HO, Ragaa NM, Borges LL, Bonato MA (2018) Efficacy of dietary yeast cell wall supplementation on the nutrition and immune response of Nile tilapia. Egypt J Aquat Res 44:333–341. https://doi.org/10.1016/j.ejar.2018.11.001
Álvarez CA, Jerez-Cepa I, Cárcamo CB, Toledo P, Flores H, Brokordt K (2020) Growth performance, physiological responses to hypoxia and flesh quality of Chilean croaker (Cilus gilberti) stocked at different densities. Aquaculture 525:735–316. https://doi.org/10.1016/j.aquaculture.2020.735316
Bakke-McKellep AM, Penn MH, Salas PM, Refstie S, Sperstad S, Landsverk T, Ringø E, Krogdahl Å (2007) Effects of dietary soyabean meal, inulin and oxytetracycline on intestinal microbiota and epithelial cell stress, apoptosis and proliferation in the teleost Atlantic salmon (Salmo salar L.). Br J Nutr 97:699–713. https://doi.org/10.1017/S0007114507381397
Brauner CJ (1999) The effect of diet and short duration hyperoxia exposure on seawater transfer in coho salmon smolts (Oncorhynchus kisutch). Aquaculture 177:257–265. https://doi.org/10.1016/S0044-8486(99)00089-7
Carbone D, Faggio C (2016) Importance of prebiotics in aquaculture as immunostimulants. Effects on immune system of Sparus aurata and Dicentrarchus labrax. Fish Shellfish Immunol 54:172–178. https://doi.org/10.1016/j.fsi.2016.04.011
Cheng CH, Yang FF, Ling RZ, Liao SA, Miao YT, Ye CX, Wang AL (2015) Effects of ammonia exposure on apoptosis, oxidative stress and immune response in pufferfish (Takifugu obscurus). Aquat Toxicol 164:61–71. https://doi.org/10.1016/j.aquatox.2015.04.004
Dimitroglou A, Merrifield DL, Moate R, Davies SJ, Spring P, Sweetman J, Bradley G (2009) Dietary mannan oligosaccharide supplementation modulates intestinal microbial ecology and improves gut morphology of rainbow trout, Oncorhynchus mykiss (Walbaum)1. J Anim Sci 87:3226–3234. https://doi.org/10.2527/jas.2008-1428
Dong C, Wang J (2013) Immunostimulatory effects of dietary fructooligosaccharides on red swamp crayfish, Procambarus clarkii (Girard). Aquac Res 44:1416–1424. https://doi.org/10.1111/j.1365-2109.2012.03146.x
Ellis RP, Parry H, Spicer JI, Hutchinson TH, Pipe RK, Widdicombe S (2011) Immunological function in marine invertebrates: responses to environmental perturbation. Fish Shellfish Immunol 30:1209–1222. https://doi.org/10.1016/j.fsi.2011.03.017
Gibson GR, Roberfroid MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125:1401–1412. https://doi.org/10.1093/jn/125.6.1401
Grisdale-Helland B, Helland SJ, Gatlin DM (2008) The effects of dietary supplementation with mannanoligosaccharide, fructooligosaccharide or galactooligosaccharide on the growth and feed utilization of Atlantic salmon (Salmo salar). Aquaculture 283:163–167. https://doi.org/10.1016/j.aquaculture.2008.07.012
Hahor W, Thongprajukaew K, Suanyuk N (2019) Effects of dietary supplementation of oligosaccharides on growth performance, gut health and immune response of hybrid catfish (Pangasianodon gigas × Pangasianodon hypophthalmus). Aquaculture 507:97–107. https://doi.org/10.1016/j.aquaculture.2019.04.010
Hoseinifar SH, Sun YZ, Wang A, Zhou Z (2018) Probiotics as means of diseases control in aquaculture, a review of current knowledge and future perspectives. Front Microbiol 9:24–29. https://doi.org/10.3389/fmicb.2018.02429
Hoseini SM, Yousefi M, Hoseinifar SH et al (2019) Effects of dietary arginine supplementation on growth, biochemical, and immunological responses of common carp (Cyprinus carpio L.), stressed by stocking density. Aquaculture 503:452–459. https://doi.org/10.1016/j.aquaculture.2019.01.031
Hu X, Yang HL, Yan YY, Zhang CX, Ye JD, Lu KL, Hu LH, Zhang JJ, Ruan L, Sun YZ (2019) Effects of fructooligosaccharide on growth, immunity and intestinal microbiota of shrimp (Litopenaeus vannamei) fed diets with fish meal partially replaced by soybean meal. Aquaculture Nutrition 25:194–204. https://doi.org/10.1111/anu.12843
