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Effects of Bacillus subtilis on hepatic lipid metabolism and oxidative stress response in grass carp (Ctenopharyngodon idellus) fed a high-fat diet

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Abstract

Bacillus subtilis is widely used in aquaculture as a probiotic. However, few studies have been conducted to examine the effect of B. subtilis on liver lipid metabolism. A total of 135 healthy grass carp (50.24 ± 1.38 g) were randomly divided into three groups: control (Con), high-fat diet (HF), and high-fat diet + B. subtilis (HF + B. subtilis), and fed for 8 weeks. The results showed that compared with the HF group, the weight gain rate (WGR) significantly increased (P < 0.05) and the hepatic lipid content, serum low-density lipoprotein cholesterol (LDL-C), and aspartate aminotransferase (AST) decreased in the group supplemented with B. subtilis (P < 0.05). Moreover, the hepatic mRNA expression of fatty acid synthase (FAS) was significantly down-regulated and the carnitine palmitoyl transferases (CPT1α1a) were up-regulated in the HF + B. subtilis group compared to the HF group (P < 0.05), respectively. Additionally, in the HF + B. subtilis group, glutathione (GSH) significantly increased (P < 0.05), while hydrogen peroxide (H2O2) and malondialdehyde (MDA) contents significantly decreased compared to the HF group (P < 0.05). B. subtilis may reduce the hepatic lipid content by inhibiting its synthesis and promoting β-oxidation of fatty acids. B. subtilis may also alleviate dyslipidaemia and prevent oxidative damage in the liver caused by the high-fat diet of grass carp. Hence, dietary supplementation with B. subtilis shows promise as a therapeutic or preventive tool against fatty liver disease.

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References

  • Abass DA, Obirikorang KA, Campion BB, Edziyie RE, Skov PV (2018) Dietary supplementation of yeast (Saccharomyces cerevisiae) improves growth, stress tolerance, and disease resistance in juvenile Nile tilapia (Oreochromis niloticus). Aquac Int 26:843–855

    CAS  Google Scholar 

  • Al-Muzafar HM, Amin KA (2017) Probiotic mixture improves fatty liver disease by virtue of its action on lipid profiles, leptin, and inflammatory biomarkers. BMC Complement Altern Med 17:43

    PubMed  PubMed Central  Google Scholar 

  • An HM, Park SY, Lee DK, Kim JR, Cha MK, Lee SW, Lim HT, Kim KJ, Ha NJ (2011) Antiobesity and lipid-lowering effects of Bifidobacterium spp. in high fat diet-induced obese rats. Lipids Health Dis 10:116

    PubMed  PubMed Central  Google Scholar 

  • Awaisheh SS, Khalifeh MS, Al-Ruwaili MA, Khalil OM, Al-Ameri OH, Al-Groom R (2013) Effect of supplementation of probiotics and phytosterols alone or in combination on serum and hepatic lipid profiles and thyroid hormones of hypercholesterolemic rats. J Dairy Sci 96:9–15

    CAS  PubMed  Google Scholar 

  • Banda IGDL, Lobo C, León-Rubio JM, Tapia-Paniagua S, Balebona MC, Moriñigo MA, Moreno-Ventas X, Lucas LM, Linares F, Arce F (2010) Influence of two closely related probiotics on juvenile Senegalese sole (Solea senegalensis, Kaup 1858) performance and protection against Photobacterium damselae subsp. piscicida. Aquaculture 306:281–288

    Google Scholar 

  • Briskey D (2015) The effects of multi-strain probiotics on liver disease. PhD thesis, The University of Queensland

  • Chatzifotis S, Panagiotidou M, Papaioannou N, Pavlidis M, Nengas I, Mylonas CC (2010) Effect of dietary lipid levels on growth, feed utilization, body composition and serum metabolites of meagre (Argyrosomus regius) juveniles. Aquaculture 307:65–70

    CAS  Google Scholar 

  • Chelladurai G, Veni T, Mohanraj J, Vijayakumar I (2012) The investigation of Lactobacillus acidophillus as probiotics on growth performance and gut microflora of cat fish (Mystus Montanus). Int J Res Fish Aquac 2:41–43

