Effects of Long-Term Feeding of Lactobacillus reuteri on expression of Genes Related to Lipid Metabolism in Subcutaneous Fat and Liver of Pigs

TIAN Zhimei; CUI Yiyan; LU Huijie; YU Miao; LIU Zhichang; LI Zhenming; RONG Ting; MA Xianyong; MA Xinyan

doi:10.3969/j.issn.1006-267x.2021.05.048

2021 , Vol. 33 >Issue 5: 2907 - 2917

DOI: https://doi.org/10.3969/j.issn.1006-267x.2021.05.048

Effects of Long-Term Feeding of Lactobacillus reuteri on expression of Genes Related to Lipid Metabolism in Subcutaneous Fat and Liver of Pigs

TIAN Zhimei ,
CUI Yiyan ,
LU Huijie ,
YU Miao ,
LIU Zhichang ,
LI Zhenming ,
RONG Ting ,
MA Xianyong ,
MA Xinyan

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1. Guangdong Engineering Technology Research Center of animal Meat Quality and Safety Control and Evaluation, Guangdong Provincial Key Laboratory of Animal Breeding and Nutrition, State Key Laboratory of Livestock and Poultry Breeding, Key Laboratory of Animal Nutrition and Feed Science in South China, Ministry of Agriculture and Rural Affairs, Institute of Animal Science, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China;
2. Maoming Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Maoming 525000, China

Received date: 2020-10-10

Online published: 2021-05-14

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Abstract

This experiment was aimed to study effects of Lactobacillus reuteri 1 (LR1) on expression of genes related to lipid metabolism in subcutaneous fat and liver of pigs. A total of 144 cross-bred (Duroc×Landrace×Yorkshire) 21-day-old weaned piglets were randomly assigned to 3 groups, each group comprised 8 replicate pens with 6 pigs per pen. The diet in the control 1 group was a basal diet, the diet in the control 2 group was the basal diet supplemented with antibiotics, and the diet in LR1 group was the basal diet supplemented with 5×10¹⁰ CFU/kg LR1. The experiment period was 175 days. The results showed as follows:1) compared with the control 1 group, the relative expression levels of sterol regulatory element binding protein (SREBP), acetyl CoA carboxylase (ACC), fatty acid synthase (FAS), stearoyl CoA desaturase (SCD) and adipose triglyceride lipase (ATGL) genes in abdominal adipose in the control 2 group were significantly increased (P<0.05), but there were no significant difference in the relative expression levels of carnitine palmitoyl transferase 1 beta (CPT-1β), peroxisome proliferator-activated receptor alfa (PPARα), fatty acid transport protein-1 (FATP-1), peroxisome proliferator-activated receptor gamma (PPARγ) genes (P>0.05); the relative expression level of FATP-1 gene was increased significantly in LR1 group (P<0.05), and the relative expression levels of SREBP, ACC, CPT-1β, FAS, PPARα, SCD, PPARγ and ATGL genes had no significant different (P>0.05); the relative expression levels of SREBP, ACC and SCD genes in LR1 group were significantly decreased compared with the control 2 group (P>0.05). 2) Compared with control 1 group, the relative expression levels of SCD and ATGL genes in back fat was increased significantly in the control 2 group (P<0.05), and the relative expression level of SCD gene was decreased significantly in LR1 group (P<0.05); compared with control 2 group, the relative expression levels of ACC, FAS and SCD genes in the LR1 group were significantly reduced (P<0.05); compared with the control 1 and 2 groups, the relative expression level of PPARγ gene in backfat in LR1 group was significantly increased (P<0.05). 3) Compared with control 1 group, the relative expression levels of SREBP, ACC, FAS and SCD genes in liver in the control 2 group and LR1 group were significantly decreased (P<0.05), but the relative expression levels of CPT-1β, PPARα, FATP-1, PPARγ and ATGL genes had no significant differences (P>0.05). In conclusion, LR1 promotes fatty acids transport in subcutaneous fat and decreases anabolism of backfat and liver in pigs compared with antibiotics. Additionally, LR1 affects lipid transport and catabolism of liver in pigs.