Huang CY, Lin HC, Lin CH (2015) Effects of hypoxia on ionic regulation, glycogen utilization and antioxidative ability in the gills and liver of the aquatic air-breathing fish Trichogaster microlepis. Comp Biochem Physiol A Mol Integr Physiol 179:25–34. https://doi.org/10.1016/j.cbpa.2014.09.001
Ibrahem MD, Fathi M, Mesalhy S, Abd El-Aty AM (2010) Effect of dietary supplementation of inulin and vitamin C on the growth, hematology, innate immunity, and resistance of Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol 29:241–246. https://doi.org/10.1016/j.fsi.2010.03.004
Jiang WD, Tang RJ, Liu Y, Kuang SY, Jiang J, Wu P, Zhao J, Zhang YA, Tang L, Tang WN, Zhou XQ, Feng L (2015) Manganese deficiency or excess caused the depression of intestinal immunity, induction of inflammation and dysfunction of the intestinal physical barrier, as regulated by NF-κB, TOR and Nrf2 signalling, in grass carp (Ctenopharyngodon idella). Fish Shellfish Immunol 46:406–416. https://doi.org/10.1016/j.fsi.2015.06.007
KeramatAmirkolaie A, Karimzadeh J, AbedianKenari A (2014) The effects of organic selenium on performance and oxidative level in rainbow trout Oncorhynchus mykiss, Walbaum, 1792 fed a high-fat diet. Journal of Animal and Feed Sciences 23:90–96. https://doi.org/10.22358/jafs/65721/2014
Kim BM, Lee JW, Seo JS, Shin KH, Rhee JS, Lee JS (2015) Modulated expression and enzymatic activity of the monogonont rotifer Brachionus koreanus Cu/Zn- and Mn-superoxide dismutase (SOD) in response to environmental biocides. Chemosphere 120:470–478. https://doi.org/10.1016/j.chemosphere.2014.08.042
Kim YS, Ke F, Zhang QY (2009) Effect of β-glucan on activity of antioxidant enzymes and Mx gene expression in virus infected grass carp. Fish Shellfish Immunol 27:336–340. https://doi.org/10.1016/j.fsi.2009.06.006
Klein JA, Ackerman SL (2003) Oxidative stress, cell cycle, and neurodegeneration. J Clin Investig 111:785–793. https://doi.org/10.1172/JCI200318182
Kubrak OI, Husak VV, Rovenko BM, Storey JM, Storey KB, Lushchak VI (2011) Cobalt-induced oxidative stress in brain, liver and kidney of goldfish Carassius auratus. Chemosphere 85:983–989. https://doi.org/10.1016/j.chemosphere.2011.06.078
Li L, Feng L, Jiang WD, Jiang J, Wu P, Zhao J, Kuang SY, Tang L, Tang WN, Zhang YA, Zhou XQ, Liu Y (2015) Dietary pantothenic acid depressed the gill immune and physical barrier function via NF-κB, TOR, Nrf2, p38MAPK and MLCK signaling pathways in grass carp (Ctenopharyngodon idella). Fish Shellfish Immunol 47:500–510. https://doi.org/10.1016/j.fsi.2015.09.038
Liu A, Leng X, Li X, Liu, Shi S, Wang L (2009) Effects of flavomycin and mannan oligosaccharides on growth performance, nutrients digestibility and non-specific immunity in tilapia (Oreochromis niloticus × O.aureus). China Feed 3:29–32. https://doi.org/10.15906/j.cnki.cn11-2975/s.2009.03.009
Liu B, Xu L, Ge X, Xie J, Xu P, Zhou Q, Pan L, Zhang YY (2013) Effects of mannan oligosaccharide on the physiological responses, HSP70 gene expression and disease resistance of Allogynogenetic crucian carp (Carassius auratus gibelio) under Aeromonas hydrophila infection. Fish Shellfish Immunol 34:1395–1403. https://doi.org/10.1016/j.fsi.2013.02.028
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT Method. Methods 5(4):402–408. https://doi.org/10.1006/meth.2001.1262
Lu J, Qi C, Limbu SM, Han F, Yang L, Wang X, Qin JG, Chen L (2019) Dietary mannan oligosaccharide (MOS) improves growth performance, antioxidant capacity, non-specific immunity and intestinal histology of juvenile Chinese mitten crabs (Eriocheir sinensis). Aquaculture 510:337–346. https://doi.org/10.1016/j.aquaculture.2019.05.048
