Applied Microbiology and Biotechnology

, Volume 97, Issue 14, pp 6477–6488 | Cite as

Effects of Clostridium butyricum and Enterococcus faecium on growth performance, lipid metabolism, and cecal microbiota of broiler chickens

  • Xu Zhao
  • Yuming GuoEmail author
  • Shuangshuang Guo
  • Jianzhuang Tan
Applied microbial and cell physiology


To investigate the effects of Clostridium butyricum and Enterococcus faecium on the growth performance, lipid metabolism, and cecal microbiota of broilers, 264 one-day-old male Ross 308 broiler chicks were randomly allocated into four treatments with six replicates in a 2 × 2 factorial arrangement and fed four diets with two levels of C. butyricum (0 or 1 × 109 cfu/kg) and two levels of E. faecium (0 or 2 × 109 cfu/kg) for 42 days. There was no significant interaction between C. butyricum and E. faecium on the growth performance, lipid metabolism, and cecal microbiota of broilers. However, broilers supplemented with E. faecium had lower (P = 0.022) serum leptin level at day 21 and higher (P < 0.001) fatty acid synthase (FAS), malic enzyme (ME), and acetyl–CoA carboxylase (ACC) mRNA levels in the liver at day 42. Supplementation of C. butyricum improved (P < 0.05) the average daily feed intake and average daily gain, increased (P = 0.016) the serum insulin level at 21 days of age, enhanced (P < 0.05) the content of intramuscular fat, activities of FAS in the liver and lipoprotein lipase (LPL) in the breast muscle, mRNA expression of FAS, ME, and ACC in the liver and LPL in the breast muscle at 42 days of age, but reduced (P = 0.030) cecal Bacteroidetes relative abundance at 21 days of age. The results of this study indicate that the increased intramuscular fat content of broilers fed C. butyricum as observed may be the result of enhanced lipogenesis.


C. butyricum E. faecium Broiler Growth Lipid metabolism Microbiota 



This work was supported by the Chinese Universities Scientific Fund and the Yangtz River Scholarship and Innovation Research Team Development Program (Project No. IRT0945).