    Google Scholar 

  • Chen QL, Luo Z, Pan YX, Zheng JL, Zhu QL, Sun LD, Zhuo MQ, Hu W (2013) Differential induction of enzymes and genes involved in lipid metabolism in liver and visceral adipose tissue of juvenile yellow catfish Pelteobagrus fulvidraco exposed to copper. Aquat Toxicol 136–137:72–78

    PubMed  Google Scholar 

  • Chen QQ, Liu WB, Zhou M, Dai YJ, Xu C, Tian HY, Xu WN (2016) Effects of berberine on the growth and immune performance in response to ammonia stress and high-fat dietary in blunt snout bream Megalobrama amblycephala. Fish Shellfish Immunol 55:165–172

    CAS  PubMed  Google Scholar 

  • Du Z, Liu Y, Tian L, Wang J, Wang Y, Liang G (2005) Effect of dietary lipid level on growth, feed utilization and body composition by juvenile grass carp (Ctenopharyngodon idella). Aquac Nutr 11:139–146

    CAS  Google Scholar 

  • Du ZY, Clouet P, Zheng WH, Degrace P, Tian LX, Liu YJ (2006) Biochemical hepatic alterations and body lipid composition in the herbivorous grass carp (Ctenopharyngodon idella) fed high-fat diets. Br J Nutr 95:905–915

    CAS  PubMed  Google Scholar 

  • Eberle D, Hegarty B, Bossard P, Ferre P, Foufelle F (2004) SREBP transcription factors: master regulators of lipid homeostasis. Biochimie 86:839–848

    CAS  PubMed  Google Scholar 

  • Falcinelli S, Picchietti S, Rodiles A, Cossignani L, Merrifield DL, Taddei AR, Maradonna F, Olivotto I, Gioacchini G, Carnevali O (2015) Lactobacillus rhamnosus lowers zebrafish lipid content by changing gut microbiota and host transcription of genes involved in lipid metabolism. Sci Rep 5:9336

    CAS  PubMed  PubMed Central  Google Scholar 

  • Falcinelli S, Rodiles A, Hatef A, Picchietti S, Cossignani L, Merrifield DL, Unniappan S, Carnevali O (2017) Dietary lipid content reorganizes gut microbiota and probiotic L. rhamnosus attenuates obesity and enhances catabolic hormonal milieu in zebrafish. Sci Rep 7:5512

    PubMed  PubMed Central  Google Scholar 

  • Hassaan MS, Soltan MA, Jarmołowicz S, Abdo HS (2018) Combined effects of dietary malic acid and Bacillus subtilis on growth, gut microbiota and blood parameters of Nile tilapia (Oreochromis niloticus). Aquac Nutr 24:83–93

    CAS  Google Scholar 

  • Hillestad M, Johnsen F, Austreng E, Åsgård T (1998) Long-term effects of dietary fat level and feeding rate on growth, feed utilization and carcass quality of Atlantic salmon. Aquac Nutr 4(2):89–97

    CAS  Google Scholar 

  • Huang C, Zhang Z, Wu S, Zhang D, Li S, Chen X, Wu Z (2017) The protective effect of probiotic Bacillus subtilis on the intestinal mucosal structure of Ctenopharyngodon idellus. Acta Hydrobiol Sin 41:774–780

    Google Scholar 

  • Huang L, Cheng Y, Huang K, Zhou Y, Ma Y, Zhang M (2018) Ameliorative effect of Sedum sarmentosum Bunge extract on Tilapia fatty liver via the PPAR and P53 signaling pathway. Sci Rep 8:8456

    PubMed  PubMed Central  Google Scholar 

  • Ji H, Li J, Liu P (2011) Regulation of growth performance and lipid metabolism by dietary n-3 highly unsaturated fatty acids in juvenile grass carp, Ctenopharyngodon idellus. Comp Biochem Physiol B 159:49–56

    PubMed  Google Scholar 

  • Jung CH, Cho I, Ahn J, Jeon TI, Ha TY (2013) Quercetin reduces high-fat diet-induced fat accumulation in the liver by regulating lipid metabolism genes. Phytother Res 27:139–143

    CAS  PubMed  Google Scholar 

  • Kerner J, Hoppel C (2000) Fatty acid import into mitochondria. Biochim Biophys Acta 1486:1–17

