Effects of Low-Protein Diet Supplemented with Fermented Broussonetia papyrifera Feed on Fat Deposition and Gut Microbiota Composition of Finishing Pigs

  • DUAN Geyan ,
  • SONG Bo ,
  • CHEN Xiaoan ,
  • ZHENG Changbing ,
  • ZHENG Jie ,
  • ZHANG Shiyu ,
  • GUO Qiuping ,
  • LI Fengna ,
  • DUAN Yehui ,
  • YIN Yulong
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  • 1. Key Laboratory of Agro-Ecological Process in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha 410125, China;
    2. University of Chinese Academy of Sciences, Beijing 100039, China;
    3. Hunan Lifeng Biological Technology Co., Ltd., Changsha 410125, China

Received date: 2021-08-26

  Online published: 2022-04-14

Abstract

This study aimed to investigate the effects of low-protein diet supplemented with fermented Broussonetia papyrifera feed on fat deposition and gut microbiota composition of finishing pigs. Eighteen healthy and similar body weight[(63.53±0.40) kg] three-way cross-finishing pigs (Duroc×Landrace×Yorhshire) were randomly divided into 3 groups (n=6):1) normal protein diet group (as control group, dietary crude protein content was 16%); 2) low protein diet group (dietary crude protein content was 13%); 3) fermented Broussonetia papyrifera feed group (the diet contained 10% fermented Broussonetia papyrifera feed, and dietary crude protein content was 13%). The test period was 45 days. The results showed that compared with the normal protein diet, the low protein diet significantly increased the body fat weight and significantly reduced the concentration of acetic acid and propionic acid in colon (P<0.05), but diet supplemented with fermented Broussonetia papyrifera feed could alleviate these effects of low protein diets. The results of correlation analysis showed that the body fat weight of fattening pigs was significantly negatively correlated with the concentrations of acetic acid and propionic acid in colon (P<0.05). In addition, compared with the low protein diet, diet supplemented with fermented Broussonetia papyrifera feed significantly reduced the mRNA expression levels of gene related to adipogenesis (P<0.05), and significantly increased the relative abundance of Bacteroidetes in colon (P<0.05), significantly decreased the relative abundance of Firmicutes in colon (P<0.05), while significantly reduced the concentrations of cadaverine and skatole in colon (P<0.05). In summary, adding fermented Broussonetia papyrifera feed to the low protein diet can inhibit the synthesis of dorsal subcutaneous adipose, reduce the body fat weight, improve the composition of intestinal microbes, and increase the concentrations of acetic acid and propionic acid in colon of finishing pigs.

Cite this article

DUAN Geyan , SONG Bo , CHEN Xiaoan , ZHENG Changbing , ZHENG Jie , ZHANG Shiyu , GUO Qiuping , LI Fengna , DUAN Yehui , YIN Yulong . Effects of Low-Protein Diet Supplemented with Fermented Broussonetia papyrifera Feed on Fat Deposition and Gut Microbiota Composition of Finishing Pigs[J]. Chinese Journal of Animal Nutrition, 2022 , 34(4) : 2186 -2195 . DOI: 10.3969/j.issn.1006-267x.2022.04.015

