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Journal of Integrative Agriculture  2017, Vol. 16 Issue (06): 1383-1392    DOI: 10.1016/S2095-3119(16)61510-1
Animal Science · Veterinary Science Advanced Online Publication | Current Issue | Archive | Adv Search |
Effects of different proportions of two Bacillus sp. on the growth performance, small intestinal morphology, caecal microbiota and plasma biochemical profile of Chinese Huainan Partridge Shank chickens
YANG Jia-jun, QIAN Kun, WU Dong, ZHANG Wei, WU Yi-jing, XU Ya-yuan

Institute of Animal Husbandry and Veterinary Medicine, Anhui Academy of Agricultural Sciences, Hefei 230031, P.R.China

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Abstract  A total of 900 one-d-old Chinese Huainan Partridge Shank chickens were randomly allocated into nine groups with five replicates of 20 each.  Birds were fed with basal diet, basal diet supplemented with 150 mg kg–1 aureomycin, basal diet supplemented with different proportions of Bacillus licheniformis and Bacillus subtilis, which was 0:1.0×106, 2.5×105:7.5×105, 3.3×105:6.6×105, 5.0×105:5.0×105, 6.6×105:3.3×105, 7.5×105:2.5×105 and 1.0×106:0, respectively.  The duration of the experiment was 56 d.  The results indicated that dietary supplementation of 6.6×105:3.3×105 of B. lichenifornis:B. subtilis improved final body weight, increased the average daily gain, and reduced feed/gain ratio (P<0.05).  The numbers of total Lactobacillus and Bifidobacterium sp. in the caecum significantly increased, and the numbers of Escherichia coli and Salmonella sp. significantly declined compared to that of the control (P<0.05).  Intestinal villous height and villous height to crypt depth ratio of the duodenum, jejunum, and ileum were significantly higher than that of the control, and intestinal crypt depth of the duodenum and ileum was significantly lower (P<0.05).  The total antioxidant capacity, total superoxide dismutase, and glutathione peroxidase ability in plasma significantly improved, while the malondialdehyde concentration in plasma decreased (P<0.05).  Compared to the control, plasma concentrations of ammonia, uric acid and urea nitrogen and the activity of xanthine oxidase were reduced (P<0.05).  In conclusion, an inclusion of 6.6×105:3.3×105 of B. licheniformis: B. subtilis to the diet improved the growth performance, caecal microbiota, plasma biochemical profile, and significantly improved the small intestine morphology, while reducing the mortality rate. 
Keywords:  two-strain Bacillus      proportion      growth performance      small intestinal morphology      biochemical profile  
Received: 21 June 2016   Accepted:

The work was supported by the fund of Doctor Startup Project in Anhui Academy of Agricultural Sciences of China and the Project of Anhui Poultry Technology Committee, China (AHCYTX-10).

Corresponding Authors:  QIAN Kun, Tel: +86-551-62160275, E-mail:   
About author:  YANG Jia-jun, Tel: +86-551-62160012, E-mail:

Cite this article: 

YANG Jia-jun, QIAN Kun, WU Dong, ZHANG Wei, WU Yi-jing, XU Ya-yuan. 2017. Effects of different proportions of two Bacillus sp. on the growth performance, small intestinal morphology, caecal microbiota and plasma biochemical profile of Chinese Huainan Partridge Shank chickens. Journal of Integrative Agriculture, 16(06): 1383-1392.