Lushchak VI, Bagnyukova TV, Husak VV, Luzhna LI, Lushchak OV, Storey KB (2005) Hyperoxia results in transient oxidative stress and an adaptive response by antioxidant enzymes in goldfish tissues. Int J Biochem Cell Biol 37:1670–1680. https://doi.org/10.1016/j.biocel.2005.02.024
Lushchak VI, Bagnyukova TV (2007) Hypoxia induces oxidative stress in tissues of a goby, the rotan Perccottus glenii. Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology 148:390–397. https://doi.org/10.1016/j.cbpb.2007.07.007
Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101:13–30. https://doi.org/10.1016/j.aquatox.2010.10.006
Lushchak VI (2016) Contaminant-induced oxidative stress in fish: a mechanistic approach. Fish Physiol Biochem 42:711–747. https://doi.org/10.1007/s10695-015-0171-5
Magnoni LJ, Martos-Sitcha JA, Queiroz A et al (2017) Dietary supplementation of heat-treated Gracilaria and Ulva seaweeds enhanced acute hypoxia tolerance in gilthead sea bream (Sparus aurata). Biology Open 6(6):897–908. https://doi.org/10.1242/bio.024299
Matozzo V, Gallo C, Monari M, Marin MG (2011) Cellular and biochemical parameters in the crab Carcinus aestuarii after experimentally-induced stress: Effects of bacterial injection, leg ablation and bacterial injection/leg ablation combination. J Exp Mar Biol Ecol 398:18–25. https://doi.org/10.1016/j.jembe.2010.11.014
Mo WY, Cheng Z, Choi WM, Lun CHI, Man YB, Wong JTF, Chen XW, Lau SCK, Wong MH (2015) Use of food waste as fish feeds: effects of prebiotic fibers (inulin and mannanoligosaccharide) on growth and non-specific immunity of grass carp (Ctenopharyngodon idella). Environ Sci Pollut Res 22:17663–17671. https://doi.org/10.1007/s11356-015-4971-z
Momeni-Moghaddam P, Keyvanshokooh S, Ziaei-Nejad S, ParvizSalati A, Pasha-Zanoosi H (2015) Effects of mannan oligosaccharide supplementation on growth, some immune responses and gut lactic acid bacteria of common carp (Cyprinus Carpio) fingerlings. Veterinary research forum: an international quarterly journal 6:239–44 (https://www.researchgate.net/publication/295251825)
Ni M, Wen H, Li J, Chi M, Bu Y, Ren Y, Zhang M, Song Z, Ding H (2014) The physiological performance and immune responses of juvenile Amur sturgeon (Acipenser schrenckii) to stocking density and hypoxia stress. Fish Shellfish Immunol 36:325–335. https://doi.org/10.1016/j.fsi.2013.12.002
Nikinmaa M (2002) Oxygen-dependent cellular functions - why fishes and their aquatic environment are a prime choice of study. Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology 133:1–16. https://doi.org/10.1016/S1095-6433(02)00132-0
Olsen RE, Myklebust R, Kryvi H, Mayhew TM, Ringø E (2001) Damaging effect of dietary inulin on intestinal enterocytes in Arctic charr (Salvelinus alpinus L.). Aquac Res 32:931–934. https://doi.org/10.1046/j.1365-2109.2001.00626.x
Ortiz LT, Rebolé A, Velasco S, Rodríguez ML, Treviño J, Tejedor JL, Alzueta C (2013) Effects of inulin and fructooligosaccharides on growth performance, body chemical composition and intestinal microbiota of farmed rainbow trout (Oncorhynchus mykiss). Aquac Nutr 19:475–482. https://doi.org/10.1111/j.1365-2095.2012.00981.x
Pelster B, Wood CM, Jung E, Val AL (2018) Air-breathing behavior, oxygen concentrations, and ROS defense in the swimbladders of two erythrinid fish, the facultative air-breathing jeju, and the non-air-breathing traira during normoxia, hypoxia and hyperoxia. J Comp Physiol [b] 188:437–449. https://doi.org/10.1007/s00360-017-1142-1
Piccolo G, Centoducati G, Marono S, Bovera F, Tudisco R, Nizza A (2011) Effects of the partial substitution of fish meal by soy bean meal with or without mannanoligosaccharide and fructooligosaccharide on the growth and feed utilization of sharpsnout seabream, Diplodus puntazzo (Cetti, 1777): Preliminary results. Ital J Anim Sci 10:195–199. https://doi.org/10.4081/ijas.2011.e37