Key words： Lactobacillus reuteri; carcass traits; subcutaneous adipose; liver; lipid metabolism; fattening pigs

Cite this article

TIAN Zhimei , CUI Yiyan , LU Huijie , YU Miao , LIU Zhichang , LI Zhenming , RONG Ting , MA Xianyong , MA Xinyan . Effects of Long-Term Feeding of Lactobacillus reuteri on expression of Genes Related to Lipid Metabolism in Subcutaneous Fat and Liver of Pigs[J]. Chinese Journal of Animal Nutrition, 2021 , 33(5) : 2907 -2917 . DOI: 10.3969/j.issn.1006-267x.2021.05.048

References

[1] GUSTAFSON R H,BOWEN R E.Antibiotic use in animal agriculture[J].Journal of Applied Microbiology,1997,83(5):531-541.

[2] CHATTOPADHYAY M K.Use of antibiotics as feed additives:a burning question[J].Frontiers in Microbiology,2014,5:334.
[3] LI J Y.Current status and prospects for in-feed antibiotics in the different stages of pork production-a review[J].Asian-Australasian Journal of Animal Sciences,2017,30(12):1667-1673.

[4] LEE J H.Perspectives towards antibiotic resistance:from molecules to population[J].Journal of Microbiology,2019,57(3):181-184.

[5] LIU W C,DEVI S,PARK J,et al.Effects of complex probiotic supplementation in growing pig diets with and without palm kernel expellers on growth performance,nutrient digestibility,blood parameters,fecal microbial shedding and noxious gas emission[J].Animal Science Journal,2018,89(3):552-560.

[6] ZHANG D Y,JI H F,LIU H,et al.Changes in the diversity and composition of gut microbiota of weaned piglets after oral administration of Lactobacillus or an antibiotic[J].Applied Microbiology and Biotechnology,2016,100(23):10081-10093.

[7] TIAN Z M,CUI Y Y,LU H J,et al.Effects of long-term feeding diets supplemented with Lactobacillus reuteri 1 on growth performance,digestive and absorptive function of the small intestine in pigs[J].Journal of Functional Foods,2020,71:104010.
[8] WANG X Q,YANG F,LIU C,et al.Dietary supplementation with the probiotic Lactobacillus fermentum I5007 and the antibiotic aureomycin differentially affects the small intestinal proteomes of weanling piglets[J].The Journal of Nutrition,2012,142(1):7-13.

[9] HOU C L,ZENG X F,YANG F J,et al.Study and use of the probiotic Lactobacillus reuteri in pigs:a review[J].Journal of Animal Science and Biotechnology,2015,6(1):14.
[10] OH P L,BENSON A K,PETERSON D A,et al.Diversification of the gut symbiont Lactobacillus reuteri as a result of host-driven evolution[J].The ISME Journal,2010,4(3):377-387.

[11] WANG T W,TENG K L,LIU G,et al.Lactobacillus reuteri HCM2 protects mice against enterotoxigenic Escherichia coli through modulation of gut microbiota[J].Scientific Reports,2018,8(1):17485.
[12] WANG Z L,WANG L,CHEN Z,et al.In vitro evaluation of swine-derived Lactobacillus reuteri:probiotic properties and effects on intestinal porcine epithelial cells challenged with enterotoxigenic Escherichia coli K88[J].Journal of Microbiology and Biotechnology,2016,26(6):1018-1025.

[13] YI H B,WANG L,XIONG Y X,et al.Lactobacillus reuteri LR1 improved expression of genes of tight junction proteins via the MLCK pathway in IPEC-1 cells during infection with enterotoxigenic Escherichia coli K88[J].Mediators of Inflammation,2018,2018:6434910.
[14] YI H B,WANG L,XIONG Y X,et al.Effects of Lactobacillus reuteri LR1 on the growth performance,intestinal morphology,and intestinal barrier function in weaned pigs[J].Journal of Animal Science,2018,96(6):2342-2351.