    CAS  PubMed  Google Scholar 

  • Kong W, Huang C, Tang Y, Zhang D, Wu Z, Chen X (2017a) Effect of Bacillus subtilis on Aeromonas hydrophila-induced intestinal mucosal barrier function damage and inflammation in grass carp (Ctenopharyngodon idella). Sci Rep 7:1588

    PubMed  PubMed Central  Google Scholar 

  • Kong WG, Li SS, Chen XX, Huang YQ, Tang Y, Wu ZX (2017b) A study of the damage of the intestinal mucosa barrier structure and function of Ctenopharyngodon idella with Aeromonas hydrophila. Fish Physiol Biochem 43:1223–1235

    CAS  PubMed  Google Scholar 

  • Lee HY, Park JH, Seok SH, Baek MW, Kim DJ, Lee KE, Paek KS, Lee Y, Park JH (2006) Human originated bacteria, Lactobacillus rhamnosus PL60, produce conjugated linoleic acid and show anti-obesity effects in diet-induced obese mice. Biochim Biophys Acta 1761:736–744

    CAS  PubMed  Google Scholar 

  • Li W, Zhang X, Song W, Deng B, Zheng J, Liang Q, Wang Y, Fu L, Yu D (2012) Effects of Bacillus preparations on immunity and antioxidant activities in grass carp (Ctenopharyngodon idellus). Fish Physiol Biochem 38:1585–1592

    CAS  Google Scholar 

  • Li A, Yuan X, Liang XF, Liu L, Li J, Li B, Fang J, Li J, He S, Xue M, Wang J, Tao Y-X (2016) Adaptations of lipid metabolism and food intake in response to low and high fat diets in juvenile grass carp (Ctenopharyngodon idellus). Aquaculture 457:43–49

    CAS  Google Scholar 

  • Ma X, Hua J, Li Z (2008) Probiotics improve high fat diet-induced hepatic steatosis and insulin resistance by increasing hepatic NKT cells. J Hepatol 49:821–830

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ma Q, Li LY, Le JY, Lu DL, Qiao F, Zhang ML, Du ZY, Li DL (2018) Dietary microencapsulated oil improves immune function and intestinal health in Nile tilapia fed with high-fat diet. Aquaculture 496:19–29

    CAS  Google Scholar 

  • Morash AJ, Kajimura M, McClelland GB (2008) Intertissue regulation of carnitine palmitoyltransferase I (CPTI): mitochondrial membrane properties and gene expression in rainbow trout (Oncorhynchus mykiss). Biochim Biophys Acta 1778:1382–1389

    CAS  PubMed  Google Scholar 

  • Munirasu S, Ramasubramanian V, Arunkumar P (2017) Effect of Probiotics diet on growth and biochemical performance of freshwater fish Labeo rohita fingerlings. J Entomol Zool Stud 5:1374–1379

    Google Scholar 

  • Ozer J, Ratner M, Shaw M, Bailey W, Schomaker S (2008) The current state of serum biomarkers of hepatotoxicity. Toxicology 245:194–205

    CAS  PubMed  Google Scholar 

  • Ren Y, Li S, Wu Z, Zhou C, Zhang D, Chen X (2017) The influences of Bacillus subtilis on the virulence of Aeromonas hydrophila and expression of luxs gene of both bacteria under co-cultivation. Curr Microbiol 74:718–724

    CAS  PubMed  Google Scholar 

  • Rincon-Cervera MA, Valenzuela R, Hernandez-Rodas MC, Marambio M, Espinosa A, Mayer S, Romero N, Barrera MSC, Valenzuela A, Videla LA (2016) Supplementation with antioxidant-rich extra virgin olive oil prevents hepatic oxidative stress and reduction of desaturation capacity in mice fed a high-fat diet: effects on fatty acid composition in liver and extrahepatic tissues. Nutrition 32:1254–1267

    CAS  PubMed  Google Scholar 

  • Roberto G, Giovanni M, Maurizio C (2011) Redox balance in the pathogenesis of nonalcoholic fatty liver disease: mechanisms and therapeutic opportunities. Antioxid Redox Signal 15:1325–1365

    Google Scholar 

  • Rosen ED, Sarraf P, Troy AE, Bradwin G, Moore K, Milstone DS, Spiegelman BM, Mortensen RM (1999) PPAR gamma is required for the differentiation of adipose tissue in vivo and in vitro. Mol Cell 4:611–617

