Effects on Dietary Supplementation of Algal Oligosaccharides or Red Algal Oligosaccharides on Growth Performance, Muscle Nutrient Composition and Serum Immune Function of Oncorhynchus mykiss
TANG Wei1,2,3, WANG Qi3, LI Jia-Xin1, ZHANG Jun1,3, WU Chun-Guang3, HE Zeng-Guo2,3,*
1 School of Medicine and Pharmacy, Ocean University of China, Qingdao 266003, China; 2 Marine Microbiology Engineering Research and Development Center, Marine Biomedical Research Institute of Qingdao, Qingdao 266100, China; 3 Qingdao Bioantai Biotechnology Limited Company, Qingdao 266100, China
Abstract:As functional marine oligosaccharides, algae oligosaccharides (AOS) and red algae oligosaccharides (ROS) had a variety of biological activities, they gradually showed excellent characteristics and potential. In this study, to explore the role of marine functional oligosaccharides in aquaculture, the growth performance, muscle nutrient composition and serum immunity function of Oncorhynchus mykiss were investigated by adding AOS or ROS in diets. The experiment was divided into 5 groups: The control group was fed a basic diet, while the experimental groups were supplemented with either 0.25% or 0.5% AOS or ROS in the basic feed, respectively. The experimental period was 37 d. The results showed that 0.25% of AOS had significant effects on the weight gain rate (WGR) and specific growth rate of O. mykiss (P<0.05). In terms of nutrition, both oligosaccharides could significantly increase the content of crude lipid, essential amino acids and flavor amino acids in back muscle (P<0.05), and the high-dose group was superior to the low-dose group. At the same time, the content of unsaturated fat acid was increased, and the content of eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) were significantly increased when the addition amount was 0.5% (P<0.01). In terms of immune function, both could improve the activities of lysozyme, acid phosphatase, alkaline phosphatase, superoxide dismutase, catalase, glutathione peroxidase and total antioxidant capacity in the serum of O. mykiss, the high-dose group was generally outperforming the low-dose group. This study indicated that feeding AOS or ROS to O. mykiss had a promoting effect on growth, which is helpful in improving the nutritional and flavor quality of fish meat. It also improved the immunity and disease resistance of O. mykiss, and has potential applications value in the addition of aquatic feed.
汤伟, 王祺, 李佳欣, 张军, 吴春光, 何增国. 饲料中添加褐藻寡糖、红藻寡糖对虹鳟生长性能、肌肉营养成分及血清免疫功能的影响[J]. 农业生物技术学报, 2024, 32(9): 2100-2111.
TANG Wei, WANG Qi, LI Jia-Xin, ZHANG Jun, WU Chun-Guang, HE Zeng-Guo. Effects on Dietary Supplementation of Algal Oligosaccharides or Red Algal Oligosaccharides on Growth Performance, Muscle Nutrient Composition and Serum Immune Function of Oncorhynchus mykiss. 农业生物技术学报, 2024, 32(9): 2100-2111.
