Progressive response of large intestinal bacterial community and fermentation to the stepwise decrease of dietary crude protein level in growing pigs
- 526 Downloads
The study aimed to determine the effects of reduction of dietary crude protein (CP) level with balanced essential amino acids (EAA) on intestinal bacteria and their metabolites of growing pigs. Forty pigs (initial BW 13.50 ± 0.50 kg, 45 ± 2 days of age) were randomly assigned to four dietary treatments containing CP levels at 20.00% (normal crude protein, NP); 17.16% (medium crude protein, MP); 15.30% (low crude protein, LP); and 13.90% (extremely low crude protein, ELP), respectively. Crystalline AAs were added to meet the EAA requirement of pigs. After 4-week feeding, eight pigs per treatment (n = 8) were randomly selected and slaughtered for sampling of ileal, cecal, and colonic digesta and mucosa. Pigs with moderately reduced CP level had increased bacterial diversity, with the Shannon diversity indices for the colon digesta in the LP group and mucosa in the MP and LP groups significantly (P < 0.05) higher than those in the NP and ELP groups. As the CP level reduces, the Bifidobacterium population were linearly decreased (P < 0.05) both in ileum, cecum, and colon, and the ELP group had the lowest Bifidobacterium population in the cecum and colon, with its value significantly lower than NP and MP groups (P < 0.05). However, the ELP group had the highest population of Escherichia coli in the colon, with its value significantly higher than the LP group (P < 0.05). For bacterial metabolites, as CP level decreased, total short-chain fatty acid (T-SCFA), acetate, and butyrate were linearly increased (linear, P < 0.05) in the ileum, while all SCFAs except formate in the cecum and T-SCFA and acetate in the colon, were linearly decreased (P < 0.05). Reducing CP level led to a linear decrease of microbial crude protein (MCP) in the ileum (P < 0.05) and ammonia in all intestine segments (P < 0.05). The spermidine in cecum and total amines, cadaverine, methylamine, and spermidine in colon were shown a quadratic change (P < 0.05) as dietary CP decreases, with the highest concentration in LP group. These findings suggest that moderate reduction of dietary CP level may benefit large intestinal bacterial community and its fermentation, which was negatively affected by extremely low CP diet.
KeywordsLow-protein diets Crude protein level Intestinal microbiota Microbial metabolites
Compliance with ethical standards
This study was supported by National Key Basic Research Program of China, 973 program (Beijing, grant no. 2013CB127300), Natural Science Foundation of China (31430082). W. Zhu also thanks Jiangsu Collaboration Innovation Center of Meat Production and Processing, Quality and Safety Control for support.
Conflict of interest
The authors declare that they have no competing interests.
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
- Dong G, Zhou A, Yang F, Chen K, Wang K, Dao D (1996) Effect of dietary protein levels on the bacterial breakdown of protein in the large intestine and diarrhoea in early weaned piglets. Acta Vet Zootec Sin 27:293–302Google Scholar
- Drew MD, Van Kessel AG, Estrada AE, Ekpe ED, Zijlstra RT (2002) Effect of dietary cereal on intestinal bacterial populations in weaned pigs. Can Vet J 82:607–609Google Scholar
- Fan P, Li L, Rezaei A, Eslamfam S, Che D, Ma X (2015) Metabolites of dietary protein and peptides by intestinal microbes and their impacts on gut. Curr Protein Pep Sci 16Google Scholar
- Graf D, Cagno RD, Fåk F, Flint HJ, Nyman M, Saarela M, Watzl B (2015) Contribution of diet to the composition of the human gut microbiota. Biochem J 285(Pt 2):477–480Google Scholar
- Hopner T, Knappe J, Jensen BB (1974) Formate determination with formate dehydrogenase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Academic Press, New York, pp 1551–1555Google Scholar
- Htoo JK, Araiza BA, Sauer WC, Rademacher M, Zhang Y, Cervantes M, Zijlstra RT (2007) Effect of dietary protein content on ileal amino acid digestibility, growth performance, and formation of microbial metabolites in ileal and cecal digesta of early-weaned pigs. J Anim Sci 85(12):3303–3312. doi: 10.2527/jas.2007-0105 CrossRefPubMedGoogle Scholar
- Konstantinov SR, Zhu WY, Williams BA, Tamminga S, Vos WM, Akkermans ADL (2003) Effect of fermentable carbohydrates on piglet faecal bacterial communities as revealed by denaturing gradient gel electrophoresis analysis of 16S ribosomal DNA. FEMS 43:225–235Google Scholar
- Manichanh C, Rigottier-Gois L, Bonnaud E, Gloux K, Pelletier E, Frangeul F, Nalin R, Jarrin C, Chardon P, Marteau P, Roca J, Dore J (2006) Reduced diversity of faecal microbiota in Crohn’s disease revealed by a metagenomic approach. Gut 55(2):205–211. doi: 10.1136/gut.2005.073817 CrossRefPubMedPubMedCentralGoogle Scholar
- NRC (2012) Nutrient requirements of swine, 11th edn. Nat Acad Press, WashingtonGoogle Scholar
- Peng X, Hu L, Liu Y, Yan C, Fang ZF, Lin Y, Xu SY, Li J, Wu CM, Chen DW, Sun H, Wu D, Che LQ (2016) Effects of low-protein diets supplemented with indispensable amino acids on growth performance, intestinal morphology and immunological parameters in 13 to 35 kg pigs. Animal 1:1–9. doi: 10.1017/S175173111600099 Google Scholar
- Suda Y, Villena J, Takahashi Y, Hosoya S, Tomosada Y, Tsukida K, Shimazu T, Aso H, Tohno M, Ishida M, Makino S, Ikegami S, Kitazawa H (2014) Immunobiotic Lactobacillus jensenii as immune-health promoting factor to improve growth performance and productivity in post-weaning pigs. BMC Immunol 15:1–18Google Scholar
- Zhang CJ, Yu M, Yang YX, Mu CL, Su Y, Zhu WY (2016b) Differential effect of early antibiotic intervention on bacterial fermentation patterns and mucosal gene expression in the colon of pigs under diets with different protein levels. Appl Microbiol Biotechnol. doi: 10.1007/s00253-016-7985-7 Google Scholar