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Effects of Bacillus subtilis and antibiotic growth promoters on the growth performance, intestinal function and gut microbiota of pullets from 0 to 6 weeks

Published online by Cambridge University Press:  28 February 2020

Y. L. Liu ,
T. Yan ,
X. Y. Li ,
Y. L. Duan ,
X. Yang Open the ORCID record for X. Yang [Opens in a new window]  and
X. J. Yang
Y. L. Liu
Affiliation:
College of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi712100, China
T. Yan
Affiliation:
College of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi712100, China
X. Y. Li
Affiliation:
College of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi712100, China
Y. L. Duan
Affiliation:
College of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi712100, China
X. Yang
Affiliation:
College of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi712100, China
X. J. Yang*
Affiliation:
College of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi712100, China
*
†E-mail: [email protected]
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Abstract

The development of digestive organs and the establishment of gut microbiota in pullets play an important role throughout life. This study was conducted to investigate the effects of Bacillus subtilis (BS) on growth performance, intestinal function and gut microbiota in pullets from 0 to 6 weeks of age. Hy-line Brown laying hens (1-day-old, n = 504) were randomly allotted into four diets with a 2 × 2 factorial design: (1) basal diet group (control); (2) antibiotics group (AGP), the basal diet supplemented with 20 mg/kg Bacitracin Zinc and 4 mg/kg Colistin Sulphate; (3) BS group, the basal diet supplemented with 500 mg/kg BS and (4) mixed group, the basal diet supplemented with both AGP and BS. As a result, when BS was considered the main effect, BS addition (1) reduced the feed conversion ratio at 4 to 6 weeks (P < 0.05); (2) decreased duodenal and jejunal crypt depth at 3 weeks; (3) increased the villus height : crypt depth (V : C) ratio in the duodenum at 3 weeks and jejunal villus height at 6 weeks and (4) increased sucrase mRNA expression in the duodenum at 3 weeks as well as the jejunum at 6 weeks, and jejunal maltase and aminopeptidase expression at 3 weeks. When AGP was considered the main effect, AGP supplementation (1) increased the V : C ratio in the ileum at 3 weeks of age; (2) increased sucrase mRNA expression in the duodenum at 3 weeks as well as the ileum at 6 weeks, and increased maltase expression in the ileum. The BS × AGP interaction was observed to affect average daily feed intake at 4 to 6 weeks, and duodenal sucrase and jejunal maltase expression at 3 weeks. Furthermore, dietary BS or AGP addition improved caecal microbial diversity at 3 weeks, and a BS × AGP interaction was observed (P < 0.05) for the Shannon and Simpson indexes. At the genus level, the relative abundance of Lactobacillus was found to be higher in the mixed group at 3 weeks and in the BS group at 6 weeks. Moreover, Anaerostipes, Dehalobacterium and Oscillospira were also found to be dominant genera in pullets with dietary BS addition. In conclusion, BS could improve intestinal morphology and change digestive enzyme relative expression and caecum microbiota, thereby increasing the efficiency of nutrient utilization. Our findings suggested that BS might have more beneficial effects than AGP in the study, which would provide theoretical evidence and new insight into BS application in layer pullets.

Keywords

chickenprobioticsmicrofloraintestinal morphologydigestive enzyme
Type
Research Article
Information
animal , Volume 14 , Issue 8 , August 2020 , pp. 1619 - 1628
Copyright
© The Animal Consortium 2020

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Footnotes

*

These authors contributed equally to this work.

