Effects of Carrageenan on Growth, Enzyme Activities and Intestinal Microbial Composition of Discus Fish Symphysodon haraldi
ZHANG Haoran1,2,3, WEN Bin1,2,3,4, PAN Yunchao1,2,3, YANG Botian1,2,3 , GAO Jianzhong1,2,3,4, CHEN Zaizhong1,2,3,4
1. Key Laboratory of Freshwater Aquatic Genetic Resources, Ministry of Agriculture and Rural Affairs, Shanghai Ocean University, Shanghai 201306, China; 2. Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai 201306, China; 3. Shanghai Engineering Research Center of Aquaculture, Shanghai Ocean University, Shanghai 201306, China; 4. National Demonstration Centre for Experimental Fisheries Science Education, Shanghai Ocean University, Shanghai 201306, China
Abstract：In order to evaluate effects of carrageenan on growth, digestive enzyme activity, antioxidant enzyme activity and intestinal microbial composition of discus fish Symphysodon haraldi, the discus fish with initial body weight of (10.81±2.41) g was reared in 80 L breeding tanks at stocking density of 15 individuals per tank, and fed diet containing 0% (and beef heart burger as controls), 3%, 6%, 9%, 12% and 15% carrageenan at water temperature of (28.0±0.5) ℃ for 56 days. The results showed that the maximal weight gain rate and specific growth rate were observed in 3% carrageenan group. There were significantly higher pepsin activity and foregut amylase activity in 3% carrageenan group than those in other groups, and significantly lower liver malondialdehyde level and glutathione peroxidase activities than other experimental groups. The activity of superoxide dismutase was significantly higher in liver of the discus fish fed the diet containing 12% of carrageenan than that in other experimental groups. The relative abundance of Proteobacteria was significantly higher in intestinal microbial composition in 3% carrageenan group than that in other groups at phylum level, and the relative abundance of Fusobacteria decreased. In terms of genus level, there was no Lactococcus in the beef heart burger group, significantly higher content of Rombuutsia in 3% carrageenan group than that in other carrageenan groups, and significantly higher content of the Cetobacterium than that in other groups. It was found that addition of 3% carrageenan improved the weight gain rate and specific growth rate of disc fish, significantly increased the activity of pepsin and foregut amylase, without oxidative stress, and with increase in relative abundance of Proteus, Rombudsia and Lactococcus. Under the conditions of this experiment, 3% of carrageenan is of the appropriate dietary amount for discus fish.
[1] SONG X L, WANG L, LI X Q, et al. Dietary astaxanthin improved the body pigmentation and antioxidant function, but not the growth of discus fish (Symphysodon spp.)[J]. Aquaculture Research,2017,48(4):1359-1367. [2] WEN B, CHEN Z Z, QU H C, et al. Growth and fatty acid composition of discus fish Symphysodon haraldi given varying feed ratios of beef heart, duck heart, and shrimp meat[J]. Aquaculture and Fisheries,2018,3(2):84-89. [3] HENCHION M, MCCARTHY M, O′CALLAGHAN J. Transforming beef by-products into valuable ingredients:which spell/recipe to use?[J]. Frontiers in Nutrition,2016,3:53. [4] ARGÜELLO-GUEVARA W, MOLINA-POVEDA C. Effect of binder type and concentration on prepared feed stability, feed ingestion and digestibility of Litopenaeus vannamei broodstock diets[J]. Aquaculture Nutrition,2013,19(4):515-522. [5] 林建斌,李金秋,朱庆国.