Effects of Dietary Selenium Yeast on Antioxidant Capacity, Immune Response, and Digestive Enzyme Activities in Manila Clam Ruditapes philippinarum
LU Yanfeng1,2, XIONG Yuyang1,2, HUO Zhongming1,2, GAO Zhiying1,2, WANG Lianshun1, DING Jianfeng1,2
1. College of Fisheries and Life Science, Dalian Ocean University, Dalian 116023, China; 2. Engineering Research Center of Shellfish Culture and Breeding in Liaoning Province, Dalian 116023, China
Abstract:To investigate the effects of different concentrations of selenium yeast on the antioxidant capacity, immune function, and digestion of Manila clam Ruditapes philippinarum, healthy clams with initial shell length of (32.49±2.50) mm and body weight of (8.16±1.81) g were cultured in 20 L tanks at water temperature of (20±1) °C and salinity of 31±1, and fed with selenium yeast powder (selenium content 6500 mg/kg) at final mass concentrations of 0 (control), 2, 4, 6, and 8 mg/L for 30 days. Activities of superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GSH-Px), acid phosphatase (ACP), alkaline phosphatase (AKP), lysozyme (LZM), and malondialdehyde (MDA), as well as total antioxidant capacity (T-AOC) in the hemolymph and hepatopancreas, along with the activities of α-amylase, trypsin, and lipase in the hepatopancreas, were determined at the end of the experiment. The results showed that: (1) SOD activity and T-AOC in hemolymph in the 8 mg/L group, CAT activity in the 2 mg/L group, and GSH-Px activity in the 6 mg/L group were significantly increased (P<0.05). In the hepatopancreas, CAT activity in the 4 mg/L group, and GSH-Px activities in the 6 and 8 mg/L groups were significantly increased (P<0.05), with the maximal SOD activity and T-AOC in the 4 mg/L group. (2) The maximal ACP activity in hemolymph was observed in the 4 mg/L group (P<0.05), with significant increase in the 8 mg/L group (P<0.05). LZM activity in hemolymph was significantly increased in the 2, 6, and 8 mg/L groups (P<0.05). In the hepatopancreas, ACP and LZM activities in the 4 mg/L group were significantly increased (P<0.05). (3) There were significant increases in trypsin activity in the 8 mg/L group and significant decrease in lipase activities in the hepatopancreas in the 2—6 mg/L groups (P<0.05), without significant difference in α-amylase activity. In conclusion, appropriate supplementation of selenium yeast can significantly regulate the antioxidant and immune functions and affect digestive enzyme activities in the hepatopancreas of Manila clam. The findings provide a foundation for the healthy aquaculture of the clam.
[1] CHEN Z, LIU H K, LIU C, et al. Effects of different dietary selenium sources on the meat quality and antioxidant capacity of yellow catfish (Pelteobagrus fulvidraco)[J].Aquaculture Nutrition,2023,2023(1):7981183. [2] YU Y L, ZHANG F M, LU D, et al. Selenium bioavailability from shrimps (Penaeus vannamei Boone) and its effect on the metabolism of phospholipid and cholesterol ester[J].Journal of Functional Foods,2014,6:186-195. [3] LE K T, FOTEDAR R. Immune responses to Vibrio anguillarum in yellowtail kingfish, Seriola lalandi, fed selenium supplementation[J].Journal of the World Aquaculture Society,2014,45(2):138-148. [4] WANG L, WU L, LIU Q, et al. Improvement of flesh quality in rainbow trout (Oncorhynchus mykiss) fed supranutritional dietary selenium yeast is associated with the inhibited muscle protein degradation[J].Aquaculture Nutrition,2018,24(4):1351-1360. [5] IBRAHIM M S, EL-GENDY G M, AHMED A I, et al. Nanoselenium versus bulk selenium as a dietary supplement: effects on growth, feed efficiency, intestinal histology, haemato-biochemical and oxidative stress biomarkers in Nile tilapia (Oreochromis niloticus Linnaeus, 1758) fingerlings[J].Aquaculture Research,2021,52(11):5642-5655. [6] WANG C, LOVELL R T, KLESIUS P H. Response to Edwardsiella ictaluri challenge by channel catfish fed organic and inorganic sources of selenium[J].Journal of Aquatic Animal Health,1997,9(3):172-179. [7] KIELISZEK M, BŁAŻ EJAK S. Selenium: significance, and outlook for supplementation[J].Nutrition,2013,29(5):713-718. [8] KIELISZEK M. Selenium-fascinating microelement, properties and sources in food[J].Molecules,2019,24(7):1298. [9] DOYOTTE A, COSSU C, JACQUIN