Rahimnejad S, Bang IC, Park JY, Sade A, Choi J, Lee SM (2015) Effects of dietary protein and lipid levels on growth performance, feed utilization and body composition of juvenile hybrid grouper, Epinephelus fuscoguttatus × E. lanceolatus. Aquaculture 446:283–289. https://doi.org/10.1016/j.aquaculture.2015.05.019
Ren ZL, Wang SF, Cai Y, Wu Y, Tian LJ, Wang SQ, Jiang L, Guo WL, Sun Y, Zhou YC (2020) Effects of dietary mannan oligosaccharide supplementation on growth performance, antioxidant capacity, non-specific immunity and immune-related gene expression of juvenile hybrid grouper (Epinephelus lanceolatus ♂ × Epinephelus fuscoguttatus ♀ ). Aquaculture 23:735195. https://doi.org/10.1016/j.aquaculture.2020.735195
Ringø E, Olsen RE, Gifstad T, Dalmo RA, Amlund H, Hemre GI, Bakke AM (2010) Prebiotics in aquaculture: a review. Aquac Nutr 16:117–136. https://doi.org/10.1111/j.1365-2095.2009.00731.x
Song SK, Beck BR, Kim D, Park J, Kim J, Kim HD, Ringø E (2014) Prebiotics as immunostimulants in aquaculture: a review. Fish Shellfish Immunol 40:40–48. https://doi.org/10.1016/j.fsi.2014.06.016
Sun Z, Tan X, Ye H, Zou C, Ye C, Wang A (2018) Effects of dietary Panax notoginseng extract on growth performance, fish composition, immune responses, intestinal histology and immune related genes expression of hybrid grouper (Epinephelus lanceolatus ♂ × Epinephelus fuscoguttatus ♀ ). Fish Shellfish Immunol 73:234–244. https://doi.org/10.1016/j.fsi.2017.11.007
Talpur AD, Ikhwanuddin M (2013) Azadirachta indica (neem) leaf dietary effects on the immunity response and disease resistance of Asian seabass, Lates calcarifer challenged with Vibrio harveyi. Fish Shellfish Immunol 34:254–264. https://doi.org/10.1016/j.fsi.2012.11.003
Tan X, Sun Z, Liu Q, Ye H, Zou C, Ye C, Wang A, Lin H (2018) Effects of dietary ginkgo biloba leaf extract on growth performance, plasma biochemical parameters, fish composition, immune responses, liver histology, and immune and apoptosis-related genes expression of hybrid grouper (Epinephelus lanceolatus ♂ × Epinephelus fuscoguttatus ♀ ). Fish Shellfish Immunol 72:399–409. https://doi.org/10.1016/j.fsi.2017.10.022
Torrecillas S, Makol A, Caballero MJ, Montero D, Robaina L, Real F, Sweetman J, Tort L, Izquierdo MS (2007) Immune stimulation and improved infection resistance in European sea bass (Dicentrarchus labrax) fed mannan oligosaccharides. Fish Shellfish Immunol 23:969–981. https://doi.org/10.1016/j.fsi.2007.03.007
Trachootham D, Lu W, Ogasawara MA, Valle NRD, Huang P (2008) Redox regulation of cell survival. Antioxid Redox Signal 10:1343–1374. https://doi.org/10.1089/ars.2007.1957
Tripathi T, Shahid M, Raza A, Khan HM, Khan RA, Mahdi AA, Siddiqui M, Malik A, Khan AA (2012) Dose-dependent effect of histamine on liver function markers in immunized rabbits. Exp Toxicol Pathol 64:875–881. https://doi.org/10.1016/j.etp.2011.03.010
Tuo Y, Song X, Song Y, Liu W, Tang Y, Gao Y, Jiang S, Qian F, Mu G (2018) Screening probiotics from Lactobacillus strains according to their abilities to inhibit pathogen adhesion and induction of pro-inflammatory cytokine IL-8. J Dairy Sci 101:4822–4829. https://doi.org/10.3168/jds.2017-13654
Welker AF, Moreira DC, Campos ÉG, Hermes-Lima M (2013) Role of redox metabolism for adaptation of aquatic animals to drastic changes in oxygen availability. Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology 165:384–404. https://doi.org/10.1016/j.cbpa.2013.04.003
WendelaarBonga SE (1997) The stress response in fish. Physiol Rev 77(3):591–625. https://doi.org/10.1152/physrev.1997.77.3.591
Wu Y, Liu WB, Li HY, Xu WN, He JX, Li XF, Jiang GZ (2013) Effects of dietary supplementation of fructooligosaccharide on growth performance, body composition, intestinal enzymes activities and histology of blunt snout bream (Megalobrama amblycephala) fingerlings. Aquac Nutr 19:886–894. https://doi.org/10.1111/anu.12033