References

Abdelqader, A, Alfataftah, AR and Daş, G 2013. Effects of dietary Bacillus subtilis and inulin supplementation on performance, eggshell quality, intestinal morphology and microflora composition of laying hens in the late phase of production. Animal Feed Science and Technology 179, 103–111.CrossRefGoogle Scholar
Adil, S and Magray, SN 2012. Impact and manipulation of gut microflora in poultry: a review. Journal of Animal and Veterinary Advances 11, 873–877.CrossRefGoogle Scholar
Awad, WA, Ghareeb, K, Abdel-Raheem, S and Böhm, J 2009. Effects of dietary inclusion of probiotic and synbiotic on growth performance, organ weights, and intestinal histomorphology of broiler chickens. Poultry Science 88, 49–56.CrossRefGoogle ScholarPubMed
Bar-Shira, E, Sklan, D and Friedman, A 2003. Establishment of immune competence in the avian GALT during the immediate post-hatch period. Developmental and Comparative Immunology 27, 147–157.CrossRefGoogle ScholarPubMed
Coloe, PJ, Bagust, TJ and Ireland, L 1984. Development of the normal gastrointestinal microflora of specific pathogen-free chickens. Epidemiology & Infection 92, 79–87.Google ScholarPubMed
Duc, LH, Hong, HA and Cutting, SM 2003. Germination of the spore in the gastrointestinal tract provides a novel route for heterologous antigen delivery. Vaccine 21, 4215–4224.CrossRefGoogle Scholar
Duc, LH, Hong, HA, Uyen, NQ and Cutting, SM 2004. Intracellular fate and immunogenicity of B-subtilis spores. Vaccine 22, 1873–1885.CrossRefGoogle Scholar
Gupta, R, Beg, Q, Khan, S and Chauhan, B 2002. An overview on fermentation, downstream processing and properties of microbial alkaline proteases. Applied Microbiology and Biotechnology 60, 381–395.Google ScholarPubMed
Hong, HA, Le, HD and Cutting, SM 2005. The use of bacterial spore formers as probiotics. FEMS Microbiology Reviews 29, 813–835.CrossRefGoogle ScholarPubMed
Jayaraman, S, Thangavel, G, Kurian, H, Mani, R, Mukkalil, R and Chirakkal, H 2013. Bacillus subtilis PB6 improves intestinal health of broiler chickens challenged with Clostridium perfringens-induced necrotic enteritis. Poultry Science 92, 370–374.CrossRefGoogle ScholarPubMed
Ju, KO, Pajarillo, EAB, Chae, JP, Kim, IH, Dang, SY and Kang, DK 2017. Effects of Bacillus subtilis CSL2 on the composition and functional diversity of the faecal microbiota of broiler chickens challenged with Salmonella gallinarum. Journal of Animal Science and Biotechnology 8, 1–9.Google Scholar
Kaewtapee, C, Burbach, K, Tomforde, G, Hartinger, T, Camarinhasilva, A, Heinritz, S, Seifert, J, Wiltafsky, M, Mosenthin, R and Rosenfelderkuon, P 2017. Effect of Bacillus subtilis and Bacillus licheniformis supplementation in diets with low- and high-protein content on ileal crude protein and amino acid digestibility and intestinal microbiota composition of growing pigs. Journal of Animal Science and Biotechnology 8, 686–700.CrossRefGoogle ScholarPubMed
Knap, I, Kehlet, AB, Bennedsen, M, Mathis, GF, Hofacre, CL, Lumpkins, BS, Jensen, MM, Raun, M and Lay, A 2011. Bacillus subtilis (DSM17299) significantly reduces Salmonella in broilers. Poultry Science 90, 1690–1694.CrossRefGoogle ScholarPubMed
Konikoff, T and Gophna, U 2016. Oscillospira: a central, enigmatic component of the human gut microbiota. Trends in Microbiology 24, 523–524.CrossRefGoogle ScholarPubMed
Kőrösi, MA, Podmaniczky, B, Kürti, P, Glávits, R, Virág, G, Szabó, Z and Farkas, Z 2011. Effect of different concentrations of Bacillus subtilis on immune response of broiler chickens. Probiotics & Antimicrobial Proteins 3, 8–14.CrossRefGoogle Scholar
Lam, KH, Chow, KC and Wong, WK 1998. Construction of an efficient Bacillus subtilis system for extracellular production of heterologous proteins. Journal of Biotechnology 63, 167–177.CrossRefGoogle ScholarPubMed
Lesuisse, E, Schanck, K and Colson, C 1993. Purification and preliminary characterization of the extracellular lipase of Bacillus subtilis 168, an extremely basic pH-tolerant enzyme. The FEBS Journal 216, 155–160.Google ScholarPubMed
Li, X, Wu, S, Li, X, Yan, T, Duan, Y, Yang, X, Duan, Y, Sun, Q and Yang, X 2018. Simultaneous supplementation of Bacillus subtilis and antibiotic growth promoters by stages improved intestinal function of pullets by altering gut microbiota. Frontiers in Microbiology 9, 2328–2343.CrossRefGoogle ScholarPubMed