[1] 曹岩磊, 鲁耀鹏, 许嘉芮, 等. 2022. 功能性寡糖在水产动物饲料中的应用研究进展[J]. 中国饲料, 669(07): 88-95. (Cao Y L, Lu Y P, Xu J R, et al.2022. Research progress of functional oligosaccharides in aquatic animal feed[J]. China Feed, 669(07): 88-95.) [2] 高沛, 葛鹏飞, 姜启兴, 等. 2022. 虹鳟鱼各组织营养成分分析及评价[J]. 食品安全质量检测学报, 13(17): 5578-5585. (Gao P, Ge P F, Jiang Q X, et al.2022. Nutritional analysis and evaluation of different tissues of Oncorhynchus mykiss[J]. Journal of Food Safety and Quality, 13(17): 5578-5585.) [3] 管玲玲, 刘小红, 田海宁, 等. 2022. 不同养殖模式下三倍体虹鳟鱼肉品质差异的研究[J]. 水生生物学报, 46(07): 1016-1028. (Guan L L, Liu X H, Tian H N, et al.2022. Fillet quality difference of triploid rainbow trout (Oncorhynchus mykiss) cultured under different modes[J]. Acta Hydrobiologica Sinica, 46(07): 1016-1028.) [4] 胡凌豪, 杨红玲, 赵芸, 等. 2019. 果寡糖对斜带石斑鱼免疫功能和肠道形态的影响[J]. 水产科学, 38(05): 589-594. (Hu L H, Yang H L, Zhao Y, et al.2019. Effects of fructooligosaccharide on immune function and intestinal morphology of grouper Epinephelus coioides[J]. Fisheries Science, 38(05): 589-594.) [5] 黄健彬, 迟艳, 周传朋, 等. 2022. 褐藻寡糖对卵形鲳鲹幼鱼生长性能、抗氧化能力和免疫功能的影响[J]. 南方水产科学, 18(03): 118-128. (Huang J B, Chi Y, Zhou C P, et al.2022. Effects of dietary alginate oligosaccharide on growth performance, antioxidative capacity and immune function of juvenile Trachinotus ovatus[J]. South China Fisheries Science, 18(03): 118-128.) [6] 霍圃宇, 潘金露, 韩雨哲, 等. 2015. 褐藻酸寡糖对大菱鲆幼鱼生长性能、血液学指标及非特异性免疫影响[J]. 广东海洋大学学报, 35(04): 10-16. (Huo P Y, Pan J L, Han Y Z, et al.2015. Effects of alginate oligosaccharides on the growth performance, hematological parameters and non-specific immunity of juvenile turbot, Scophthalmus maximus[J]. Journal of Guangdong Ocean University, 35(04): 10-16.) [7] 江晓路, 杜以帅, 王鹏, 等. 2009. 褐藻寡糖对刺参体腔液和体壁免疫相关酶活性变化的影响[J]. 中国海洋大学学报(自然科学版), 39(06): 1188-1192. (Jiang X L, Du Y S, Wang P, et al.2009. Effects of alginate-derived oligosaccharide on the activities of immunoenzymes in the coelomic fluid and body wall of sea cucumber (Apostichopus japonicus)[J]. Periodical of Ocean University of China, 39(06): 1188-1192.) [8] 李温蓉, 田明礼, 安玥琦, 等. 2022. 池塘养殖和大湖养殖对“华海1号”团头鲂鱼肉品质的影响[J]. 水产学报, 46(07): 1220-1234. (Li W R, Tian M L, An Y Q, et al.2022. Effects of pond culture and lake culture on fish quality of Megalobrama amblycephala "Huahai No.1"[J]. Journal of Fisheries of China, 46(07): 1220-1234.) [9] 陆凤霞. 2016. 龙须菜寡糖和藻渣对罗非鱼生理特性的影响[D]. 硕士学位论文, 集美大学, 导师: 曾润颖, 张志刚. pp. 40-48. (Lu F X.2016. Effects of aparagus oligosaccharides and algae residue on the physiological characteristics of Tilapia[D]. Thesis for M.S., Jimei University, Supervisor: Zeng R Y, Zhang Z G. pp. 40-48.) [10] 马莹莹, 贾永义, 顾亭亭, 等. 2023. 甘露寡糖对高糖饲喂下尼罗罗非鱼肌肉品质的影响[J/OL]. 水产学报, 1-14. (Ma Y Y, Jia Y Y, Gu T T, et al.2023. Effects of manna oligosaccharides on flesh quality of Nile tilapia (Oreochromis niloticus) fed with high carbohydrate diet[J]. Journal of Fisheries of China, 1-14.) [11] 马悦欣, 许珂, 王银华, 等. 2010. κ-卡拉胶寡糖对仿刺参溶菌酶、碱性磷酸酶和超氧化物歧化酶活性的影响[J]. 大连海洋大学学报, 25(03): 224-227. (Ma Y X, Xu K, Wang Y H, et al.2010. Effects of κ-carrageenan oligosaccharides on activities of lysozyme, alkaline phosphatase and superoxide dismutase of coelomic fluid in sea cucumber Apostichopus japonica[J]. Journal of Dalian Ocean University, 25(03): 224-227.) [12] 孟繁伊, 黄权, 郝凤奇. 2009. 