Abriouel H, Franz C M, Omar N B, Galvez A. 2011. Diversity and applications of Bacillus bacteriocins. FEMS Microbiology Reviews, 35, 201–232.
Awad W, Ghareeb K, Bohm J. 2008. Intestinal structure and function of broiler chickens on diets supplemented with a synbiotic containing Enterococcus faecium and oligosaccharides. International Journal of Molecular Sciences, 9, 2205–2216.
Bader J, Albin A, Stahl U. 2012. Spore-forming bacteria and their utilization as probiotics. Benefical Microbes, 3, 67–75.
Barbosa T M, Serra C R, La Ragione R M, Woodward M J, Henriques A O. 2005. Screening for Bacillus isolates in the broiler gastrointestinal tract. Applied and Environmental Microbiology, 71, 968–978.
Chapman C M, Gibson G R, Rowland I. 2011. Health benefits of probiotics: Are mixtures more effective than single strains? European Journal of Nutrition, 50, 1–17.
Choe D W, Loh T C, Foo H L, Hair-Bejo M, Awis Q S. 2012. Egg production, faecal pH and microbial population, small intestine morphology, and plasma and yolk cholesterol in laying hens given liquid metabolites produced by Lactobacillus plantarum strains. British Poultry Science, 53, 106–135.
Engin K N, Yemisci B, Yigit U, Agachan A, Coskun C. 2010. Variability of serum oxidative stress biomarkers relative to biochemical data and clinical parameters of glaucoma patients. Molecular Vision, 16, 1260–1271.
Giannenas I, Papadopoulos E, Tsalie E, Triantafillou E, Henikl S, Teichmann K, Tontis D. 2012. Assessment of dietary supplementation with probiotics on performance, intestinal morphology and microflora of chickens infected with Eimeria tenella. Veterinary Parasitology, 188, 31–40.
Guarner F, Malagelada J R. 2003. Gut flora in health and disease. Lancet, 361, 512–519.
Hagedorn S R, Bradley G, Chapman P J. 1985. Glutathione-independent isomerization of maleylpyruvate by Bacillus megaterium and other Gram-positive bacteria. Journal of Bacteriology, 163, 640–647.
Hill C, Guarner F, Reid G, Gibson G R, Merenstein D J, Pot B, Morelli L, Canani R B, Flint H J, Salminen S, Calder P C, Sanders M E. 2014. Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nature Reviews Gastroenterology & Hepatology, 11, 506–514.
Hooper L V, Gordon J I. 2001. Commensal host-bacterial relationships in the gut. Science, 292, 1115–1158.
Hu Y, Dun Y, Li S, Zhao S, Peng N, Liang Y. 2014. Effects of Bacillus subtilis KN–42 on growth performance, diarrhea and faecal bacterial flora of weaned piglets. Asian-Australasian Journal of Animal Sciences, 27, 1131–1140.
Huang M K, Choi Y J, Houde R, Lee J W, Lee B, Zhao X. 2004. Effects of Lactobacilli and an acidophilic fungus on the production performance and immune responses in broiler chickens. Poultry Science, 83, 788–795.
Jiang Y B, Yin Q Q, Yang Y R. 2009. Effect of soybean peptides on growth performance, intestinal structure and mucosal immunity of broilers. Journal of Animal Physiology and Animal Nutrition, 93, 754–760.
Kim J S, Ingale S L, Kim Y W, Kim K H, Sen S, Ryu M H, Lohakare J D, Kwon IK, Chae B J. 2011. Effect of supplementation of multi-microbe probiotic product on growth performance, apparent digestibility, cecal microbiota and small intestinal morphology of broilers. Journal of Animal Physiology and Animal Nutrition, 96, 618–626.
Lei K, Li Y L, Yu D Y, Rajput I R, Li W F. 2013. Influence of dietary inclusion of Bacillus licheniformis on laying performance, egg quality, antioxidant enzyme activities, and intestinal barrier function of laying hens. Poultry Science, 92, 2389–2395.
Li L, Xu C L, Ji C, Ma Q, Hao K, Jin Z Y, Li K. 2006. Effects of a dried Bacillus subtilis culture on egg quality. Poultry Science, 85, 364–368.
Li Q F, Wang L L, Shah S B, Jayanty R K, Bloomfield P. 2014. Ammonia concentrations and modeling of inorganic particulate matter in the vicinity of an egg production facility in Southeastern USA. Environmental Science and Pollution Research International, 21, 4675–4685.
Lin M Y, Chang F J. 2000. Antioxidative effect of intestinal bacteria Bifidobacterium longum ATCC 15708 and Lactobacillus acidophilus ATCC 4356. Digestive Disease and Science, 45, 1617–1622.
Loh T C, Thanh N T, Foo H L, Hair-Bejo M, Azhar B K. 2010. Feeding of different levels of metabolite combinations produced by Lactobacillus plantarum on growth performance, fecal microflora, volatile fatty acids and villi height in broilers. Animal Science Journal, 81, 205–214.
Ma Q G, Gao X, Zhou T, Zhao L H, Fan Y, Li X Y, Lei Y P, Ji C, Zhang J Y. 2012. Protective effect of Bacillus subtilis ANSB060 on egg quality, biochemical and histopathological changes in layers exposed to aflatoxin B1. Poultry Science, 91, 2852–2857.