Liu, Y, Yang, X, Xin, H, Chen, S, Yang, CDuan, Y and Yang, X 2017a. Effects of a protected inclusion of organic acids and essential oils as antibiotic growth promoter alternative on growth performance, intestinal morphology and gut microflora in broilers. Animal Science Journal 88, 1414–1424.CrossRefGoogle ScholarPubMed
Liu, YL, Yin, RQ, Liang, SS, Duan, YL, Yao, JH and Yang, XJ 2017b. Effect of dietary Lycium barbarum polysaccharide on growth performance and immune function of broilers. Journal of Applied Poultry Research 26, 200–208.CrossRefGoogle Scholar
Livak, KJ and Schmittgen, TD 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25, 402–408.CrossRefGoogle Scholar
Maynard, CL, Elson, CO, Hatton, RD and Weaver, CT 2012. Reciprocal interactions of the intestinal microbiota and immune system. Nature 489, 231–241.CrossRefGoogle ScholarPubMed
Mcghee, JR, Mestecky, J, Dertzbaugh, MT, Eldridge, JH, Hirasawa, M and Kiyono, H 1992. The mucosal immune system: from fundamental concepts to vaccine development. Vaccine 10, 75–88.CrossRefGoogle ScholarPubMed
Mendelson, NH 1999. Bacillus subtilis macrofibres, colonies and bioconvection patterns use different strategies to achieve multicellular organization. Environmental Microbiology 1, 471–477.CrossRefGoogle ScholarPubMed
Naghi Shokri, A, Ghasemi, HA and Taherpour, K 2016. Evaluation of Aloe vera and synbiotic as antibiotic growth promoter substitutions on performance, gut morphology, immune responses and blood constitutes of broiler chickens. Animal Science Journal 88, 306–313.CrossRefGoogle ScholarPubMed
Outtrup, H and Norman, BE 1984. Properties and application of a thermostable maltogenic amylase produced by a strain of bacillus modified by recombinant-DNA techniques. Starch/Starke 36, 405–411.CrossRefGoogle Scholar
Pelícia, K, Mendes, AA, Saldanha, ESPB, Pizzolante, CC, Takahashi, SE, Moreira, J, Garcia, RG, Quinteiro, RR, Paz, ICLA and Komiyama, CM 2004. Use of prebiotics and probiotics of bacterial and yeast origin for free-range broiler chickens. Revista Brasileira De Ciência Avícola 6, 163–169.CrossRefGoogle Scholar
Perumalla, AVS, Hettiarachchy, NS and Ricke, SC 2012. Direct-fed microbials and prebiotics for animals. Springer Science & Business Media, New York, NY, USA.Google Scholar
Polansky, O, Sekelova, Z, Faldynova, M, Sebkova, A, Sisak, F and Rychlik, I 2016. Important metabolic pathways and biological processes expressed by chicken cecal microbiota. Applied and Environmental Microbiology 82, 1569–1577.CrossRefGoogle Scholar
Probert, HM and Gibson, GR 2002. Bacterial biofilms in the human gastrointestinal tract. Current Issues in Intestinal Microbiology 3, 23–27.Google ScholarPubMed
Rajput, IR, Li, LY, Xin, X, Wu, BB, Juan, ZL, Cui, ZW, Yu, DY and Li, WF 2013. Effect of Saccharomyces boulardii and Bacillus subtilis B10 on intestinal ultrastructure modulation and mucosal immunity development mechanism in broiler chickens. Poultry Science 92, 956–965.CrossRefGoogle ScholarPubMed
Sen, S, Ingale, SL, Kim, JS, Kim, KH, Kim, YW, Khong, C, Lohakare, JD, Kim, EK, Kim, HS and Kwon, IK 2012. Effect of supplementation of Bacillus subtilis LS 1-2 grown on citrus-juice waste and corn-soybean meal substrate on growth performance, nutrient retention, caecal microbiology and small intestinal morphology of broilers. Research in Veterinary Science 93, 264–268.CrossRefGoogle Scholar
Song, J, Xiao, K, Ke, YL, Jiao, LF, Hu, CH, Diao, QY, Shi, B and Zou, XT 2014. Effect of a probiotic mixture on intestinal microflora, morphology, and barrier integrity of broilers subjected to heat stress. Poultry Science 93, 581–588.CrossRefGoogle ScholarPubMed
Tam, NKM, Uyen, NQ, Hong, HA, Le, HD, Hoa, TT, Serra, CR, Henriques, AO and Cutting, SM 2006. The Intestinal life cycle of Bacillus subtilis and close relatives. Journal of Bacteriology 188, 2692–2700.CrossRefGoogle ScholarPubMed
Xu, ZR, Hu, CH, Xia, MS, Zhan, XA and Wang, MQ 2003. Effects of dietary fructooligosaccharide on digestive enzyme activities, intestinal microflora and morphology of male broilers. Poultry Science 82, 1030–1036.CrossRefGoogle ScholarPubMed
Yang, L, Liu, S, Ding, J, Dai, R, He, C, Xu, K, Honaker, CF, Zhang, Y, Siegel, P and Meng, H 2017. Gut microbiota co-microevolution with selection for host humoral immunity. Frontiers in Microbiology 8, 1243–1254.CrossRefGoogle ScholarPubMed
Yitbarek, A, Echeverry, H, Munyaka, P and Rodriguez-Lecompte, JC 2015. Innate immune response of pullets fed diets supplemented with prebiotics and synbiotics. Poultry Science 94, 1802–1811.CrossRefGoogle ScholarPubMed
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