Effects of Small Peptides on Growth and Intestine Development of Larval Large Yellow Croaker (Larimichthys crocea) and Its Anti-Oxidative Stress Effect under Low-Temperature Stress
LI Wencheng1,2, ZHAO Xumin3, ZHANG Yanjun3, SONG Wei1,2,4, ZENG Lin1, ZHANG Hui1, ZHAO Xiangjiong1
1. National Engineering Research Center of Marine Facilities Aquaculture, Zhejiang Ocean University, Zhoushan 316000, China;
2. East China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Shanghai 200090, China;
3. Zhejiang Huatai Biological Technology Co., Ltd., Yiwu 322005, China;
4. Pilot National Laboratory for Marine Science and Technology(Qingdao), Qingdao 266237, China
Abstract：This experiment included two parts: growth trial and low-temperature stress trial. Larval large yellow croakers (Larimichthys crocea) were fed rotifers and Artemia nauplii fortified with different concentrations (0, 0.5, 1.0, 2.0 and 3.0 mL/m3) of small peptides for 12 d, which aimed to evaluate the effects of small peptides on growth and intestine development of larval large yellow croaker. Then, larval large yellow croakers were exposed to low-temperature environment (at 12 ℃) for 24 h, which aimed to evaluate the antioxidant ability and non-specific immunity of larvae large yellow croaker under low-temperature stress. The results showed that different concentrations of small peptides significantly increased the contents of essential amino acids and total amino acids of rotifers and Artemia nauplii. Fish fed rotifers and Artemia nauplii fortified with small peptides significantly increased body length, villi height, villi number and tissue area (P<0.05). Small peptides significantly reduced oxygen species (ROS) content (P<0.05), and significantly increased GSH content and the expression levels of liver antioxidant-related genes [copper-zinc superoxide dismutase (Cu/Zn-SOD and manganese superoxide dismutase (Mn-SOD), catalase (CAT), glutathione peroxidase-1a (GPx-1a), glutathione peroxidase-1b (GPx-1b) and glutathione reductase (GR)] and non-specific immune-related genes [c-type lysozyme (c-type LZM), g-type lysozyme (g-type LZM) and alkaline phophatase (AKP)] when fish exposed to low temperature (P<0.05). Nuclear transcription factors NF-E2-related nuclear factor 2 (Nrf2) and nuclear transcription factor-κB (NF-κB)] gene expression levels were significantly positively correlated with the expression levels of antioxidant enzyme genes and immune enzyme genes (P<0.05), and both of them were significantly negatively correlated with ROS content (P<0.05). In conclusion, small peptides can increase the nutritional value of rotifers and Artemia nauplii, and improve the growth and intestine development of larval large yellow croaker; small peptides can increase the expression levels of antioxidant enzyme genes and immune enzyme genes by inducing the expression of Nrf2 and NF-κB genes, and ameliorate the oxidative damage of large yellow croaker larvae induced by low-temperature stress.
李文成, 赵旭民, 张延军, 宋炜, 曾霖, 张惠, 赵向炯. 小肽对大黄鱼仔鱼生长和小肠发育的影响及其在低温胁迫下的抗氧化应激效应[J]. 动物营养学报, 2021, 33(1): 572-583.
LI Wencheng, ZHAO Xumin, ZHANG Yanjun, SONG Wei, ZENG Lin, ZHANG Hui, ZHAO Xiangjiong. Effects of Small Peptides on Growth and Intestine Development of Larval Large Yellow Croaker (Larimichthys crocea) and Its Anti-Oxidative Stress Effect under Low-Temperature Stress. Chinese Journal of Animal Nutrition, 2021, 33(1): 572-583.
WU C W,ZHANG D,KAN M Y,et al.The draft genome of the large yellow croaker reveals well-developed innate immunity[J].Nature Communications,2014,5:5227.
[21]
REGOLI F,GIULIANI M E.Oxidative pathways of chemical toxicity and oxidative stress biomarkers in marine organisms[J].Marine Environmental Research,2014,93:106-117.
