Skip to main content Accessibility help
×
Home

Inulin alleviates adverse metabolic syndrome and regulates intestinal microbiota composition in Nile tilapia (Oreochromis niloticus) fed with high-carbohydrate diet

  • Tong Wang (a1), Ning Zhang (a1), Xiao-Bo Yu (a1), Fang Qiao (a1), Li-Qiao Chen (a1), Zhen-Yu Du (a1) and Mei-Ling Zhang (a1)...

Abstract

A high-carbohydrate diet could achieve a protein-sparing effect, but it may cause negative impacts on the growth condition of fish due to their poor utilisation ability of carbohydrate. How to reduce the adverse effects caused by a high-carbohydrate diet is important for the development of aquaculture. In the present study, we aimed to identify whether inulin could attenuate the metabolic syndrome caused by a high-carbohydrate diet in fish. Nile tilapia (Oreochromis niloticus) (1·19 (sd 0·01) g) were supplied with 35 % carbohydrate (CON), 45 % carbohydrate (HC) and 45 % carbohydrate + 5 g/kg inulin (HCI) diets for 10 weeks. The results showed that addition of inulin improved the survival rate when fish were challenged with Aeromonas hydrophila, indicating that inulin had an immunostimulatory effect. Compared with the HC group, the HCI group had lower lipid accumulation in liver and the gene expression analyses indicated that addition of inulin down-regulated genes related to lipogenesis and up-regulated genes relevant to β-oxidation significantly (P < 0·05). Higher liver glycogen and glucose tolerance were found in the HCI group compared with the HC group (P < 0·05). These results indicated that inulin could alleviate the metabolic syndrome induced by a high-carbohydrate diet. Furthermore, addition of inulin to a high-carbohydrate diet changed the intestinal bacterial composition and significantly increased the concentration of acetic acid and propionic acid in fish gut which have the potential to increase pathogen resistance and regulate metabolic characteristics in fish. Collectively, our results demonstrated a possible causal role for the gut microbiome in metabolic improvements induced by inulin in fish.

Copyright

Corresponding author

*Corresponding author: Mei-Ling Zhang, fax +86 21 54345354, email mlzhang@bio.ecnu.cn

