Metabolomic Effects of Biofloc Technology on Ovarian Development inPengze Crucian Carp Carassius auratus var. Pengze
ZHONG Jiahui1,2, ZHANG Yanping1,2, CUI Jiaqin3, WU Zijun1,2, QUE Xiangyao1,2, YU Jianfang1,2, DING Liyun1, ZHANG Guifang1, LUO Guozhi3, ZHANG Haixin1,2
1. Jiangxi Fisheries Research Institute, Nanchang 330039, China; 2. Fishery Resources Ecological EnvironmentMonitoring Center of Jiangxi Province, Nanchang 330039, China; 3. Shanghai Engineering Research Center ofAquaculture, Shanghai Ocean University, Shanghai 201306, China
Abstract：In order to explore the effects of biofloc technology on ovarian development of Pengze crucian carp Carassius auratus var. Pengze, female Pengze crucian carp with body weight of (56.67±0.38) g were reared in a circular culture buckets with a diameter of 0.8 m, a depth of 0.65 m, and with biofloc containing C/N of 15, total suspended solids (TSS) of 5000 mg/L, and 0 mg/L of nitrous nitrogen and total ammonia nitrogen at water temperature of 25—32 ℃. The Pengze crucian carp was exposed to the bioflocs at concentrations of 0 mg/L (control group), 200 mg/L (200 mg/L group), and 400 mg/ L (400 mg/L group) and 600 mg/L (600 mg/L group) for 56 days. During the feeding trail, glucose was added to the culture buckets to ensure the C/N of 15. At the end of the feeding, the fish body indices, reproductive performance and serum biochemical indices were measured in each group, and the composition and content of metabolites in ovarian tissue were analyzed by liquid chromatography combined with mass spectrometry (LC-MS) non-targeted metabolomics technology, and significant altered metabolites were identified by multivariate statistical analysis to analyze the enrichment of metabolic pathways. The results showed that there were 35.90% higher hepatosomatic index, 6.88% higher visceral index, and 6.89% higher condition factor in the control group than those in the 600 mg/L group (P<0.05). A descending order of gonadosomatic index, absolute fecundity, relative fecundity, and egg diameter was described as control group> 200 mg/L group > 400 mg/L group > 600 mg/L group. Histological analysis revealed that the ovarian was predominantly developed into stage Ⅳ in the control group, whereas ovaries were dominated by stages Ⅰ and Ⅱ in the 600 mg/L group. Serum biochemical analysis demonstrated that the contents of estradiol, triglyceride, and total cholesterol were showed to be 10.37%, 3.74%, and 15.11% lower than those in the control group and in the 600 mg/L group, respectively (P<0.05). A total of 107 significantly differential metabolites (VIP>1, P<0.05) was observed in ovarian tissues in the 600 mg/L group relative to the control group by metabolomic analysis, primarily including amino acid/peptide analogs, fatty acids, glycerophospholipids, and steroids/derivatives. These metabolites were found to be enriched in 37 downregulated pathways, among which the pathways closely related to reproductive regulation were involved in gonadotropin-releasing hormone, estrogen signaling pathway, arginine and proline metabolism, neuroactive ligand-receptor interaction, β-alanine metabolism, and glycerophospholipid metabolism. The findings indicate that biofloc aquaculture, particularly at a TSS concentration of 600 mg/L, exerts inhibitory effects on ovarian development in Pengze crucian carp, forming a synergistic inhibitory effect by down-regulating the expression of pathways including GnRH secretion, estrogen signaling pathway, amino acid metabolism, and lipid metabolism.