  1. Angelakis E, Raoult D (2010) The increase of Lactobacillus species in the gut flora of newborn broiler chicks and ducks is associated with weight gain. PLoS One 5:e10463. doi: 10.1371/journal.pone.0010463 CrossRefGoogle Scholar
  2. Awad WA, Ghareeb K, Abdel-Raheem S, Böhm J (2009) Effects of dietary inclusion of probiotic and synbiotic on growth performance, organ weights, and intestinal histomorphology of broiler chickens. Poult Sci 88:49–56. doi: 10.3382/ps.2008-00244 CrossRefGoogle Scholar
  3. Böhmer BM, Branner GR, Roth-Maier DA (2005) Precaecal and faecal digestibility of inulin (DP 10-12) or an inulin/Enterococcus faecium mix and effects on nutrient digestibility and microbial gut flora. J Anim Physiol Anim Nutr (Berl) 89:388–396. doi: 10.1111/j.1439-0396.2005.00530.x CrossRefGoogle Scholar
  4. Cai Y, Song Z, Zhang X, Wang X, Jiao H, Lin H (2009) Increased de novo lipogenesis in liver contributes to the augmented fat deposition in dexamethasone exposed broiler chickens (Gallus gallus domesticus). Comp Biochem Physiol C Toxicol Pharmacol 150:164–169. doi: 10.1016/j.cbpc.2009.04.005 CrossRefGoogle Scholar
  5. Capcarova M, Weiss J, Hrncar C, Kolesarova A, Pal G (2010) Effect of Lactobacillus fermentum and Enterococcus faecium strains on internal milieu, antioxidant status and body weight of broiler chickens. J Anim Physiol Anim Nutr (Berl) 94:e215–e224. doi: 10.1111/j.1439-0396.2010.01010.x CrossRefGoogle Scholar
  6. Chen XL, Wang JK, Wu YM, Liu JX (2008) Effects of chemical treatments of rice straw on rumen fermentation characteristics, fibrolytic enzyme activities and populations of liquid- and solid- associated ruminal microbes in vitro. Anim Feed Sci Technol 141:1–14. doi: 10.1016/j.anifeedsci.2007.04.006 CrossRefGoogle Scholar
  7. Chilliard Y (1993) Dietary fat and adipose tissue metabolism in ruminants, pigs and rodents: a review. J Dairy Sci 76:3897–3931. doi: 10.3168/jds.S0022-0302(93)77730-9 CrossRefGoogle Scholar
  8. Chung CS, Meserole VK, Etherton TD (1983) Temporal nature of insulin binding and insulin-stimulated glucose metabolism in isolated swine adipocytes. J Anim Sci 56:58–63Google Scholar
  9. Corrigan A, Horgan K, Clipson N, Murphy RA (2011) Effect of dietary supplementation with a Saccharomyces cerevisiae mannan oligosaccharide on the bacterial community structure of broiler cecal contents. Appl Environ Microbiol 77:6653–6662. doi: 10.1128/AEM.05028-11 CrossRefGoogle Scholar
  10. Druyan S, Cahaner A, Ashwell CM (2007) The expression patterns of hypoxia-inducing factor subunit α-1, heme oxygenase, hypoxia upregulated protein 1, and cardiac troponin T during development of the chicken heart. Poult Sci 86:2384–2389. doi: 10.3382/ps.2007-00152 CrossRefGoogle Scholar
  11. Dunshea FR, Harris DM, Bauman DE, Boyd RD, Bell AW (1992) Effect of porcine somatotropin on in vivo glucose kinetics and lipogenesis in growing pigs. J Anim Sci 70:141–151Google Scholar
  12. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA (2005) Diversity of the human intestinal microbial flora. Science 308:1635–1638. doi: 10.1126/science.1110591 CrossRefGoogle Scholar
  13. Etherton TD (2000) The biology of somatotropin in adipose tissue growth and nutrient partitioning. J Nutr 130:2623–2625Google Scholar
  14. Fierer N, Jackson JA, Vilgalys R, Jackson RB (2005) Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl Environ Microbiol 71:4117–4120. doi: 10.1128/AEM.71.7.4117-4120.2005 CrossRefGoogle Scholar
  15. Goldberg IJ (1996) Lipoprotein lipase and lipolysis: central roles in lipoprotein metabolism and atherogenesis. J Lipid Res 37:693–707Google Scholar
  16. Greiner T, Bäckhed F (2011) Effects of the gut microbiota on obesity and glucose homeostasis. Trends Endocrinol Metab 22:117–123. doi: 10.1016/j.tem.2011.01.002 CrossRefGoogle Scholar
  17. Guo X, Xia X, Tang R, Zhou J, Zhao H, Wang K (2008a) 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. Lett Appl Microbiol 47:367–373. doi: 10.1111/j.1472-765X.2008.02408.x CrossRefGoogle Scholar
  18. Guo X, Xia X, Tang R, Wang K (2008b) Real-time PCR quantification of the predominant bacterial divisions in the distal gut of Meishan and Landrace pigs. Anaerobe 14:224–228. doi: 10.1016/j.anaerobe.2008.04.001 CrossRefGoogle Scholar
  19. Hermier D (1997) Lipoprotein metabolism and fattening in poultry. J Nutr 127:805S–808SGoogle Scholar
  20. Huang J, Yang D, Gao S, Wang T (2008) Effects of soy-lecithin on lipid metabolism and hepatic expression of lipogenic genes in broiler chickens. Livest Sci 118:53–60. doi: 10.1016/j.livsci.2008.01.014 CrossRefGoogle Scholar