References

Hide All
1. Lin, SM, Shi, CM, Mu, MM, et al. (2018) Effect of high dietary starch levels on growth, hepatic glucose metabolism, oxidative status and immune response of juvenile largemouth bass, Micropterus salmoides . Fish Shellfish Immunol 78, 121126.
2. Zhou, C, Ge, X, Lin, H, et al. (2014) Effect of dietary carbohydrate on non-specific immune response, hepatic antioxidative abilities and disease resistance of juvenile golden pompano (Trachinotus ovatus). Fish Shellfish Immunol 41, 183190.
3. Shiau, S-Y & Peng, C-Y (1993) Protein-sparing effect by carbohydrates in diets for tilapia, Oreochromis niloticus × O. aureus . Aquaculture 117, 327334.
4. Li, XF, Liu, WB, Lu, KL, et al. (2012) Dietary carbohydrate/lipid ratios affect stress, oxidative status and non-specific immune responses of fingerling blunt snout bream, Megalobrama amblycephala . Fish Shellfish Immunol 33, 316323.
5. Li, M, Hu, FC, Qiao, F, et al. (2020) Sodium acetate alleviated high-carbohydrate induced intestinal inflammation by suppressing MAPK and NF-κB signaling pathways in Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol 98, 758765.
6. Tan, Q, Wang, F, Xie, S, et al. (2009) Effect of high dietary starch levels on the growth performance, blood chemistry and body composition of gibel carp (Carassius auratus var. gibelio). Aqua Res 40, 10111018.
7. Boonanuntanasarn, S, Jangprai, A, Kumkhong, S, et al. (2018) Adaptation of Nile tilapia (Oreochromis niloticus) to different levels of dietary carbohydrates: New insights from a long term nutritional study. Aquaculture 496, 5865.
8. Felip, O, Ibarz, A, Fernández-Borràs, J, et al. (2012) Tracing metabolic routes of dietary carbohydrate and protein in rainbow trout (Oncorhynchus mykiss) using stable isotopes ([13C]starch and [15N]protein): effects of gelatinisation of starches and sustained swimming. Br J Nutr 107, 834844.
9. Gou, S, Chen, N, Xiangtai, XU, et al. (2015) Effects of dietary digestible starch levels on growth performance, body composition, and non- specific immunological index of largemouth bass (Micropterus salmoides). J Fish China 39, 14991510.
10. Kumar, S, Sahu, NP, Pal, AK, et al. (2005) Effect of dietary carbohydrate on haematology, respiratory burst activity and histological changes in L. rohita juveniles. Fish Shellfish Immunol 19, 0344.
11. Guo, JL, Kuang, WM, Zhong, YF, et al. (2020) Effects of supplemental dietary bile acids on growth, liver function and immunity of juvenile largemouth bass (Micropterus salmoides) fed high-starch diet. Fish Shellfish Immunol 97, 602607.
12. Yu, H, Zhang, L, Chen, P, et al. (2019) Dietary bile acids enhance growth, and alleviate hepatic fibrosis induced by a high starch diet via AKT/FOXO1 and cAMP/AMPK/SREBP1 pathway in Micropterus salmoides . Front Physiol 10, 1430.
13. Ganguly, S, Dora, KC, Sarkar, S, et al. (2012) Supplementation of prebiotics in fish feed: a review. Rev Fish Biol Fisheries 23, 195199.
14. Gibson, GR, Hutkins, R, Sanders, ME, et al. (2017) Expert consensus document: the International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastro Hepat 14, 491502.
15. Ringø, E, Dimitroglou, A, Hoseinifar, SH, et al. (2014) Prebiotics in finfish: an update. In Aquaculture Nutrition: Gut Health, Probiotics and Prebiotics, pp. 360400 [D Merrifield and E Ringø, editors]. Chichester: John Wiley & Sons, Ltd.
16. Tiengtam, N, Khempaka, S, Paengkoum, P, et al. (2015) Effects of inulin and Jerusalem artichoke (Helianthus tuberosus) as prebiotic ingredients in the diet of juvenile Nile tilapia (Oreochromis niloticus). Anim Feed Sci Tech 207, 120129.
17. Tiengtam, N, Paengkoum, P, Sirivoharn, S, et al. (2017) The effects of dietary inulin and Jerusalem artichoke (Helianthus tuberosus) tuber on the growth performance, haematological, blood chemical and immune parameters of Nile tilapia (Oreochromis niloticus) fingerlings. Aquac Res 48, 52805288.
18. Zhang, Q, Yu, H, Xiao, X, et al. (2018) Inulin-type fructan improves diabetic phenotype and gut microbiota profiles in rats. Peer J 6, e4446.
19. Dewulf, EM, Cani, PD, Neyrinck, AM, et al. (2011) Inulin-type fructans with prebiotic properties counteract GPR43 overexpression and PPARγ-related adipogenesis in the white adipose tissue of high-fat diet-fed mice. J Nutr Biochem 22, 712722.
20. Kostic, AD, Howitt, MR & Garrett, WS (2013) Exploring host–microbiota interactions in animal models and humans. Genes Dev 27, 701718.
21. He, AY, Ning, LJ, Chen, LQ, et al. (2015) Systemic adaptation of lipid metabolism in response to low- and high-fat diet in Nile tilapia (Oreochromis niloticus). Physiol Rep 3, e12485.
22. Liu, CZ, He, AY, Ning, LJ, et al. (2018) Leptin selectively regulates nutrients metabolism in Nile tilapia fed on high carbohydrate or high fat diet. Front Endocrinol 9, 574.
23. Bligh, EG & Dyer, WJ (1959) A rapid method of total lipid extraction and purification. Can Journal Biochem Physiol 37, 911917.
24. Livak, KJ & Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT Method. Methods 25, 402408.
25. Caporaso, JG, Kuczynski, J, Stombaugh, J, et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Met 7, 335336.
26. Mo, WY, Cheng, Z, Choi, WM, et al. (2015) Use of food waste as fish feeds: effects of prebiotic fibers (inulin and mannanoligosaccharide) on growth and non-specific immunity of grass carp (Ctenopharyngodon idella). Environ Sci Pollut Res Int 22, 1766317671.