不同年龄花羔红点鲑肌肉成分和血液指标的比较研究[J]. 中国水产科学, 16(1): 113-119. (Meng F Y, Huang Q, Hao F Q, et al.2009. Comparative studies on muscle composition and blood index of Salvelinus malma at different ages[J]. Fisheries Science, 16(1): 113-119.) [13] 潘金露, 韩雨哲, 霍圃宇, 等. 2016. 饲料中添加褐藻酸寡糖对大菱鲆肠道结构、消化酶活性及表观消化率的影响[J]. 广东海洋大学学报, 36(03): 39-44. (Pan J L, Han Y Z, Huo P Y, et al.2016. Effects of dietary alginate oligosaccharide on intestinal morphology, activities of digestive enzymes and apparent digestibility of turbot (Scophthalmus maximus L)[J]. Journal of Guangdong Ocean University, 36(03): 39-44.) [14] 邱愚蘅, 孙孟辉, 王欣, 等. 2019. 不同暂养添加物对Cd2+胁迫的紫贻贝机体免疫功能的调节作用[J]. 食品工业科技, 40(23): 10-16. (Qiu Y H, Sun M H, Wang X, et al.2019. Effects of different temporary additives on immune function of Mytilus edulis under cadmium (Cd2+) stress[J]. Science and Technology of Food Industry, 40(23): 10-16.) [15] 施斐, 黄垚, 卢志杰, 等. 2022. 壳寡糖对虎龙斑的生长、免疫及肠道菌群的影响[J]. 水产学报, 46(09): 1689-1700. (Shi F, Huang Y, Lu Z J, et al.2022. Effects of oligochitosan on the growth, immune responses and gut microbes of hybrid groupers [Epinephelus fuscoguttatus (♀)× E. lanceolatu (♂)][J]. Journal of Fisheries of China, 46(09): 1689-1700.) [16] 孙慧慧, 杨国淞, 程伊梦, 等. 2022. 海洋寡糖的生物活性研究进展[J]. 食品科学, 43(13): 276-284. (Sun H H, Yang G S, Cheng Y M, et al.2022. Progress in understanding the biological activities of marine oligosaccharides[J]. Food Science, 43(13): 276-284.) [17] 吴永俊, 王玉涛, 施文正, 等. 2017. 不同产地虹鳟鱼肉风味物质的比较[J]. 上海海洋大学学报, 26(06): 888-899. (Wu Y J, Wang Y T, Shi W Z, et al.2017. Comparison of flavor substances of different parts of rainbow trout in different regions[J]. Journal of Shanghai Ocean University, 26(06): 888-899.) [18] 谢全森, 蔡灵, 孙彩娟, 等. 2019. 不同生长阶段的生态养殖台湾鳗鳅的营养特性研究[J]. 食品研究与开发, 40(15): 36-42. (Xie Q S, Cai L, Sun C J, et al.2019. Nutritional quality of ecological breeding Taiwan Paracobitis anguillioides with different growth phase[J]. Food Research and Development, 40(15): 36-42.) [19] 张梦婷, 李兆新, 邢丽红, 等. 2023. 褐藻寡糖及其锌络合物对暗纹东方鲀消化能力、血清生化指标及肠道菌群的影响[J]. 饲料工业, 44(04): 85-91. (Zhang M T, Li Z X, Xing L H, et al.2023. Effects of alginate oligosaccharides and its zinc complex on digestive ability, serum biochemical indexes and intestinal microflora of Takifugu Obscurus[J]. Feed Industry, 44(04): 85-91.) [20] 张意敏, 朱华平, 卢迈新, 等. 2014. 果寡糖对尼罗罗非鱼非特异性免疫及抗病力的影响[J].淡水渔业, 44(2): 62-66+76. (Zhang Y M, Zhu H P, Lu M X, et al.2014. Effects of fructooligosaccharides on non-specific immunity and disease resistance of tilapia (Oreochromis niloticus)[J]. Freshwater Fisheries, 44(2): 62-66+76.) [21] 赵吉伟, 张颖, 卢彤岩, 等. 2005. 不同硒源对虹鳟生长性能及抗氧化能力的影响[J]. 水产学杂志, 18(2): 28-34. (Zhao J W, Zhang Y, Lu T Y, et al.2005. Effects of different selenium resources on growth performance and antioxidant defenses of rainbow trout[J]. Chinese Journal of Fisheries, 18(2): 28-34.) [22] 钟绮媚, 张晶晶, 杨志友, 等. 2022. 不同ω-3多不饱和脂肪酸对斑马鱼阿尔茨海默病模型记忆损伤和神经病理学变化影响[J]. 