[15] TIAN Z M,CUI Y Y,LU H J,et al.Effect of long-term dietary probiotic Lactobacillus reuteri 1 or antibiotics on meat quality,muscular amino acids and fatty acids in pigs[J].Meat Science,2021,171:108234.
[16] 中华人民共和国农业部.GB/T 8467-1987瘦肉型种猪性能测定技术规程[S].北京:中国标准出版社,1988. Ministry of Agriculture of the People's Republic of China.GB/T 8467-1987 Regulation for performance testing techniques of lean-type breeding pigs[S].Beijing:China Standard Press,1988.(in Chinese)
[17] NPPC.National pork producers council[S].Des Moines,I.A.:National Pork Producers Council,1991.
[18] 田志梅,马现永,王丽,等.长期饲喂不同蛋白质水平饲粮对猪脂肪代谢相关基因表达的影响[J].动物营养学报,2017,29(10):3761-3772. TIAN Z M,MA X Y,WANG L,et al.Effects of long-term feeding diets with different protein levels on gen expressions related to lipid metabolism of pigs[J].Chinese Journal of Animal Nutrition,2017,29(10):3761-3772.(in Chinese)
[19] LOWELL J E,BOHRER B M,WILSON K B,et al.Growth performance,carcass quality,fresh belly characteristics,and commercial bacon slicing yields of growing-finishing pigs fed a subtherapeutic dose of an antibiotic,a natural antimicrobial,or not fed an antibiotic or antimicrobial[J].Meat Science,2018,136:93-103.
[20] LE M H A,GALLE S,YANG Y,et al.Effects of feeding fermented wheat with Lactobacillus reuteri on gut morphology,intestinal fermentation,nutrient digestibility,and growth performance in weaned pigs[J].Journal of Animal Science,2016,94(11):4677-4687.

[21] YANG J J,WANG C L,HUANG K H,et al.Compound Lactobacillus sp.administration ameliorates stress and body growth through gut microbiota optimization on weaning piglets[J].Applied Microbiology and Biotechnology,2020,104(15):6749-6765.

[22] DOWARAH R,VERMA A K,AGARWAL N,et al.Efficacy of species-specific probiotic Pediococcus acidilactici FT28 on blood biochemical profile,carcass traits and physicochemical properties of meat in fattening pigs[J].Research in Veterinary Science,2018,117:60-64.
[23] ALEXOPOULOS C,GEORGOULAKIS I E,TZIVARA A,et al.Field evaluation of the effect of a probiotic-containing Bacillus licheniformis and Bacillus subtilis spores on the health status,performance,and carcass quality of grower and finisher pigs[J].Journal of Veterinary Medicine Series A,2004,51(6):306-312.

[24] ZHAO S M,REN L J,CHEN L,et al.Differential expression of lipid metabolism related genes in porcine muscle tissue leading to different intramuscular fat deposition[J].Lipids,2009,44(11):1029.
[25] XU H F,LUO J,MA G Z,et al.Acyl-CoA synthetase short-chain family member 2(ACSS2) is regulated by SREBP-1 and plays a role in fatty acid synthesis in caprine mammary epithelial cells[J].Journal of Cellular Physiology,2018,233(2):1005-1016.

[26] RITTNER A,PAITHANKAR K S,HIMMLER A,et al.Type Ⅰ fatty acid synthase trapped in the octanoyl-bound state[J].Protein Science,2020,29(2):589-605.

[27] GREEN C D,OZGUDEN-AKKOC C G,WANG Y,et al.Role of fatty acid elongases in determination of de novo synthesized monounsaturated fatty acid species[J].Journal of Lipid Research,2010,51(7):1871-1877.

[28] ZHANG J,CUI L,MA J,et al.Transcriptome analyses reveal genes and pathways associated with fatty acid composition traits in pigs[J].Animal Genetics,2017,48(6):645-652.

[29] DEIULⅡS J A,SHIN J,BAE D,et al.Developmental,hormonal,and nutritional regulation of porcine adipose triglyceride lipase (ATGL)[J].Lipids,2008,43(3):215-225.