Yeh CH, Hsu SP, Yang CC, Chien CT, Wang NP (2010) Hypoxic preconditioning reinforces HIF-alpha-dependent HSP70 signaling to reduce ischemic renal failure-induced renal tubular apoptosis and autophagy. Life Sci 86:115–123. https://doi.org/10.1016/j.lfs.2009.11.022
Zeng L, Wang YH, Ai CX, Zheng JL, Wu CW, Cai R (2016) Effects of β-glucan on ROS production and energy metabolism in yellow croaker (Pseudosciaena crocea) under acute hypoxic stress. Fish Physiol Biochem 42:1395–1405. https://doi.org/10.1007/s10695-016-0227-1
Zhang C, Zhang J, Ren H, Guan W (2017) Effects of fructo-oligosaccharide on immune response and antioxidant capability in serum of blunt snout bream Megalobrama amblycephala exposed to thermal stress. Journal Of Dalian Ocean University 32(04):399–404. https://doi.org/10.16535/j.cnki.dlhyxb.2017.04.004
Zhang D, Zhang L, Wang J, Ma J, Li B, Jiang K (2013) Effect of dairy-yeast prebiotic on growth performance and antioxidant capability of juvenile starry flounder Platichthys stellatus. Progress in Fishery Sciences 34(4):34–42. https://doi.org/10.3969/j.issn.1000-7075.2013.04.006
Zhang G, Mao J, Liang F, Chen J, Zhao C, Yin S, Wang L, Tang Z, Chen S (2016) Modulated expression and enzymatic activities of Darkbarbel catfish, Pelteobagrus vachelli for oxidative stress induced by acute hypoxia and reoxygenation. Chemosphere 151:271–279. https://doi.org/10.1016/j.chemosphere.2016.02.072
Zhang X, Wu I, Jiang Z, Lu Y, Chen W (2014) Effects of fructo-oligosaccharides and mannan oligosaccharides on growth performance and serum biochemical indices of juvenile turbot Scophthalmus maximus. Fisheries Science 33(9):545–550. https://doi.org/10.16378/j.cnki.1003-1111.2014.09.004
Zhang Z, Yang Z, Ding N, Xiong W, Zheng G, Lin Q, Zhang G (2018) Effects of temperature on the survival, feeding, and growth of pearl gentian grouper (female Epinephelus fuscoguttatus × male Epinephelus lanceolatus). Fish Sci 84:399–404. https://doi.org/10.1007/s12562-017-1163-4
Zhao J, Liu Y, Jiang J, Wu P, Jiang W, Li S, Tang L, Kuang S, Feng L, Zhou X (2013) Effects of dietary isoleucine on the immune response, antioxidant status and gene expression in the head kidney of juvenile Jian carp (Cyprinus carpio var. Jian). Fish Shellfish Immunol 35:572–580. https://doi.org/10.1016/j.fsi.2013.05.027
Zhou QC, Buentello JA, Gatlin DM (2010) Effects of dietary prebiotics on growth performance, immune response and intestinal morphology of red drum (Sciaenops ocellatus). Aquaculture 309:253–257. https://doi.org/10.1016/j.aquaculture.2010.09.003
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This study was funded by the National Natural Science Foundation of China (No. 31860739, 42066007), Major Science and Technology Projects in Hainan Province (No. ZDKJ2019011).
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SW and LT designed and carried out majority of the experiments and drafted the article. YW participated in aquaculture experiment, sample collecting. BG participated in aquaculture experiment, and sample collecting. YC helped design the experiments, provided funding support and was involved in writing-review and editing. JL participated in data collecting and analyzing. YZ provided funding and was involved in writing-review and editing. All authors read and approved the final manuscript.
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Wang, S., Tian, L., Wu, Y. et al. An accidental discovery of mannan-oligosaccharide’s protection effect against air exposure and its potential mechanism in hybrid grouper (Epinephelus lanceolatus ♂ × Epinephelus fuscoguttatus ♀). Fish Physiol Biochem 48, 1285–1297 (2022). https://doi.org/10.1007/s10695-022-01118-9
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DOI: https://doi.org/10.1007/s10695-022-01118-9