[1] XIAO J, LONG F, DING L Y, et al. Effects of three different protein levels on the growth, gonad development, and physiological biochemistry of female Pengze crucian carp (Carassius auratus var. Pengze) broodstock[J]. Frontiers in Marine Science,2024,11:1459412. [2] 王学耕,吴碧瑜,陈前辉,等.彭泽鲫种质特性与品种改良研究进展及展望[J].水产学报,2025,49(3):4-21. [3] 丁立云,陈文静,付辉云.彭泽鲫饲料营养与健康养殖技术[M].南昌:江西科学技术出版社,2024. [4] 李萍.生物絮团的营养价值及其在水产养殖中的研究进展[J].中国饲料,2024(18):1-4. [5] KHANJANI M H, MOZANZADEH M T, SHARIFINIA M, et al. Broodstock and seed production in biofloc technology (BFT):an updated review focused on fish and penaeid shrimp[J]. Aquaculture,2024,579:740278. [6] 赵志刚,罗亮,王常安,等.不同鲤养殖模式生物絮团系统中鱼体的生长及水质[J].水产学报,2017,41(1):99-108. [7] SOAUDY M R, GHONIMY A, GRECO L S L, et al. Total suspended solids and their impact in a biofloc system:current and potentially new management strategies[J]. Aquaculture,2023,572:739524. [8] 崔佳勤.生物絮团养殖过程中C/N、磷酸盐浓度和硝酸盐浓度对土腥味物质产生的影响[D].上海:上海海洋大学,2023. [9] 于哲,吴莉芳,代忠义,等.不同C/N水平生物絮团对黄金鲫生长性能、消化酶活力及养殖水体水质的影响[J].饲料工业,2019(22):40-47. [10] 张明明,徐晨,赵志刚,等.生物絮团技术对异育银鲫生长性能和抗性的影响[J].中国水产科学,2017,24(3):533-542. [11] EKASARI J, SUPRAYUDI M A, WIYOTO W, et al. Biofloc technology application in African catfish fingerling production:the effects on the reproductive performance of broodstock and the quality of eggs and larvae[J]. Aquaculture,2016,464:349-356. [12] MAGAÑA-GALLEGOS E, ARÉVALO M, CUZON G, et al. Effects of using the biofloc system and eyestalk ablation on reproductive performance and egg quality of Litopenaeus vannamei (Boone,1931) (Decapoda:Dendrobranchiata:Penaeidae)[J]. Animal Reproduction Science,2021,228:106749. [13] LI J S, SONG M, WEN H S, et al. Gonadal lipidomics profile of an ovoviviparity teleost, black rockfish, during gonadal development[J]. Fish Physiology and Biochemistry,2021,47(4):811-828. [14] LADISA C, MA Y F, HABIBI H R. Metabolic changes during growth and reproductive phases in the liver of female goldfish (Carassius auratus)[J]. Frontiers in Cell and Developmental Biology, 2022,10:834688. [15] MENG L J, HU X, WEN B, et al. Microplastics inhibit biofloc formation and alter microbial community composition and nitrogen transformation function in aquaculture[J]. Science of the Total Environment,2023,866:161362. [16] 国家环境保护总局,水和废水监测分析方法编委会编.水和废水监测分析方法[M].4版.北京:中国环境科学出版社,2002. [17] 赵玉柱,陈张帆,马腾,等.斑石鲷性腺发育的组织学观察与初步分析[J].上海海洋大学学报,2021,30(4):675-683. [18] 崔庆奎,沈志刚,田宇,等.大口黑鲈的卵巢发育周年变化及反季节繁殖研究[J].水生生物学报,2021,45(1):76-88. [19] EMERENCIANO M, CUZON G, PAREDES A, et al. Evaluation of biofloc technology in pink shrimp Farfantepenaeus duorarum culture:growth performance, water quality, microorganisms profile and proximate analysis of biofloc[J]. Aquaculture International,2013,21(6):1381-1394. [20] 肖俊,姚远,丁立云,等.不同脂肪源对彭泽鲫亲本生长性能、卵巢脂肪酸组成、性腺发育以及血清生化和抗氧化指标的影响[J].动物营养学报,2024,36(10):6599-6610. [21] STUART K R, ARMBRUSTER L, JOHNSON R, et al. Egg diameter as a predictor for egg quality of California yellowtail (Seriola dorsalis)[J]. Aquaculture,2020,522:735154. [22] 王腾飞,张鼎元,郭春阳,等.养殖银鲳性腺发育规律和性类固醇激素变化[J].水产学报,2017,41(2):198-211. [23] 李亚宁,陈敏,刘洋,等.饲料中小麦胚芽对黄颡鱼雌性亲鱼繁殖性能的影响[J].水生生物学报,2024,48(2):264-274. [24] YU J, LI D Y, ZHU J L, et al. Effects of different oxytocin and temperature on reproductive activity in Nile tilapia (Oreochromis niloticus):based on sex steroid hormone and GtHR gene expression[J]. Fishes,2022,7(6):316. [25] 史存卓,程学文,刘鹰,等.光照周期对红鳍东方鲀雌鱼繁殖调控的初步研究[J].海洋科学,2023,47(4):137-144. [26] 肖俊,龙凡,丁立云,等.维生素E对彭泽鲫亲本生长、繁殖及免疫力的影响[J].中国水产科学,2024,31(11):1387-1398. [27] 孙艳秋,刘鉴毅,庄平,等.温度、盐度和pH对多纹钱蝶鱼胚胎发育的影响[J].