广东海洋大学学报, 42(04): 118-128. (Zhong Q M, Zhang J J, Yang Z Y, et al.2022. Effects of different ω-3 polyunsaturated fatty acids on memory impairment and neuropathological changes in zebrafish alzheimer's disease model[J]. Journal of Guangdong Ocean University, 42(04): 118-128.) [23] Abasubong K P, Li X F, Zhang D D, et al.2018. Dietary supplemen tation of xylooligosaccharides benefits the growth performance and lipid metabolism of common carp (Cyprinus carpio) fed high-fat diets[J]. Aquaculture Nutrition, 24(5): 1416-1424. [24] Adeyemi W J, Lawal S I, Olatunji D B, et al.2021. Omega 3 fatty acids favour lipid and bone metabolism in orchidectomised rats[J]. Clinical Nutrition Open Science, 35: 67-76. [25] Ashouri G, Soofiani N M, Hoseinifar S H, et al.2020. Influence of dietary sodium alginate and Pediococcus acidilactici on liver antioxidant status, intestinal lysozyme gene expression, histomorphology, microbiota, and digestive enzymes activity, in Asian sea bass (Lates calcarifer) juveniles[J]. Aquaculture, 518: 734638. [26] Bagin M, Romano N, Finia M G, et al.2005. Short- and longterm effects of a dietary yeast β-glucan (Macrogard) and alginic acid (Ergosan) preparation on immune response in sea bass (Dicentrarchus labrax)[J]. Fish Shellfish Immunol, 18(4): 311-325. [27] Bilen S, Bulut M, Bilen A M.2011. Immunostimulant effects of Cotinus coggyria on rainbow trout (Oncorhynchus mykiss)[J]. Fish & Shellfish Immunology, 30(2): 451-455. [28] Chi C, Giri S S, Jun J W, et al.2017. Effects of algal toxin okadaic acid on the non-specific immune and antioxidant response of bay scallop (Argopecten irradians)[J]. Fish & Shellfish Immunology, 65: 111-117. [29] Ding Z J, Wang X, Liu YL, et al.2022. Dietary mannan oligosaccharides enhance the non-specific immunity, intestinal health, and resistance capacity of juvenile blunt snout bream (Megalobrama amblycephala) against Aeromonas hydrophila[J]. Frontiers in Immunology, 13: 863657. [30] Gainza O, Romero J.2020. Effect of mannan oligosaccharides on the microbiota and productivity parameters of Litopenaeus vannamei shrimp under intensive cultivation in Ecuador[J]. Scientific Reports, 10(1): 2719. [31] González A, Martínez M L, Paredes A J, et al.2016. Study of the preparation process and variation of wall components in chia (Salvia hispanica L.) oil microencapsulation[J]. Powder Technology, 301: 868-875. [32] Gu M, Pan S, Li Q, et al.2021. Chitosan and chitooligosaccharides attenuate soyabean meal-induced intestinal inflammation of turbot (Scophthalmus maximus): Possible involvement of NF-кB, activator protein-1 and mitogen-activated protein kinases pathways[J]. The British Journal of Nutrition, 126(11): 1651-1662. [33] Gupta S, Lokesh J, Abdelhafiz Y, et al.2019. Macroalga-derived alginate oligosaccharide alters intestinal bacteria of atlantic salmon[J]. Frontiers in Microbiology, 10: 1-15. [34] Han Z L, Yang M, Fu X D, et al.2019. Evaluation of prebiotic potential of three marine algae oligosaccharides from enzymatic hydrolysis[J]. Marine Drugs, 17(3): 173. [35] Hoseinifar S H, Mirvaghefi A, Amoozegar M A, et al.2015. Modulation of innate immune