    CAS  PubMed  Google Scholar 

  • Sabzi E, Mohammadiazarm H, Salati AP (2017) Effect of dietary l -carnitine and lipid levels on growth performance, blood biochemical parameters and antioxidant status in juvenile common carp (Cyprinus carpio). Aquaculture 480:89–93

    CAS  Google Scholar 

  • Schroeder F, Jolly CA, Cho TH, Frolov A (1998) Fatty acid binding protein isoforms: structure and function. Chem Phys Lipids 92:1–25

    CAS  PubMed  Google Scholar 

  • Shen WY, Fu LL, Li WF, Zhu YR (2010) Effect of dietary supplementation with Bacillus subtilis on the growth, performance, immune response and antioxidant activities of the shrimp (Litopenaeus vannamei). Aquac Res 41:1691–1698

    CAS  Google Scholar 

  • Shimada Y, Kuninaga S, Ariyoshi M, Zhang B, Shiina Y, Takahashi Y, Umemoto N, Nishimura Y, Enari H, Tanaka T (2015) E2F8 promotes hepatic steatosis through FABP3 expression in diet-induced obesity in zebrafish. Nutr Metab 12:17

    Google Scholar 

  • Song YF, Luo Z, Zhang LH, Hogstrand C, Pan YX (2016) Endoplasmic reticulum stress and disturbed calcium homeostasis are involved in copper-induced alteration in hepatic lipid metabolism in yellow catfish Pelteobagrus fulvidraco. Chemosphere 144:2443–2453

    CAS  PubMed  Google Scholar 

  • Standen BT, Peggs DL, Rawling MD, Foey A, Davies SJ, Santos GA, Merrifield DL (2016) Dietary administration of a commercial mixed-species probiotic improves growth performance and modulates the intestinal immunity of tilapia, Oreochromis niloticus. Fish Shellfish Immunol 49:427–435

    CAS  PubMed  Google Scholar 

  • Tang Y, Han L, Chen X, Xie M, Kong W, Wu Z (2018) Dietary supplementation of probiotic Bacillus subtilis affects antioxidant defenses and immune response in grass carp under Aeromonas hydrophila Challenge. Probiotics Antimicro. https://doi.org/10.1007/s12602-018-9409-8

    Article  Google Scholar 

  • Tapia-Paniagua ST, Díaz-Rosales P, García de la Banda I, Lobo C, Clavijo E, Balebona MC, Moriñigo MA (2014) Modulation of certain liver fatty acids in Solea senegalensis is influenced by the dietary administration of probiotic microorganisms. Aquaculture 424–425:234–238

    Google Scholar 

  • Tian Y, Wang H, Yuan F, Li N, Huang Q, He L, Wang L, Liu Z (2016) Perilla oil has similar protective effects of fish oil on high-fat diet-induced nonalcoholic fatty liver disease and gut dysbiosis. Biomed Res Int 2016:1–11

    Google Scholar 

  • Tontonoz P, Hu E, Spiegelman BM (1994) Stimulation of adipogenesis in fibroblasts by PPAR gamma 2, a lipid-activated transcription factor. Cell 79:1147–1156

    CAS  PubMed  Google Scholar 

  • Venkatachalam AB, Sawler DL, Wright JM (2013) Tissue-specific transcriptional modulation of fatty acid-binding protein genes, fabp2, fabp3 and fabp6, by fatty acids and the peroxisome proliferator, clofibrate, in zebrafish (Danio rerio). Gene 520:14–21

    CAS  PubMed  Google Scholar 

  • Wang WN, Zhou J, Peng W, Tian TT, Ying Z, Yuan L, Mai WJ, Wang AL (2009) Oxidative stress, DNA damage and antioxidant enzyme gene expression in the Pacific white shrimp, Litopenaeus vannamei when exposed to acute pH stress. Comp Biochem Physiol C 150:428–435

    Google Scholar 

  • Wang X, Li Y, Hou C, Gao Y, Wang Y (2015) Physiological and molecular changes in large yellow croaker (Pseudosciaena crocea R.) with high-fat diet-induced fatty liver disease. Aquac Res 46:272–282