南方水产科学,2021,17(6):122-129. [28] CARDONA E, LORGEOUX B, CHIM L, et al. Biofloc contribution to antioxidant defence status, lipid nutrition and reproductive performance of broodstock of the shrimp Litopenaeus stylirostris:consequences for the quality of eggs and larvae[J]. Aquaculture,2016,452:252-262. [29] SHARMA P, PUROHIT S, KOTHIYAL S, et al. Germ cell development in teleost gonads[J]. Aquaculture and Fisheries,2024,9(3):422-436. [30] MILLAR R P, LU Z L, PAWSON A J, et al. Gonadotropin-releasing hormone receptors[J]. Endocrine Reviews,2004,25(2):235-275. [31] WELTZIEN F A, ANDERSSON E, ANDERSEN Ø, et al. The brain-pituitary-gonad axis in male teleosts, with special emphasis on flatfish (Pleuronectiformes)[J]. Comparative Biochemistry and Physiology Part A:Molecular & Integrative Physiology,2004,137(3):447-477. [32] LEVAVI-SIVAN B, BOGERD J, MAÑANÓS E L, et al. Perspectives on fish gonadotropins and their receptors[J]. General and Comparative Endocrinology,2010,165(3):412-437. [33] 张效宇,贾玉东,陈丽梅.鱼类促性腺激素研究进展[J].农业科学,2024(10):1094-1101. [34] ZOHAR Y, MUÑOZ-CUETO J A, ELIZUR A, et al. Neuroendocrinology of reproduction in teleost fish[J]. General and Comparative Endocrinology,2010,165(3):438-455. [35] 艾庆辉,严晶,麦康森.鱼类脂肪与脂肪酸的转运及调控研究进展[J].水生生物学报,2016,40(4):859-868. [36] 张硕,孔杰,曹家旺,等.凡纳滨对虾(Litopenaeus vannamei)不同产卵频次雌虾卵巢比较代谢组学分析[J].海洋与湖沼,2024,55(6):1522-1531. [37] 朱艳红.中华鲟卵巢发育Ⅱ——Ⅳ期养分沉积、机体代谢响应及相关机制研究[D].武汉:华中农业大学,2020. [38] SEILIEZ I, GABILLARD J C, SKIBA-CASSY S, et al. An in vivo and in vitro assessment of TOR signaling cascade in rainbow trout (Oncorhynchus mykiss)[J]. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology,2008,295(1):R329-R335. [39] SINCLAIR K, LUNN L, KWONG W, et al. Amino acid and fatty acid composition of follicular fluid as predictors of in-vitro embryo development[J]. Reproductive BioMedicine Online,2008,16(6):859-868. [40] MATOBA S, BENDER K, FAHEY A G, et al. Predictive value of bovine follicular components as markers of oocyte developmental potential[J]. Reproduction, Fertility, and Development,2014,26(2):337-345. [41] 李禹韬,王若愚,马波,等.杂交鲟(达氏鳇♀×施氏鲟♂)不同繁殖力群体间卵巢代谢组分析[J].中国水产科学,2025,32(2):139-149. [42] ZHU T T, HE Y, CAO H Q, et al. Insights into lipid function for ovarian development in the swimming crab (Portunus trituberculatus):a comparison of lipid mobilization and deposition in hepatopancreas and ovary[J]. Aquaculture Reports,2024,38:102326. [43] 刘权迪,宁延昶,温斌,等.饲料中脂肪水平对海湾扇贝性腺发育、脂肪酸组成和组织结构的影响[J].上海海洋大学学报,2021,30(6):981-991. [44] 何先达,钟文杰,余金达,等.拟穴青蟹不同卵巢发育时期各组织的脂肪酸组成[J].汕头大学学报(自然科学版),2022,37(4):41-50. [45] SUI L Y, WU X G, WILLE M, et al. Effect of dietary soybean lecithin on reproductive performance of Chinese mitten crab Eriocheir sinensis (H. Milne-Edwards) Broodstock[J]. Aquaculture International,2009,17(1):45-56. [46] WEI F, YUE H F, WANG B J, et al. Endocrine disrupting effects of parabens in zebrafish (Danio rerio):new insights from transcriptomics, metabolomics, and molecular dynamics simulation[J]. Chemosphere,2024,354:141682. [47] SONG Y L, TAO B B, CHEN J, et al. GABAergic neurons and their modulatory effects on GnRH3 in zebrafish[J]. Endocrinology,2017,158(4):874-886. [48] CHANG J P, PEMBERTON J G. Comparative aspects of GnRH-stimulated signal transduction in the vertebrate pituitary-contributions from teleost model systems[J]. Molecular and Cellular Endocrinology, 2018,463:142-167. [49] VIDAL B, PASQUALINI C, LE BELLE N, et al. Dopamine inhibits luteinizing hormone synthesis and release in the juvenile European eel:a neuroendocrine lock for the onset of puberty[J]. Biology of Reproduction,2004,71(5):1491-1500. [50] GISSIS A, LEVAVI S B, RUBIN K H, et al. The effect of gonadotropin releasing hormone superactive analog and dopamine antagonists on gonadotropin level and ovulation in tilapia hybrids[J]. 1991,43(4):123-136. [51] MA Y F, LADISA C, CHANG J P, et al. Seasonal related multifactorial control of pituitary gonadotropin and growth hormone in female goldfish:influences of neuropeptides and thyroid hormone[J]. Frontiers in Endocrinology,2020,11:175. [52] 陈华谱.卵形鲳鲹生物学及繁养殖技术研究进展[J].大连海洋大学学报,2025,40(1):1-11.
2026, Vol. 45 