M C, et al. Antioxidant enzymes, glutathione and lipid peroxidation as relevant biomarkers of experimental or field exposure in the gills and the digestive gland of the freshwater bivalve Unio tumidus[J].Aquatic Toxicology,1997,39(2):93-110. [10] HAN D, XIE S, LIU M, et al. The effects of dietary selenium on growth performances, oxidative stress and tissue selenium concentration of gibel carp (Carassius auratusgibelio)[J].Aquaculture Nutrition,2011,17(3):e741-e749. [11] ARAMLI M S, SARVI MOGHANLOU K, IMANI A. Effect of dietary antioxidant supplements (selenium forms, alpha-tocopherol, and coenzyme Q10) on growth performance, immunity, and physiological responses in rainbow trout (Oncorhynchus mykiss) using orthogonal array design[J].Fish & Shellfish Immunology,2023,134:108615. [12] ZHANG P H, ZHANG C, YAO X F, et al. Selenium yeast improve growth, serum biochemical indices, metabolic ability, antioxidant capacity and immunity in black carp Mylopharyngodon piceus[J].Fish & Shellfish Immunology,2024,146:109414. [13] YU Q R, XIA C Y, HAN F L, et al. Effect of different dietary selenium sources on growth performance, antioxidant capacity, gut microbiota, and molecular responses in Pacific white shrimp Litopenaeus vannamei[J].Aquaculture Nutrition,2022(1):5738008. [14] 包鹏云,李璐瑶,陈炜,等.饲料中添加混合益生菌对幼参生长、消化酶活力和体壁营养组成的影响[J].大连海洋大学学报,2018,33(1):52-56. [15] ABDOLLAHI-MOUSAVI S E, KEYVANSHOKOOH S, TORFI MOZANZADEH M, et al. Efficacy of nutritional selenium nanoparticles on growth performance, immune response, antioxidant capacity, expression of growth and immune-related genes, and post-stress recovery in juvenile Sobaity seabream (Sparidentex hasta)[J].Fish & Shellfish Immunology,2024,147:109452. [16] BLOKHINA O, VIROLAINEN E, FAGERSTEDT K V. Antioxidants, oxidative damage and oxygen deprivation stress: a review[J].Annals of Botany,2003,91(2):179-194. [17] GUAN Y Q, WANG Z H, XIAO G H, et al. Effects of selenium on the activity of antioxidant enzymes in the shrimp, Neocaridina heteropoda[J].Israeli Journal of Aquaculture-Bamidgeh,2009,61(4): 322-329. [18] ZHANG J Q, ZHENG S F, WANG S C, et al. Cadmium-induced oxidative stress promotes apoptosis and necrosis through the regulation of the miR-216a-PI3K/AKT axis in common carp lymphocytes and antagonized by selenium[J].Chemosphere,2020,258:127341. [19] 王亭亭,蔡完其.饲料中添加花粉和酵母硒对中华鳖幼鳖生长和非特异性免疫功能的影响[J].上海水产大学学报,2005,14(2):97-102. [20] KONG Y Y, LI S Q, LIU M F, et al. Effect of dietary organic selenium on survival, growth, antioxidation, immunity and gene expressions of selenoproteins in abalone Haliotis discushannai[J].Aquaculture Research,2019,50(3):847-855. [21] 赵荣文,谭丽萍,刘同军.溶菌酶及其应用研究进展[J].齐鲁工业大学学报,2021,35(1):12-18. [22] NUGROHO R A, FOTEDAR R. Effects of dietary organic selenium on immune responses, total selenium accumulation and digestive system health of marron, Cherax cainii (Austin, 2002)[J].Aquaculture Research,2015,46(7):1657-1667. [23] NING Y C, WU X Y, ZHOU X H, et al. An evaluation on the selenium yeast supplementation in the practical diets of early juvenile sea cucumber (Apostichopus japonicus): growth performance, digestive enzyme activities, immune and antioxidant capacity, and body composition[J].Aquaculture Nutrition,2021,27(6):2142-2153. [24] QIANG J, DUAN X J, ZHU C K, et al. Selenium-cultured Potamogeton maackianus in the diet can alleviate oxidative stress and immune suppression in Chinese mitten crab (Eriocheir sinensis) under copper exposure[J].Frontiers in Physiology,2020,11:713. [25] WANG L, LI X L, LU K L, et al. Dietary hydroxyl methionine selenium supplementation enhances growth performance, antioxidant ability and nitrite tolerance of Litopenaeus vannamei[J].Aquaculture,2021,537:736513. [26] CHEN L P, YU F, SUN S H, et al. Evaluation indicators of Ruditapes philippinarum nutritional quality[J].Journal of Food Science and Technology,2021,58(8):2943-2951. [27] 宋晓楠,马峻峰,秦艳杰,等.盐度骤降对菲律宾蛤仔抗氧化酶活力及组织结构的影响[J].