[10]
JIA R,DU J L,CAO L P,et al.Antioxidative,inflammatory and immune responses in hydrogen peroxide-induced liver injury of tilapia (GIFT,Oreochromis niloticus)[J].Fish & Shellfish Immunology,2019,84:894-905.
[30]
TACCHI L,BICKERDIKE R,DOUGLAS A,et al.Transcriptomic responses to functional feeds in Atlantic salmon (Salmo salar)[J].Fish & Shellfish Immunology,2011,31(5):704-715.
[2]
刘家富.大黄鱼养殖与生物学[M].厦门:厦门大学出版社,2013:1-6. LIU J F.Culture and biology of large yellow croaker[M].Xiamen:Xiamen University Press,2013:1-6.(in Chinese)
[7]
HALLIWELL B.Free radicals and antioxidants:updating a personal view[J].Nutrition Reviews,2012,70(5):257-265.
[12]
NAPETSCHNIG J,WU H.Molecular basis of NF-κB signaling[J].Annual Review of Biophysics,2013,42:443-468.
[5]
LUSHCHAK V I.Environmentally induced oxidative stress in aquatic animals[J].Aquatic Toxicology,2011,101(1):13-30.
[3]
LIU C,SHEN W L,HOU C C,et al.Low temperature-induced variation in plasma biochemical indices and aquaglyceroporin gene expression in the large yellow croaker Larimichthys crocea[J].Scientific Reports,2019,9(1):2717.
[8]
SRIKANTH K,PEREIRA E,DUARTE A C,et al.Glutathione and its dependent enzymes' modulatory responses to toxic metals and metalloids in fish-a review[J].Environmental Science and Pollution Research,2013,20(4):2133-2149.
[13]
SHEN W L,MATSUI T.Intestinal absorption of small peptides:a review[J].International Journal of Food Science & Technology,2019,54(6):1942-1948.
[18]
ZENG L,ZHENG J L,WANG Y H,et al.The role of Nrf2/Keap1 signaling in inorganic mercury induced oxidative stress in the liver of large yellow croaker Pseudosciaena crocea[J].Ecotoxicology and Environmental Safety,2016,132:345-352.
[23]
王际英,姜柯君,夏斌,等.小肽对星斑川鲽幼鱼消化酶活性、抗氧化能力和生化组成的影响[J].中国水产科学,2014,21(6):1154-1164. WANG J Y,JIANG K J,XIA B,et al.Effects of small dietary peptides on digestive enzyme activity,antioxidative capability,and biochemical composition in tissues of juvenile starry flounder Platichthys stellatus[J].Journal of Fishery Sciences of China,2014,21(6):1154-1164.(in Chinese)
[1]
AO J Q,MU Y N,XIANG L X,et al.Genome sequencing of the perciform fish Larimichthys crocea provides insights into molecular and genetic mechanisms of stress adaptation[J].PLoS Genetics,2015,11(4):e1005118.
[4]
YE C X,WAN F,SUN Z Z,et al.Effect of phosphorus supplementation on cell viability,anti-oxidative capacity and comparative proteomic profiles of puffer fish (Takifugu obscurus) under low temperature stress[J].Aquaculture,2016,452:200-208..
[6]
BANH S,WIENS L,SOTIRI E,et al.Mitochondrial reactive oxygen species production by fish muscle mitochondria:potential role in acute heat-induced oxidative stress[J].Comparative Biochemistry and Physiology,Part B:Biochemistry and Molecular Biology,2016,191:99-107.
[11]
SANT K E,HANSEN J M,WILLIAMS L M,et al.The role of Nrf1 and Nrf2 in the regulation of glutathione and redox dynamics in the developing zebrafish embryo[J].Redox Biology,2017,13:207-218.
[14]
LEÓN R,RUIZ M,VALERO Y,et al.Exploring small cationic peptides of different origin as potential antimicrobial agents in aquaculture[J].Fish & Shellfish Immunology,2020,98:720-727.