    CAS  Google Scholar 

  • Wu ZX, Feng X, Xie LL, Peng XY, Yuan J, Chen XX (2012) Effect of probiotic Bacillus subtilis Ch9 for grass carp, Ctenopharyngodon idella (Valenciennes, 1844), on growth performance, digestive enzyme activities and intestinal microflora. J Appl Ichthyol 28:721–727

    Google Scholar 

  • Xin J, Zeng D, Wang H, Ni X, Yi D, Pan K, Jing B (2014) Preventing non-alcoholic fatty liver disease through Lactobacillus johnsonii BS15 by attenuating inflammation and mitochondrial injury and improving gut environment in obese mice. Appl Microbiol Biot 98:6817–6829

    CAS  Google Scholar 

  • Xu JH, Qin J, Yan BL, Zhu M, Luo G (2011) Effects of dietary lipid levels on growth performance, feed utilization and fatty acid composition of juvenile Japanese seabass (Lateolabrax japonicus) reared in seawater. Aquac Int 19:79–89

    CAS  Google Scholar 

  • Xu RY, Wan YP, Fang QY, Lu W, Cai W (2012) Supplementation with probiotics modifies gut flora and attenuates liver fat accumulation in rat nonalcoholic fatty liver disease model. J Clin Biochem Nutr 50:72–77

    CAS  PubMed  Google Scholar 

  • Yang SP, Wu ZH, Jian JC, Zhang XZ (2010) Effect of marine red yeast Rhodosporidium paludigenum on growth and antioxidant competence of Litopenaeus vannamei. Aquaculture 309:62–65

    CAS  Google Scholar 

  • Yoo SR, Kim YJ, Park DY, Jung UJ, Jeon SM, Ahn YT, Huh CS, McGregor R, Choi MS (2013) Probiotics L. plantarum and L. curvatus in combination alter hepatic lipid metabolism and suppress diet-induced obesity. Obesity 21:2571–2578

    CAS  PubMed  Google Scholar 

  • Yuan X, Liang XF, Liu L, Fang J, Li J, Li A, Cai W, Xue M, Wang J, Wang Q (2016) Fat deposition pattern and mechanism in response to dietary lipid levels in grass carp, Ctenopharyngodon idellus. Fish Physiol Biochem 42:1557–1569

    CAS  PubMed  Google Scholar 

  • Zang L, Shimada Y, Tanaka T, Nishimura N (2015) Rhamnan sulphate from Monostroma nitidum attenuates hepatic steatosis by suppressing lipogenesis in a diet-induced obesity zebrafish model. J Funct Foods 17:364–370

    CAS  Google Scholar 

  • Zhang D, Yan Y, Tian H, Jiang G, Li X, Liu W (2018) Resveratrol supplementation improves lipid and glucose metabolism in high-fat diet-fed blunt snout bream. Fish Physiol Biochem 44:163–173

    CAS  PubMed  Google Scholar 

  • Zokaeifar H, Balcazar JL, Saad CR, Kamarudin MS, Sijam K, Arshad A, Nejat N (2012) Effects of Bacillus subtilis on the growth performance, digestive enzymes, immune gene expression and disease resistance of white shrimp, Litopenaeus vannamei. Fish Shellfish Immunol 33:683–689

    CAS  PubMed  Google Scholar 

  • Zuenko VA, Laktionov KS, Pravdin IV, Kravtsova LZ, Ushakova NA (2017) Effect of Bacillus subtilis in feed probiotic on the digestion of fish cultured in cages. J Ichthyol 57:152–157

    Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant nos. 31472310 and 31672683) and the Technical Innovation Project of Hubei Province (Grant No. 2018ABA103).

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Conceptualization, HZ and YL; methodology, HZ, YL, YZ, XC, HW, DG and ZW; validation, HZ and YL; writing-original draft preparation, HZ and YL; writing-review and editing, XC and ZW; supervision, ZW; project administration, ZW.

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Correspondence to Zhixin Wu.

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All applicable international, national, and institutional guidelines for the care and use of animals were followed by the authors.

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Edited by Xin Yu.

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Zhao, H., Luo, Y., Zhang, Y. et al. Effects of Bacillus subtilis on hepatic lipid metabolism and oxidative stress response in grass carp (Ctenopharyngodon idellus) fed a high-fat diet. Mar Life Sci Technol 2, 50–59 (2020). https://doi.org/10.1007/s42995-019-00005-2

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