软颗粒饲料与干颗粒饲料饲养牙鲆试验报告[J].科学养鱼,2006(4):67. [6] 林建斌,李金秋,朱庆国.软颗粒与膨化颗粒饲料饲喂点带石斑鱼试验[J].饲料研究,2007(10):46-47. [7] 韩金林.不同加工饲料的理化特性及其对罗非鱼生长性能的影响[D].武汉:武汉轻工大学,2015. [8] 林建斌,李金秋,朱庆国,等.不同饲料形态对点带石斑鱼摄食的影响[J].科学养鱼,2008(3):66-67. [9] ANDREW J E, ANRAS M L B, KADRI S, et al. Feeding responses of hatchery-reared gilthead sea bream (Sparus aurata L.) to a commercial diet and natural prey items[J]. Marine and Freshwater Behaviour and Physiology,2003,36(2):77-86. [10] 肖瑶,王振洁,孙涛,等.水产饲料粘合剂应用及展望[J].山东畜牧兽医,2016,37(5):56-57. [11] LANGENDORFF V, CUVELIER G, MICHON C, et al. Effects of carrageenan type on the behaviour of carrageenan/milk mixtures[J]. Food Hydrocolloids,2000,14(4):273-280. [12] FUJIKI K, SHIN D H, NAKAO M, et al. Effects of κ-carrageenan on the non-specific defense system of carp Cyprinus carpio[J]. Fisheries Science,1997,63(6):934-938. [13] VILLAMIL L, VILLAMIL S I, ROZO G, et al. Effect of dietary administration of kappa carrageenan extracted from Hypnea musciformis on innate immune response, growth, and survival of Nile tilapia (Oreochromis niloticus)[J]. Aquaculture International,2019,27(1):53-62. [14] 陈笑冰,王小洁,麦康森,等.添加不同种类的粘合剂对微颗粒饲料物理性状及大菱鲆稚鱼生长状况的影响[J].饲料工业,2011,32(10):6-10. [15] BRINKER A. Guar gum in rainbow trout (Oncorhynchus mykiss) feed:the influence of quality and dose on stabilisation of faecal solids[J]. Aquaculture,2007,267(1/2/3/4):315-327. [16] GAWLICKA A, MCLAUGHLIN L, HUNG S S O, et al. Limitations of carrageenan microbound diets for feeding white sturgeon, Acipenser transmontanus, larvae[J]. Aquaculture,1996,141(3/4):245-265. [17] AMERAH A M, RAVINDRAN V, LENTLE R G, et al. Feed particle size:implications on the digestion and performance of poultry[J]. World′s Poultry Science Journal,2007,63(3):439-455. [18] 聂国兴,王俊丽,朱命炜,等.小麦基础饲料添加木聚糖酶对尼罗罗非鱼肠道食糜粘度和绒毛、微绒毛发育的影响[J].水产学报,2007,31(1):54-61. [19] GARA A B, HAMMAMI N, CHAABEN R, et al. Inhibition of key digestive enzymes related to diabetes and protection of β-cell and liver-kidney functions by Hypnea spinella sulfated polysaccharide in diabetic rats [J/OL]. (2022-05-20)[2022-06-20]. https://www.researchsquare.com/article/rs-1665279/v1. [20] BARROSO F E C, RODRIGUES J A G, TORRES V M, et al. Efeito do polissacarídeo sulfatado extraído da alga marinha vermelha Botryocladia occidentalis nas pós-larvas do camarão Litopenaeus vannamei[J]. Revista Ciência Agronômica, 2007, 38(1): 58-63. [21] KRAUGERUD O F, PENN M, STOREBAKKEN T, et al. Nutrient digestibilities and gut function in Atlantic salmon (Salmo salar) fed diets with cellulose or non-starch polysaccharides from soy[J]. Aquaculture,2007,273(1):96-107. [22] LEENHOUWERS J I, ADJEI-BOATENG D, VERRETH J A J, et al. Digesta viscosity,nutrient digestibility and organ weights in African catfish (Clarias gariepinus) fed diets supplemented with different levels of a soluble non-starch polysaccharide[J]. Aquaculture Nutrition,2006,12(2):111-116. [23] 张振龙.胶和木聚糖对中华绒螯蟹和黄颡鱼生长、消化和肠道菌群的影响[D].苏州:苏州大学,2014. [24] TRAN-TU L C, HIEN T T T, BOSMA R H, et al. Effect of ingredient particle sizes and dietary viscosity on digestion and faecal waste of striped catfish (Pangasianodon hypophthalmus)[J]. Aquaculture Nutrition,2018,24(3):961-969. [25] BRINKER A. Improving the mechanical characteristics of faecal waste in rainbow trout:the influence of fish size and treatment with a non-starch polysaccharide (guar gum)[J]. Aquaculture Nutrition,2009,15(3):229-240. [26] THOMSON A W, FOWLER E F. Carrageenan:a review of its effects