[16]
李日美,申光荣,黄放,等.小肽对凡纳滨对虾幼虾生长、体成分、非特异性免疫力及抗病力的影响[J].动物营养学报,2018,30(8):3082-3090. LI R M,SHEN G R,HUANG F,et al.Effects of small peptides on growth,body composition,non-specific immunity and disease resistance of juvenile Litopenaeus vannamei[J].Chinese Journal of Animal Nutrition,2018,30(8):3082-3090.(in Chinese)
[24]
UMENO A,BIJU V,YOSHIDA Y.In vivo ROS production and use of oxidative stress-derived biomarkers to detect the onset of diseases such as Alzheimer's disease,Parkinson's disease,and diabetes[J].Free Radical Research,2017,51(4):413-427.
WANG T,CHENG Y,CHEN X,et al.Effects of small peptides,probiotics,prebiotics,and synbiotics on growth performance,digestive enzymes,and oxidative stress in orange-spotted grouper,Epinephelus coioides,juveniles reared in artificial seawater[J].Chinese Journal of Oceanology and Limnology,2017,35(1):89-97.
[17]
ZENG L,AI C X,ZHENG J L,et al.Cu pre-exposure alters antioxidant defense and energy metabolism in large yellow croaker Larimichthys crocea in response to severe hypoxia[J].Science of the Total Environment,2019,687:702-711.
[19]
ZENG L,AI C X,ZHANG J S,et al.Pre-hypoxia exposure inhibited copper toxicity by improving energy metabolism,antioxidant defence and mitophagy in the liver of the large yellow croaker Larimichthys crocea[J].Science of the Total Environment,2020,708:134961.
[22]
李杰.日粮中大豆蛋白小肽添加水平对虹鳟生产性能、消化及免疫功能的影响[D].硕士学位论文.雅安:四川农业大学,2017:16-29. LI J.Effects of dietary small peptides levels on growth performance,muscle quality,physiological and biochemical indexes in juvenile starry flounder (Platichthys stellatus)[D].Master's Thesis.Ya'an:Sichuan Agricultural University,2017:16-29. in Chinese)
[25]
ZENG L,AI C X,WANG Y H,et al.Abrupt salinity stress induces oxidative stress via the Nrf2-Keap1 signaling pathway in large yellow croaker Pseudosciaena crocea[J].Fish Physiology and Biochemistry,2017,43(4):955-964.
[27]
ZENG L,AI C X,ZHANG J S,et al.Essential element Cu and non-essential element Hg exposures have different toxicological effects in the liver of large yellow croaker[J].Marine Pollution Bulletin,2019,139:6-13.
[29]
MONTEIRO D A,RANTIN F T,KALININ A L.Inorganic mercury exposure:toxicological effects,oxidative stress biomarkers and bioaccumulation in the tropical freshwater fish matrinxã,Brycon amazonicus (Spix and Agassiz,1829)[J].Ecotoxicology,2010,19:105-123.
[32]
DODSON M,REDMANN M,RAJASEKARAN N S,et al.KEAP1-NRF2 signalling and autophagy in protection against oxidative and reductive proteotoxicity[J].Biochemical Journal,2015,469(3):347-355.
[26]
ZENG L,AI C X,ZHANG J S,et al.Toxicological effects of waterborne Zn on the proximal and distal intestines of large yellow croaker Larimichthys crocea[J].Ecotoxicology and Environmental Safety,2019,174:324-333.
[28]
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.
[31]
OLSEN R E,MYKLEBUST R,KRYVI H,et al.Damaging effect of dietary inulin on intestinal enterocytes in Arctic charr (Salvelinus alpinus L.)[J].Aquaculture Research,2011,32(11):931-934.
[33]
WANG Y T,MANDAL A K,SON Y O,et al.Roles of ROS,Nrf2,and autophagy in cadmium-carcinogenesis and its prevention by sulforaphane[J].Toxicology and Applied Pharmacology,2018,353:23-30.
[34]
DOS-SANTOS-PEREIRA M,GUIMARÃES F S,DEL-BEL E,et al.Cannabidiol prevents LPS-induced microglial inflammation by inhibiting ROS/NF-κB-dependent signaling and glucose consumption[J].Glia,2020,68(3):561-573.