  21. Huang Q, Xu Z, Han X, Li W (2006) Changes in hormones, growth factor and lipid metabolism in finishing pigs fed betaine. Livest Sci 105:78–85. doi: 10.1016/j.livsci.2006.04.031 CrossRefGoogle Scholar
  22. Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI (2005) Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A 102:11070–11075. doi: 10.1073/pnas.0504978102 CrossRefGoogle Scholar
  23. Ley RE, Turnbaugh PJ, Klein S, Gordon JI (2006) Microbial ecology: human gut microbes associated with obesity. Nature 444:1022–1023. doi: 10.1038/4441022a CrossRefGoogle Scholar
  24. Lin SY, Hung ATY, Lu JJ (2011) Effects of supplement with different level of Bacillus coagulans as probiotics on growth performance and intestinal microflora populations of broiler chickens. J Anim Vet Adv 10:111–114. doi: 10.3923/javaa.2011.111.114 CrossRefGoogle Scholar
  25. Liu ZH, Yang FY, Kong LJ, Lai CH, Piao XS, Gu YH, Ou XQ (2007) Effects of dietary energy density on growth, carcass quality and mRNA expression of fatty acid synthase and hormone-sensitive lipase in finishing pigs. Asian-Australas J Anim Sci 20:1587–1593Google Scholar
  26. Louveau I, Gondret F (2004) Regulation of development and metabolism of adipose tissue by growth hormone and the insulin-like growth factor system. Domest Anim Endocrinol 27:241–255. doi: 10.1016/j.domaniend.2004.06.004 CrossRefGoogle Scholar
  27. Lu J, Idris U, Harmon B, Hofacre C, Maurer JJ, Lee MD (2003) Diversity and succession of the intestinal bacterial community of the maturing broiler chicken. Appl Environ Microbiol 69:6816–6824. doi: 10.1128/AEM.69.11.6816-6824.2003 CrossRefGoogle Scholar
  28. Ma HT, Tang X, Tian CY, Zou SX, Huang GQ, Chen WH (2008) Effects of dehydroepiandrosterone on growth performance, lipid metabolic hormones and parameters in broilers. Vet Med (Praha) 53:543–549Google Scholar
  29. Mao H, Wang J, Zhou Y, Liu J (2010) Effects of addition of tea saponins and soybean oil on methane production, fermentation and microbial population in the rumen of growing lambs. Livest Sci 129:56–62. doi: 10.1016/j.livsci.2009.12.011 CrossRefGoogle Scholar
  30. Mersmann HJ, MacNeil MD (1985) Relationship of plasma lipid concentrations to fat deposition in pigs. J Anim Sci 61:122–128Google Scholar
  31. Miao Z, Wang L, Xu Z, Huang J, Wang Y (2008) Developmental patterns in hormone and lipid metabolism of growing Jinhua and Landrace gilts. Can J Anim Sci 88:601–607. doi: 10.4141/CJAS08037 CrossRefGoogle Scholar
  32. Mossab A, Lessire M, Guillaumin S, Kouba M, Mourot J, Peiniau P, Hermier D (2002) Effect of dietary fats on hepatic lipid metabolism in the growing turkey. Comp Biochem Physiol B Biochem Mol Biol 132:473–483. doi: 10.1016/S1096-4959(02)00059-3 CrossRefGoogle Scholar
  33. Mountzouris KC, Tsirtsikos P, Kalamara E, Nitsch S, Schatzmayr G, Fegeros K (2007) Evaluation of the efficacy of a probiotic containing Lactobacillus, Bifidobacterium, Enterococcus, and Pediococcus strains in promoting broiler performance and modulating cecal microflora composition and metabolic activities. Poult Sci 86:309–317Google Scholar
  34. Mountzouris KC, Tsitrsikos P, Palamidi I, Arvaniti A, Mohnl M, Schatzmayr G, Fegeros K (2010) Effects of probiotic inclusion levels in broiler nutrition on growth performance, nutrient digestibility, plasma immunoglobulins, and cecal microflora composition. Poult Sci 89:58–67. doi: 10.3382/ps.2009-00308 CrossRefGoogle Scholar
  35. Murayama T, Mita N, Tanaka M, Kitajo T, Asano T, Mizuochi K, Kaneko K (1995) Effects of orally administered Clostridium butyricum MIYAIRI 588 on mucosal immunity in mice. Vet Immunol Immunopathol 48:333–342. doi: 10.1016/0165-2427(95)05437-B CrossRefGoogle Scholar
  36. Nakanishi S, Tanaka M (2010) Sequence analysis of a bacteriocinogenic plasmid of Clostridium butyricum and expression of the bacteriocin gene in Escherichia coli. Anaerobe 16:253–257. doi: 10.1016/j.anaerobe.2009.10.002 CrossRefGoogle Scholar
  37. National Research Council (1994) Nutrient requirements of poultry, 9th rev. edn. Natl. Acad., Washington, DCGoogle Scholar
  38. Numa S, Nakanishi S, Hashimoto T, Iritani N, Okazaki T (1970) Role of acetyl coenzyme A carboxylase in the control of fatty acid synthesis. Vitam Horm 28:213–243. doi: 10.1016/S0083-6729(08)60895-X CrossRefGoogle Scholar
  39. O'Hea EK, Leveille GA (1968) Lipogenesis in isolated adipose tissue of the domestic chick (Gallus domesticus). Comp Biochem Physiol 26:111–120. doi: 10.1016/0010-406X(68)90317-4 CrossRefGoogle Scholar
  40. Patterson JA, Burkholder KM (2003) Application of prebiotics and probiotics in poultry production. Poult Sci 82:627–631Google Scholar