References

[1] LEBRET B,MOUROT J.Caractéristiques et qualité des tissus adipeux chez le porc. Facteurs de variation non génétiques[J].INRAE Productions Animales,1998,11(2):131-143.
[2] SUNG H,SIEGEL R L,TORRE L A,et al.Global patterns in excess body weight and the associated cancer burden[J].CA:A Cancer Journal for Clinicians,2019,69(2):88-112.
[3] ASTRUP A,RABEN A,GEIKER N.The role of higher protein diets in weight control and obesity-related comorbidities[J].International Journal of Obesity,2015,39(5):721-726.  
[4] GARCIA CARABALLO S C,COMHAIR T M,DEJONG C H C,et al.Dietary treatment of fatty liver:high dietary protein content has an antisteatotic and antiobesogenic effect in mice[J].Biochimica et Biophysica Acta:Molecular Basis of Disease,2017,1863(7):1789-1804.  
[5] CUENCA-SÁNCHEZ M,NAVAS-CARRILLO D,ORENES-PIÑERO E.Controversies surrounding high-protein diet intake:satiating effect and kidney and bone health[J].Advances in Nutrition,2015,6(3):260-266.  
[6] WANG Y M,ZHOU J Y,WANG G,et al.Advances in low-protein diets for swine[J].Journal of Animal Science and Biotechnology,2018,9:60.
[7] KITADA M,OGURA Y,SUZUKI T,et al.A very-low-protein diet ameliorates advanced diabetic nephropathy through autophagy induction by suppression of the mTORC1 pathway in Wistar fatty rats,an animal model of type 2 diabetes and obesity[J].Diabetologia,2016,59(6):1307-1317.  
[8] ZHANG S,QIAO M,TROTTIER N L.Feeding a reduced protein diet with a near ideal amino acid profile improves amino acid efficiency and nitrogen utilization for milk production in sows[J].Journal of Animal Science,2019,97(9):3882-3897.  
[9] LEI X J,CHEONG J Y,PARK J H,et al.Supplementation of protease,alone and in combination with fructooligosaccharide to low protein diet for finishing pigs[J].Animal Science Journal,2017,88(12):1987-1993.  
[10] PÉREZ-MARTÍ A,GARCIA-GUASCH M,TRESSERRA-RIMBAU A,et al.A low-protein diet induces body weight loss and browning of subcutaneous white adipose tissue through enhanced expression of hepatic fibroblast growth factor 21(FGF21)[J].Molecular Nutrition & Food Research,2017,61(8):1600725.
[11] WU G Y.Functional amino acids in nutrition and health[J].Amino Acids,2013,45(3):407-411.  
[12] PENG X J,LIU H,CHEN P L,et al.A chromosome-scale genome assembly of paper mulberry (Broussonetia papyrifera) provides new insights into its forage and papermaking usage[J].Molecular Plant,2019,12(5):661-677.  
[13] DONG L F,ZHANG H S,GAO Y H,et al.Dynamic profiles of fermentation characteristics and bacterial community composition of Broussonetia papyrifera ensiled with perennial ryegrass[J].Bioresource Technology,2020,310:123396.
[14] HAN Q H,WU Z L,HUANG B,et al.Extraction,antioxidant and antibacterial activities of Broussonetia papyrifera fruits polysaccharides[J].International Journal of Biological Macromolecules,2016,92:116-124.
[15] 李勇.构树叶对营养性肥胖小鼠脂肪代谢的影响[D].硕士学位论文.湛江:广东海洋大学,2011. LI Y.Effects of Broussonetia papyrifera leaf on lipid metabolism of nutritive obese mice[D].Master’s Thesis.Zhanjiang:Guangdong Ocean University,2011.(in Chinese)
[16] DUAN Y H,ZHONG Y Z,XIAO H,et al.Gut microbiota mediates the protective effects of dietary β-hydroxy-β-methylbutyrate (HMB) against obesity induced by high-fat diets[J].FASEB Journal,2019,33(9):10019-10033.  
[17] TOPPING D L,CLIFTON P M.Short-chain fatty acids and human colonic function:roles of resistant starch and nonstarch polysaccharides[J].Physiological Reviews,2001,81(3):1031-1064.  
[18] KIMURA I,OZAWA K,INOUE D,et al.The gut microbiota suppresses insulin-mediated fat accumulation via the short-chain fatty acid receptor GPR43[J].Nature Communications,2013,4:1829.
[19] RIST V T S,WEISS E,EKLUND M,et al.Impact of dietary protein on microbiota composition and activity in the gastrointestinal tract of piglets in relation to gut health:a review[J].Animal,2013,7(7):1067-1078.  
[20] ZHOU L P,FANG L D,SUN Y,et al.Effects of the dietary protein level on the microbial composition and metabolomic profile in the hindgut of the pig[J].Anaerobe,2016,38:61-69.
[21] FAN P X,LIU P,SONG P X,et al.Moderate dietary protein restriction alters the composition of gut microbiota and improves ileal barrier function in adult pig model[J].Scientific Reports,2017,7:43412.
[22] 张兴,朱少中,杨旗,等.构树发酵饲料对湘沙猪配套系商品猪生长性能、胴体品质和肌肉品质的影响[J].动物营养学报,2019,31(12):5760-5771. ZHANG X,ZHU S Z,YANG Q,et al.Effects of Broussonetia papyrifera fermented diet on growth performance,carcass quality and meat quality of Xiangsha pigs commercial line of commercial pigs[J].Chinese Journal of Animal Nutrition,2019,31(12):5760-5771.(in Chinese)