on the immune system[J]. Agents and Actions,1981,11(3):265-273. [27] CAMPOS-SÁNCHEZ J C, GUARDIOLA F A, GARCÍA BELTRÁN J M, et al. Effects of subcutaneous injection of λ/κ-carrageenin on the immune and liver antioxidant status of gilthead seabream (Sparus aurata)[J]. Journal of Fish Diseases,2021,44(9):1449-1462. [28] HOSSAIN M S, KOSHIO S, ISHIKAWA M, et al. Effects of dietary administration of guanosine monophosphate on the growth, digestibility, innate immune responses and stress resistance of juvenile red sea bream, Pagrus major[J].Fish & Shellfish Immunology,2016,57:96-106. [29] DONG Y H, YANG Y Y, LIU J, et al. Inhibition of Aeromonas hydrophila-induced intestinal inflammation and mucosal barrier function damage in crucian carp by oral administration of Lactococcus lactis[J]. Fish & Shellfish Immunology,2018,83:359-367. [30] GIVENS C E, RANSOM B, BANO N, et al. Comparison of the gut microbiomes of 12 bony fish and 3 shark species[J]. Marine Ecology Progress Series,2015,518:209-223. [31] YUKGEHNAISH K, KUMAR P, SIVACHANDRAN P, et al. Gut microbiota metagenomics in aquaculture:factors influencing gut microbiome and its physiological role in fish[J]. Reviews in Aquaculture,2020,12(3):1903-1927. [32] ZHAO J F, ZHANG X Y, LIU H B, et al. Dietary protein and gut microbiota composition and function[J]. Current Protein & Peptide Science,2019,20(2):145-154. [33] LAPARRA J M, SANZ Y. Interactions of gut microbiota with functional food components and nutraceuticals[J]. Pharmacological Research,2010,61(3):219-225. [34] DAVILA A M, BLACHIER F, GOTTELAND M, et al. Re-print of “intestinal luminal nitrogen metabolism:role of the gut microbiota and consequences for the host”[J]. Pharmacological Research,2013,69(1):114-126. [35] LIU J, CUI Y, LIU J. Food consumption and growth of two piscivorous fishes, the mandarin fish and the Chinese snakehead[J]. Journal of Fish Biology,1998,53(5):1071-1083. [36] ZHANG C, ZHENG X F, REN X, et al. Bacterial diversity in gut of large yellow croaker Larimichthys crocea and black sea bream Sparus macrocephalus reared in an inshore net pen[J]. Fisheries Science,2019,85(6):1027-1036. [37] DESAI A R, LINKS M G, COLLINS S A, et al. Effects of plant-based diets on the distal gut microbiome of rainbow trout (Oncorhynchus mykiss)[J]. Aquaculture,2012,350/351/352/353:134-142. [38] RINGO E, SPERSTAD S, MYKLEBUST R, et al. The effect of dietary inulin on aerobic bacteria associated with hindgut of Arctic charr (Salvelinus alpinus L. )[J]. Aquaculture Research,2006,37(9):891-897. [39] NI J J, YAN Q Y, YU Y H, et al. Factors influencing the grass carp gut microbiome and its effect on metabolism[J]. FEMS Microbiology Ecology,2014,87(3):704-714. [40] SUN Y, HE M W, CAO Z J, et al. Effects of dietary administration of Lactococcus lactis HNL12 on growth, innate immune response, and disease resistance of humpback grouper (Cromileptes altivelis)[J]. Fish & Shellfish Immunology,2018,82:296-303. [41] SHAPAWI R, SAFIIN N S Z, SENOO S. Improving dietary red seaweed Kappaphycus alvarezii (Doty) Doty ex. P. Silva meal utilization in Asian seabass Lates calcarifer[J]. Journal of Applied Phycology,2015,27(4):1681-1688. [42] DAWOOD M A O, KOSHIO S, ISHIKAWA M, et al. Effects of dietary supplementation of Lactobacillus rhamnosus or/and Lactococcus lactis on the growth, gut microbiota and immune responses of red sea bream, Pagrus major[J]. Fish & Shellfish Immunology,2016,49:275-285.
2024, Vol. 43 