  41. Pucci E, Chiovato L, Pinchera A (2000) Thyroid and lipid metabolism. Int J Obes Relat Metab Disord 24:S109–S112. doi: 10.1038/sj.ijo.0801292 CrossRefGoogle Scholar
  42. Ramsay TG (2004) Porcine leptin alters isolated adipocyte glucose and fatty acid metabolism. Domest Anim Endocrinol 26:11–21. doi: 10.1016/j.domaniend.2003.07.001 CrossRefGoogle Scholar
  43. Ramsay TG, Yan X, Morrison C (1998) The obesity gene in swine: sequence and expression of porcine leptin. J Anim Sci 76:484–490Google Scholar
  44. Samli HE, Senkoylu N, Koc F, Kanter M, Agma A (2007) Effects of Enterococcus faecium and dried whey on broiler performance, gut histomorphology and intestinal microbiota. Arch Anim Nutr 61:42–49. doi: 10.1080/17450390601106655 CrossRefGoogle Scholar
  45. Samli HE, Dezcan S, Koc F, Ozduven ML, Okur AA, Senkoylu N (2010) Effect of Enterococcus faecium supplementation and floor type on performance, morphology of erythrocytes and intestinal microbiota in broiler chickens. Br Poult Sci 51:564–568. doi: 10.1080/00071668.2010.507241 CrossRefGoogle Scholar
  46. Sanz M, Lopez-Bote CJ, Menoyo D, Bautista JM (2000) Abdominal fat deposition and fatty acid synthesis are lower and β-oxidation is higher in broiler chickens fed diets containing unsaturated rather than saturated fat. J Nutr 130:3034–3037Google Scholar
  47. Sheridan MA, Kao Y (1998) Regulation of metamorphosis-associated changes in the lipid metabolism of selected vertebrates. Amer Zool 38:350–368. doi: 10.1093/icb/38.2.350 Google Scholar
  48. Sun JM, Richards MP, Rosebrough RW, Ashwell CM, McMurtry JP, Coon CN (2006) The relationship of body composition, feed intake, and metabolic hormones for broiler breeder females. Poult Sci 85:1173–1184Google Scholar
  49. Toussant MJ, Wilson MD, Clarke SD (1981) Coordinate suppression of liver acetyl–CoA carboxylase and fatty acid synthetase by polyunsaturated fat. J Nutr 111:146–153Google Scholar
  50. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444:1027–1031. doi: 10.1038/nature05414 CrossRefGoogle Scholar
  51. Voshol PJ, Jong MC, Dahlmans VE, Kratky D, Levak-Frank S, Zechner R, Romijn JA, Havekes LM (2001) In muscle-specific lipoprotein lipase-overexpressing mice, muscle triglyceride content is increased without inhibition of insulin-stimulated whole-body and muscle-specific glucose uptake. Diabetes 50:2585–2590. doi: 10.2337/diabetes.50.11.2585 CrossRefGoogle Scholar
  52. Wang X, Lin H, Song Z, Jiao H (2010) Dexamethasone facilitates lipid accumulation and mild feed restriction improves fatty acids oxidation in skeletal muscle of broiler chicks (Gallus gallus domesticus). Comp Biochem Physiol C Toxicol Pharmacol 151:447–454. doi: 10.1016/j.cbpc.2010.01.010 CrossRefGoogle Scholar
  53. Wise EM, Ball EG (1964) Malic enzyme and lipogenesis. Proc Natl Acad Sci U S A 52:1255–1263. doi: 10.1073/pnas.52.5.1255 CrossRefGoogle Scholar
  54. Yang CM, Cao GT, Ferket PR, Liu TT, Zhou L, Zhang L, Xiao YP, Chen AG (2012) Effects of probiotic, Clostridium butyricum, on growth performance, immune function, and cecal microflora in broiler chickens. Poult Sci 91:2121–2129. doi: 10.3382/ps.2011-02131 CrossRefGoogle Scholar
  55. Yang X, Zhang B, Guo Y, Jiao P, Long F (2010) Effects of dietary lipids and Clostridium butyricum on fat deposition and meat quality of broiler chickens. Poult Sci 89:254–260. doi: 10.3382/ps.2009-00234 CrossRefGoogle Scholar
  56. Young JW, Shrago E, Lardy HA (1964) Metabolic control of enzymes involved in lipogenesis and gluconeogenesis. Biochemistry 3:1687–1692. doi: 10.1021/bi00899a015 CrossRefGoogle Scholar
  57. Zhang B, Yang X, Guo Y, Long F (2011a) Effects of dietary lipids and Clostridium butyricum on the performance and the digestive tract of broiler chickens. Arch Anim Nutr 65:329–339. doi: 10.1080/1745039X.2011.568274 CrossRefGoogle Scholar
  58. Zhang B, Yang X, Guo Y, Long F (2011b) Effects of dietary lipids and Clostridium butyricum on serum lipids and lipid-related gene expression in broiler chickens. Animal 5:1909–1915. doi: 10.1017/S1751731111001066 CrossRefGoogle Scholar
  59. Zhu XY, Zhong T, Pandya Y, Joerger RD (2002) 16S rRNA-based analysis of microbiota from the cecum of broiler chickens. Appl Environ Microbiol 68:124–137. doi: 10.1128/AEM.68.1.124-137.2002 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Xu Zhao
    • 1
  • Yuming Guo
    • 1
    Email author
  • Shuangshuang Guo
    • 1
  • Jianzhuang Tan
    • 1
  1. 1.State Key Laboratory of Animal Nutrition, College of Animal Science and TechnologyChina Agricultural UniversityBeijingPeople’s Republic of China

Personalised recommendations