27. Ortiz, LT, Rebole, A, Velasco, S, et al. (2013) Effects of inulin and fructooligosaccharides on growth performance, body chemical composition and intestinal microbiota of farmed rainbow trout (Oncorhynchus mykiss). Aquacult Nutr 19, 475482.
28. Ibrahem, MD, Fathi, M, Mesalhy, S, et al. (2010) Effect of dietary supplementation of inulin and vitamin C on the growth, hematology, innate immunity, and resistance of Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol 29, 241246.
29. Reza, A, Abdolmajid, H, Abbas, M, et al. (2009) Effect of dietary prebiotic inulin on growth performance, intestinal microflora, body composition and hematological parameters of Juvenile Beluga, Huso huso (Linnaeus, 1758). J World Aquacult Soc 40, 771779.
30. Eshaghzadeh, H, Hoseinifar, SH, Vahabzadeh, H, et al. (2015) The effects of dietary inulin on growth performances, survival and digestive enzyme activities of common carp (Cyprinus carpio) fry. Aquacult Nutr 21, 242247.
31. Hoseinifar, SH, Ahmadi, A, Raeisi, M, et al. (2017) Comparative study on immunomodulatory and growth enhancing effects of three prebiotics (galactooligosaccharide, fructooligosaccharide and inulin) in common carp (Cyprinus carpio). Aquac Res 48, 32983307.
32. Hoseinifar, SH, Zare, P & Merrifield, DL (2010) The effects of inulin on growth factors and survival of the Indian white shrimp larvae and postlarvae (Fenneropenaeus indicus). Aquac Res 41, e348e352.
33. Li, Y, Liu, H, Dai, X, et al. (2018) Effects of dietary inulin and mannan oligosaccharide on immune related genes expression and disease resistance of Pacific white shrimp, Litopenaeus vannamei . Fish Shellfish Immunol 76, 7892.
34. Sheikholeslami, M, Yusefian, M, Yavari, V, et al. (2007) Modulation of rainbow trout immune system and enhance resistance against streptococcosis using dietary inulin. In The First National Conference on Caspian Sea Fisheries Resources, p. 12, Iran: Gorgan University.
35. Valcheva, R, Koleva, P, Martinez, I, et al. (2019) Inulin-type fructans improve active ulcerative colitis associated with microbiota changes and increased short-chain fatty acids levels. Gut Microbes 10, 334357.
36. Hoseinifar, SH, Zoheiri, F & Caipang, CM (2016) Dietary sodium propionate improved performance, mucosal and humoral immune responses in Caspian white fish (Rutilus frisii kutum) fry. Fish Shellfish Immunol 55, 523528.
37. Zhang, W, Liu, K, Tan, B, et al. (2019) Transcriptome, enzyme activity and histopathology analysis reveal the effects of dietary carbohydrate on glycometabolism in juvenile largemouth bass, Micropterus salmoides . Aquaculture 504, 3951.
38. Kamalam, BS, Medale, F & Panserat, S (2017) Utilisation of dietary carbohydrates in farmed fishes: new insights on influencing factors, biological limitations and future strategies. Aquaculture 467, 327.
39. Weitkunat, K, Stuhlmann, C, Postel, A, et al. (2017) Short-chain fatty acids and inulin, but not guar gum, prevent diet-induced obesity and insulin resistance through differential mechanisms in mice. Sci Rep 7, 6109.
40. Sugatani, J, Sadamitsu, S, Tadashi, W, et al. (2012) Effects of dietary inulin, statin, and their co-treatment on hyperlipidemia, hepatic steatosis and changes in drug-metabolizing enzymes in rats fed a high-fat and high-sucrose diet. Nutr Metab 9, 23.
41. Brennan, CA & Garrett, WS (2019) Fusobacterium nucleatum-symbiont, opportunist and oncobacterium. Nat Rev Microbiol 17, 156166.
42. Edwards, KJ, Logan, JMJ & Gharbia, SE (2015) Cetobacterium. In Bergey’s Manual of Systematics of Archaea and Bacteria. Wiley Online Library. doi: 10.1002/9781118960608.gbm00767.
43. Ortiz-Estrada, ÁM, Gollas-Galván, T, Martínez-Córdova, LR, et al. (2019) Predictive functional profiles using metagenomic 16S rRNA data: a novel approach to understanding the microbial ecology of aquaculture systems. Rev Aquacult 11, 234245.
44. Rezasoltani, S, Ahmadi Bashirzadeh, D, Nazemalhosseini Mojarad, E, et al. (2020) Signature of gut microbiome by conventional and advanced analysis techniques: advantages and disadvantages. Middle East J Dig Dis 12, 511.
45. Geraylou, Z, Souffreau, C, Rurangwa, E, et al. (2012) Effects of arabinoxylan-oligosaccharides (AXOS) on juvenile Siberian sturgeon (Acipenser baerii) performance, immune responses and gastrointestinal microbial community. Fish Shellfish Immunol 33, 718724.
46. Chen, WW, Romano, N, Ebrahimi, M, et al. (2017) The effects of dietary fructooligosaccharide on growth, intestinal short chain fatty acids level and hepatopancreatic condition of the giant freshwater prawn (Macrobrachium rosenbergii) post-larvae. Aquaculture 469, 95101.
47. Safari, R, Hoseinifar, SH & Kavandi, M (2016) Modulation of antioxidant defense and immune response in zebra fish (Danio rerio) using dietary sodium propionate. Fish Physiol Biochem 42, 17331739.
48. Zou, J, Chassaing, B, Singh, V, et al. (2018) Fiber-mediated nourishment of gut microbiota protects against diet-induced obesity by restoring IL-22-mediated colonic health. Cell Host Microbe 23, 4153.

Keywords

Type Description Title
WORD
Supplementary materials

Wang et al. supplementary material
Tables S1 and S2

 Word (28 KB)
28 KB

Inulin alleviates adverse metabolic syndrome and regulates intestinal microbiota composition in Nile tilapia (Oreochromis niloticus) fed with high-carbohydrate diet

  • Tong Wang (a1), Ning Zhang (a1), Xiao-Bo Yu (a1), Fang Qiao (a1), Li-Qiao Chen (a1), Zhen-Yu Du (a1) and Mei-Ling Zhang (a1)...

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.