[23] 宋博,郑昌炳,仲银召,等.低蛋白质饲粮中添加构树全株发酵饲料对育肥猪生长性能、胴体性状和肉品质的影响[J].动物营养学报,2020,32(10):4841-4851. SONG B,ZHENG C B,ZHONG Y Z,et al.Effects of low-protein diet supplemented with fermented Broussonetia papyrifera on growth performance,carcass traits and meat quality of finishing pigs[J].Chinese Journal of Animal Nutrition,2020,32(10):4841-4851.(in Chinese)
[24] 郑昌炳,宋博,郑界,等.饲粮中添加β-羟基-β-甲基丁酸对巴马香猪生长性能和肝脏脂肪代谢的影响[J].动物营养学报,2021,33(6):3176-3184. ZHENG C B,SONG B,ZHENG J,et al.Effects of dietary supplementation of beta-hydroxy-beta-methylbutyrate on growth performance and liver lipid metabolism of Bama Xiang pigs[J].Chinese Journal of Animal Nutrition,2021,33(6):3176-3184.(in Chinese)
[25] WANG M,YANG C,WANG Q Y,et al.The growth performance,intestinal digestive and absorptive capabilities in piglets with different lengths of small intestines[J].Animal,2020,14(6):1196-1203.  
[26] KONG X F,JI Y J,LI H W,et al.Colonic luminal microbiota and bacterial metabolite composition in pregnant Huanjiang mini-pigs:effects of food composition at different times of pregnancy[J].Scientific Reports,2016,6:37224.
[27] LEE J M,CHOI S S,PARK M H,et al.Broussonetia papyrifera root bark extract exhibits anti-inflammatory effects on adipose tissue and improves insulin sensitivity potentially via AMPK activation[J].Nutrients,2020,12(3):773.
[28] YIN J,LI Y Y,HAN H,et al.Melatonin reprogramming of gut microbiota improves lipid dysmetabolism in high-fat diet-fed mice[J].Journal of Pineal Research,2018,65(4):e12524.
[29] 张铮,朱坤,朱伟云,等.发酵饲料对生长育肥猪结肠微生物发酵及菌群组成的影响[J].微生物学报,2019,59(1):93-102. ZHANG Z,ZHU K,ZHU W Y,et al.Effect of a fermented feed on colonic fermentation and microbial composition in finishing pig[J].Acta Microbiologica Sinica,2019,59(1):93-102.(in Chinese)
[30] GUO X,XIA X,TANG R,et al.Development of a real-time PCR method for Firmicutes and Bacteroidetes in faeces and its application to quantify intestinal population of obese and lean pigs[J].Letters in Applied Microbiology,2008,47(5):367-373.  
[31] GUO X L,XIA X J,TANG R Y,et al.Real-time PCR quantification of the predominant bacterial divisions in the distal gut of Meishan and Landrace pigs[J].Anaerobe,2008,14(4):224-228.  
[32] CANI P D.Human gut microbiome:hopes,threats and promises[J].Gut,2018,67(9):1716-1725.  
[33] LUBBS D C,VESTER B M,FASTINGER N D,et al.Dietary protein concentration affects intestinal microbiota of adult cats:a study using DGGE and qPCR to evaluate differences in microbial populations in the feline gastrointestinal tract[J].Journal of Animal Physiology and Animal Nutrition,2009,93(1):113-121.  
[34] PARNELL J A,REIMER R A.Prebiotic fibres dose-dependently increase satiety hormones and alter Bacteroidetes and Firmicutes in lean and obese JCR:LA-cp rats[J].British Journal of Nutrition,2012,107(4):601-613.  
[35] MILLER T L.The pathway of formation of acetate and succinate from pyruvate by Bacteroides succinogenes[J].Archives of Microbiology,1978,117(2):145-152.  
[36] LOUIS P,FLINT H J.Formation of propionate and butyrate by the human colonic microbiota[J].Environmental Microbiology,2017,19(1):29-41.  
[37] SALONEN A,LAHTI L,SALOJÄRVI J,et al.Impact of diet and individual variation on intestinal microbiota composition and fermentation products in obese men[J].ISME Journal,2014,8(11):2218-2230.  
[38] NEISH A S.Microbes in gastrointestinal health and disease[J].Gastroenterology,2009,136(1):65-80.  
[39] ITO T,MIYAMOTO H,KUMAGAI Y,et al.Thermophile-fermented compost extract as a possible feed additive to enhance fecundity in the laying hen and pig:modulation of gut metabolism[J].Journal of Bioscience and Bioengineering,2016,121(6):659-664.  
[40] BLACHIER F,MARIOTTI F,HUNEAU J F,et al.Effects of amino acid-derived luminal metabolites on the colonic epithelium and physiopathological consequences[J].Amino Acids,2007,33(4):547-562.  
[41] JENSEN M T,COX R P,JENSEN B B.Microbial production of skatole in the hind gut of pigs given different diets and its relation to skatole deposition in backfat[J].Animal Science,1995,61(2):293-304.  
[42] LUO Z,LI C B,CHENG Y F,et al.Effects of low dietary protein on the metabolites and microbial communities in the caecal digesta of piglets[J].Archives of Animal Nutrition,2015,69(3):212-226.  
[43] MU C L,YANG Y X,LUO Z,et al.The colonic microbiome and epithelial transcriptome are altered in rats fed a high-protein diet compared with a normal-protein diet[J].The Journal of Nutrition,2016,146(3):474-483.  
[44] YU M,ZHANG C J,YANG Y X,et al.Long-term effects of early antibiotic intervention on blood parameters,apparent nutrient digestibility,and fecal microbial fermentation profile in pigs with different dietary protein levels[J].Journal of Animal Science and Biotechnology,2017,8:60.
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