Mappley L J, Tchorzewska M A, Cooley W A, Woodward M J, La Ragione R M. 2011. Lactobacilli antagonize the growth, motility, and adherence of Brachyspira pilosicoli: A potential intervention against avian intestinal spirochetosis. Applied and Environmental Microbiology, 77, 5402–5411.
Menon D G, Bennett D C, Schaefer A M, Cheng K M. 2013. Hematological and serum biochemical profile of farm emus (Dromaius novaehollandiae) at the onset of their breeding season. Poultry Science, 92, 935–944.
Moeller R, Setlow P, Reitz G, Nicholson W L. 2009. Roles of small, acid-soluble spore proteins and core water content in survival of Bacillus subtilis spores exposed to environmental solar UV radiation. Applied and Environmental Microbiology, 75, 5202–5208.
Morelli L. 2007. In vitro assessment of probiotic bacteria: From survival to functionality. International Dairy Journal, 17, 1278–1283.
Mountzouris K C, 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. Poultry Science, 86, 309–317.
Mountzouris K C, 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. Poultry Science, 89, 58–67.
NRC (National Research Council). 1994. Nutrient Requirement of Poultry. 9th ed. National Academy Press, USA.
Nicholson W L. 2002. Roles of Bacillus endospores in the environment. Cellular and Molecular Life Sciences, 59, 410–416.
Ogawa F, Shimizu K, Muroi E, Hara T, Sato S. 2011. Increasing levels of serum antioxidant status, total antioxidant power, in systemic sclerosis. Clinical Rheumatology, 30, 921–925.
Ohno A, Ano T, Shoda M. 1995. Effect of temperature on production of lipopeptide antibiotics, iturin A and surfactin by a dual producer, Bacillus subtilis RB14, in solid-state fermentation. Journal of Fermentation and Bioengineering, 80, 517–519.
O’Shea C J, Sweeney T, Bahar B, Ryan M T, Thornton K, O’Doherty J V. 2012. Indices of gastrointestinal fermentation and manure emissions of growing-finishing pigs as influenced through singular or combined consumption of Lactobacillus plantarum and inulin. Journal of Animal Science, 90, 3848–3857.
Rozs M, Manczinger L, Vágvölgyi C, Kevei F. 2001. Secretion of a trypsin-like thiol protease by a new keratinolytic strain of Bacillus licheniformis. FEMS Microbiology Letters, 205, 221–224.
Samanya M, Yamauchi K E. 2002. Histological alterations of intestinal villi in chickens fed dried Bacillus subtilis var. natto. Comparative Biochemistry and Physiology (A - Molecular & Integrative Physiology), 133, 95–104.
Santoso U, Tanaka K, Ohtani S. 1995. Effect of dried Bacillus subtilis culture on growth, body composition and hepatic lipogenic enzyme activity in female broiler chicks. British Journal of Nutrition, 74, 523–529.
Schöttker B, Zhang Y, Heiss J A, Butterbach K, Jansen E H, Bewerunge-Hudler M, Saum K U, Holleczek B, Brenner H. 2015. Discovery of a novel epigenetic cancer marker related to the oxidative status of human blood. Genes Chromosomes and Cancer, 54, 583–594.
Sharifi S D, Dibamehrb A, Lotfollahian H, Baurhoo B. 2012. Effects of flavomycin and probiotic supplementation to diets containing different sources of fat on growth performance, intestinal morphology, apparent metabolizable energy, and fat digestibility in broiler chickens. Poultry Science, 91, 918–927.
Shim Y H, Ingale S L, Kim J S, Kim K H, Seo D K, Lee S C, Chae B J, Kwon I K. 2012. A multi-microbe probiotic formulation processed at low and high drying temperatures: Effects on growth performance, nutrient retention and caecal microbiology of broilers. British Poultry Science, 53, 482–490.
Tannock G W. 2001. Molecular assessment of intestinal microflora. American Journal of Clinical Nutrition, 73, 410S–414S.
Vila B, Fontgibell A, Badiola I, Esteve-Garcia E, Jimenez G, Castillo M, Brufau J. 2009. Reduction of Salmonella enterica var. enteritidis colonization and invasion by Bacillus cereus var. toyoi inclusion in poultry feeds. Poultry Science, 88, 975–979.
Xu Z R, Hu C H, Xia M S, Zhan X A, Wang M Q. 2003. Effects of dietary fructooligosaccharide on digestive enzyme activities, intestinal microflora and morphology of male broilers. Poultry Science, 82, 1030–1036.
Yang G Y, Zhu Y H, Zhang W, Zhou D, Zhai C C, Wang J F. 2016. Influence of orally fed a select mixture of Bacillus probiotics on intestinal T-cell migration in weaned MUC4 resistant pigs following Escherichia coli challenge. Veterinary Research, 47, 71–85.
Yang J J, Huang K H, Qin S Y, Wu X S, Zhao Z P, Chen F. 2009. Antibacterial action of selenium-enriched probiotics against pathogenic Escherichia coli. Digestive Disease and Science, 54, 246–254. 
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