[30] ZIMMERMANN R,STRAUSS J G,HAEMMERLE G,et al.Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase[J].Science,2004,306(5700):1383-1386.

[31] CHEN X L,LUO Y L,WANG R S,et al.Effects of fatty acid transport protein 1 on proliferation and differentiation of porcine intramuscular preadipocytes[J].Animal Science Journal,2017,88(5):731-738.

[32] SHU G,ZHU X T,WANG X Q,et al.Identification and gene expression of porcine fatty acid transport protein 1 isoforms[J].Journal of Animal Physiology and Animal Nutrition,2009,93(4):439-446.

[33] MADEIRA M S,PIRES V M R,ALFAIA C M,et al.Combined effects of dietary arginine,leucine and protein levels on fatty acid composition and gene expression in the muscle and subcutaneous adipose tissue of crossbred pigs[J].British Journal of Nutrition,2014,111(9):1521-1535.

[34] FEIGE J N,GELMAN L,MICHALIK L,et al.From molecular action to physiological outputs:peroxisome proliferator-activated receptors are nuclear receptors at the crossroads of key cellular functions[J].Progress in Lipid Research,2006,45(2):120-159.

[35] REIJNDERS D,GOOSSENS G H,HERMES G D A,et al.Effects of gut microbiota manipulation by antibiotics on host metabolism in obese humans:a randomized double-blind placebo-controlled trial[J].Cell Metabolism,2016,24(1):63-74.

[36] RENU K,SRUTHY K B,PARTHIBAN S,et al.Elevated lipolysis in adipose tissue by doxorubicin via PPARα activation associated with hepatic steatosis and insulin resistance[J].European Journal of Pharmacology,2019,843:162-176.
[37] TORRES S,FABERSANI E,MARQUEZ A,et al.Adipose tissue inflammation and metabolic syndrome.The proactive role of probiotics[J].European Journal of Nutrition,2019,58(1):27-43.

[38] KIM D H,JEONG D,KANG I B,et al.Dual function of Lactobacillus kefiri DH5 in preventing high-fat-diet-induced obesity:direct reduction of cholesterol and upregulation of PPAR-α in adipose tissue[J].Molecular Nutrition & Food Research,2017,61(11):1700252.
[39] PARK S S,LEE Y J,KANG H,et al.Lactobacillus amylovorus KU4 ameliorates diet-induced obesity in mice by promoting adipose browning through PPARγ signaling[J].Scientific Reports,2019,9(1):20152.
[40] 崔悦悦.白藜芦醇通过脂联素信号通路调节猪脂肪沉积的机制研究[D].硕士学位论文.南宁:广西大学,2019. CUI Y Y.Study on the mechanism of resveratrol regulating fat deposition through adiponectin signaling pathway in pig[D].Master's Thesis.Nanning:Guangxi University,2019.(in Chinese)
[41] DAI J Y,LIANG K,ZHAO S,et al.Chemoproteomics reveals baicalin activates hepatic CPT1 to ameliorate diet-induced obesity and hepatic steatosis[J].Proceedings of the National Academy Sciences of the United States of America,2018,115(26):E5896-E5905.
[42] CHO M S,KIM S Y,SUK K T,et al.Modulation of gut microbiome in nonalcoholic fatty liver disease:pro-,pre-,syn-,and antibiotics[J].Journal of Microbiology,2018,56(12):855-867.

[43] YI H B,YANG G D,XIONG Y X,et al.Integrated metabolomic and proteomics profiling reveals the promotion of Lactobacillus reuteri LR1 on amino acid metabolism in the gut-liver axis of weaned pigs[J].Food & Function,2019,10(11):7387-7396.

[44] WANG Z C,HU J,ZHENG W Y,et al.Lactobacillus frumenti mediates energy production via fatty acid β-oxidation in the liver of early-weaned piglets[J].Journal of Animal Science and Biotechnology,2019,10:95.

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