农学学报,2013,3(1):50-56. [28] CHIU S T, HSIEH S L, YEH S P, et al. The increase of immunity and disease resistance of the giant freshwater prawn, Macrobrachium rosenbergii by feeding with selenium enriched-diet[J].Fish & Shellfish Immunology,2010,29(4):623-629. [29] KONG Y Q, DING Z L, ZHANG Y X, et al. Dietary selenium requirement of juvenile oriental river prawn Macrobrachium nipponense[J].Aquaculture,2017,476:72-78. [30] LIN Y H, SHIAU S Y. Dietary selenium requirements of juvenile grouper, Epinephelus malabaricus[J].Aquaculture,2005,250(1/2):356-363. [31] FAN J Q, LI B B, HONG Q M, et al. A glutathione peroxidase gene from Litopenaeus vannamei is involved in oxidative stress responses and pathogen infection resistance[J].International Journal of Molecular Sciences,2022,23(1):567. [32] HAMILTON S J. Review of selenium toxicity in the aquatic food chain[J].Science of the Total Environment,2004,326(1/2/3):1-31. [33] YU H B, ZHANG C, ZHANG X T, et al. Dietary nano-selenium enhances antioxidant capacity and hypoxia tolerance of grass carp Ctenopharyngodon idella fed with high-fat diet[J].Aquaculture Nutrition,2020,26(2):545-557. [34] CHEN J H, XING S P, XU H X, et al. Dietary nanometer selenium enhances the selenium accumulation, nutrient composition and antioxidant status of Paramisgurnus dabryanus spp.[J].Fishes,2024,9(1):28. [35] PACITTI D, WANG T, PAGE M M, et al. Characterization of cytosolic glutathione peroxidase and phospholipid-hydroperoxide glutathione peroxidase genes in rainbow trout (Oncorhynchus mykiss) and their modulation by in vitro selenium exposure[J].Aquatic Toxicology,2013,130/131:97-111. [36] GHAFFARIZADEH A, SOTOUDEH E, MOZANZADEH M T, et al. Supplementing dietary selenium nano-particles increased growth, antioxidant capacity and immune-related genes transcription in Pacific whiteleg shrimp (Penaeus vannamei) juveniles[J].Aquaculture Reports,2022,25:101215. [37] WANG Y T, AHMED W, MEHMOOD S, et al. Exploring the growth performance, antioxidant capacity, and metabolism of Babylonia areolata in response to yeast selenium supplementation[J].Aquaculture Reports,2025,40:102617. [38] MAIER K J, KNIGHT A W. Ecotoxicology of selenium in freshwater systems[M] //WARE G W. Reviews of Environmental Contamination and Toxicology. New York:Springer,1994:31-48. [39] ZHANG X L, CAO J L, CHEN J J, et al. Combined effects of fluoride and dietary seleno-L-methionine at environmentally relevant concentrations on female zebrafish (Danio rerio) liver: histopathological damages, oxidative stress and inflammation[J].Biological Trace Element Research,2024,202(5):2314-2326. [40] IGHODARO O M, AKINLOYE O A. First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): their fundamental role in the entire antioxidant defence grid[J].Alexandria Journal of Medicine,2018,54(4):287-293. [41] HAO X F, LING Q F, HONG F S. Effects of dietary selenium on the pathological changes and oxidative stress in loach (Paramisgurnus dabryanus)[J].Fish Physiology and Biochemistry,2014,40(5):1313-1323. [42] HAO J Y, LIN Y, PAN W J, et al. Dietary selenium enhances the growth and anti-oxidant capacity of juvenile blunt snout bream (Megalobrama amblycephala)[J].Fish & Shellfish Immunology,2020,101:115-125. [43] GHAZI S, DIAB A M, KHALAFALLA M M, et al. Synergistic effects of selenium and zinc oxide nanoparticles on growth performance, hemato-biochemical profile, immune and oxidative stress responses, and intestinal morphometry of Nile tilapia (Oreochromis niloticus)[J].Biological Trace Element Research,2022,200(1):364-374. [44] MATOZZO V, ZAMPIERI C, MUNARI M, et al. Glyphosate affects haemocyte parameters in the clam Ruditapes philippinarum[J].Marine Environmental Research,2019,146:66-70. [45] 王洪斌,金学萍,肖龙海,等.富硒海洋小球藻对三疣梭子蟹血清中部分免疫活性酶的影响[J].湖北农业科学,2016,55(14):3687-3689. [46] KARAMZADEH M, YAHYAVI M, SALARZADEH A R, et al. Effects of dietary selenium and zinc nanoparticles on growth performance, immune responses, and antioxidant enzymes activities of white leg shrimp (Litopenaeus vannamei)[J].Iranian Journal of Fisheries Sciences,2022,21(5):1125-1140. [47] YUAN L X, ZHANG R, MA X Z, et al. Selenium accumulation, antioxidant enzyme levels, and amino acids composition in Chinese mitten crab (Eriocheir sinensis) fed selenium-biofortified corn[J].Nutrients,2018,10(3):318. [48] ZUO R T, WU X Y, WANG Z Y, et al. Effects of selenium yeast addition on the growth, intestinal health, immune status and body composition of juvenile sea cucumber Apostichopus japonicus before and after aestivation[J].Journal of Marine Science and Engineering,2023,11(3):601.