response, mucosal parameters and disease resistance in rainbow trout (Oncorhynchus mykiss) upon synbiotic feeding[J]. Fish & shellfish immunology, 45(1): 27-32. [36] Lee H, Park W J.2014. Unsaturated fatty acids, desaturases, and human health[J]. Journal of Medicinal Food, 17(2): 189-197. [37] Li F, Tang Y, Wei L, et al.2022. Alginate oligosaccharide modulates immune response, fat metabolism, and the gut bacterial community in grass carp (Ctenopharyngodon idellus)[J]. Fish & shellfish immunology, 130: 103-113. [38] Liu M, Liu L, Zhang H F, et al.2021. Alginate oligosaccharides preparation, biological activities and their application in livestock and poultry[J]. Journal of Integrative Agriculture, 20(01): 24-34. [39] Lu Y, Zheng P, Zhang X, et al.2021. Effects of dietary trehalose on growth, trehalose content, non-specific immunity, gene expression and desiccation resistance of juvenile red claw crayfish (Cherax quadricarinatus)[J]. Fish & Shellfish Immunology, 119: 524-532. [40] Malo M S, Moaven O, Muhammad N, et al.2014. Intestinal alkaline phosphatase promotes gut bacterial growth by reducing the concentration of luminal nucleotide triphosphates[J]. American Journal of Physiology Gastrointestinal & Liver Physiology, 306(10): 826-838. [41] Maslowski K M, Mackay C R.2011. Diet, gut microbiota and immune responses[J]. Nature Immunology, 12(1):5-9. [42] Park H J, Ahn J M, Park R M, et al.2016. Effects of alginate oligosaccharide mixture on the bioavailability of lysozyme as an antimicrobial agent[J]. Journal of Nanoscience and Nanotechnology, 16(2): 1445-1449. [43] Poolsawat L, Li X Q, Xu X Y, et al.2021. Dietary xylooligosaccharide improved growth, nutrient utilization, gut microbiota and disease resistance of tilapia (Oreochromis niloticus × O. aureus)[J]. Animal Feed Science and Technology, 275(1): 114872. [44] Valente L M P, Batista S, Ribeiro C, et al.2021. Physical processing or supplementation of feeds with phytogenic compounds, alginate oligosaccharide or nucleotides as methods to improve the utilization of Gracilaria gracilis by juvenile European seabass (Dicentrarchus labrax)[J]. Aquaculture, 530(1): 735914. [45] Wang Y, Li L, Ye C, et al.2020. Alginate oligosaccharide improves lipid metabolism and inflammation by modulating gut microbiota in high-fat diet fed mice[J]. Applied Microbiology and Biotechnology, 104(11): 3541-3554. [46] Wei W T, Hu M J, Huang J, et al.2021. Anti-obesity effects of DHA and EPA in high fat-induced insulin resistant mice[J]. Food & Function, 12(4): 1614-1625. [47] Yahfoufi N, Alsadi N, Jambi M, et al.2018. The immunomodulatory and anti-inflammatory role of polyphenols[J]. Nutrients, 10(11): 1618. [48] Yang P X, Yang W N, He M, et al.2020. Dietary synbiotics improved the growth, feed utilization and intestinal structure of largemouth bass (Micropterus salmoides) juvenile[J]. Aquaculture Nutrition, 26(2): 590-600. [49] Zhao Y, Feng Y N, Liu M, et al.2020. Single-cell RNA sequencing analysis reveals alginate oligosaccharides preventing chemotherapy-induced mucositis[J]. Mucosal Immunology, 13(3): 437-448.