Asian-Australasian Journal of Animal Sciences

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
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Effect of Feeding Bacillus subtilis natto on Hindgut Fermentation and Microbiota of Holstein Dairy Cows

  • Song, D.J. (College of Animal Science and Technology, Southwest University) ;
  • Kang, H.Y. (College of Animal Science and Technology, Southwest University) ;
  • Wang, J.Q. (State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy Agricultural Sciences) ;
  • Peng, H. (State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy Agricultural Sciences) ;
  • Bu, D.P. (State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy Agricultural Sciences)
  • Received : 2013.08.20
  • Accepted : 2013.10.29
  • Published : 2014.04.01
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Abstract

The effect of Bacillus subtilis natto on hindgut fermentation and microbiota of early lactation Holstein dairy cows was investigated in this study. Thirty-six Holstein dairy cows in early lactation were randomly allocated to three groups: no B. subtilis natto as the control group, B. subtilis natto with $0.5{\times}10^{11}cfu$ as DMF1 group and B. subtilis natto with $1.0{\times}10^{11}cfu$ as DMF2 group. After 14 days of adaptation period, the formal experiment was started and lasted for 63 days. Fecal samples were collected directly from the rectum of each animal on the morning at the end of eighth week and placed into sterile plastic bags. The pH, $NH_3$-N and VFA concentration were determined and fecal bacteria DNA was extracted and analyzed by DGGE. The results showed that the addition of B. subtilus natto at either treatment level resulted in a decrease in fecal $NH_3$-N concentration but had no effect on fecal pH and VFA. The DGGE profile revealed that B. subtilis natto affected the population of fecal bacteria. The diversity index of Shannon-Wiener in DFM1 decreased significantly compared to the control. Fecal Alistipes sp., Clostridium sp., Roseospira sp., beta proteobacterium were decreased and Bifidobacterium was increased after supplementing with B. subtilis natto. This study demonstrated that B. subtilis natto had a tendency to change fecal microbiota balance.

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References

  1. Abe, F., N. Ishibashi, and S. Shimamura. 1995. Effect of administration of Bifidobacteria and lactic acid bacteria to newborn calves and piglets. J. Dairy Sci. 78:2838-2846. https://doi.org/10.3168/jds.S0022-0302(95)76914-4
  2. Berg, E. L., C. J. Fu, J. H. Porter, and M. S. Kerley. 2005. Fructooligosaccharide supplementation on the yearling horse: Effects on fecal pH, microbial content and volatile fatty acid concentrations. J. Anim. Sci. 83:1549-1553.
  3. Bromner, J. M. and D. R. Keeney. 1965. Steam distillation methods of determination of ammonium, nitrate and nitrite. Anal. Chem. Acta. 32:485-495. https://doi.org/10.1016/S0003-2670(00)88973-4
  4. Campbell, J. M., G. C. Fahey, and B. W. Wolf. 1997. Selected indigestible oligosaccharides affect large bowel mass, cecal and fecal short-chain fatty acids, pH and microflora in rats. J. Nutr. 127:130-136.
  5. Cole, N. A., R. N. Clark, R. W. Todd, C. R. Richardson, A. Gueye, L. W. Greene, and K. McBride. 2005. Influence of dietary crude protein concentration and source on potential ammonia emissions from beef cattle manure. J. Anim. Sci. 83:722-731.
  6. de Boer, I. J. M., M. C. J. Smits, H. Mollenhorst, G. van Duinkerken, and G. J. Monteny. 2002. Prediction of ammonia emission from dairy barns using feed characteristics Part 1: Relation between feed characteristics and urinary urea concentration. J. Dairy Sci. 85:3382-3388. https://doi.org/10.3168/jds.S0022-0302(02)74425-1
  7. Erickson, G. E. and T. J. Klopfenstein. 2001. Managing N inputs and the effect on losses following excretion in open-dirt feedlots in Nebraska. Sci. World J. 1(S2):830-835.
  8. FAO/WHO. 2001. Evalution of health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Exper consultation report: Cordoba, Argentina: Food and agriculture organization of the United Nations and World Health Orhanization.
  9. Fox, J. T., B. E. Depenbusch, J. S. Drouillard, and T. G. Nagaraja. 2007. Dry-rolled or steam-flaked grain-based diets and fecal shedding of Escherichia coli O157 in feedlot cattle. J. Anim. Sci. 85:1207-1212. https://doi.org/10.2527/jas.2006-079
  10. Fritts, C. A., J. H. Kersey, M. A. Motl, E. C. Kroger, F. Yan, J. Si, Q. Jiang, M. M. Campos, A. L. Waldroup, and P. W. Waldroup. 2000. Bacillus subtilis C-3102 (Calsporin) improves live performance and microbiological status of broiler chickens. 2000. J. Appl. Poult. Res. 9:149-155. https://doi.org/10.1093/japr/9.2.149
  11. Frizzo, L. S., E. Bertozzi, L. P. Soto, M. V. Zbrun, G. Sequeira, R. D. Santina, R. R. Armesto, and M. R. Rosmini. 2008. The effect of supplementation with three Lactic acid bacteria from bovine origin on growth performance and health status of young calves. J. Anim. Vet. Adv. 7:400-408.
  12. Fromin, N., J. Hamelin, S. Tarnawski, D. Roesti, K. Jourdain-Miserez, N. Forestier, S. Teyssier-Cuvelle, F. Gillet, M. Aragno, and P. Rossi. 2002. Statistical analysis of denaturing gel electrophoresis (DGE) fingerprinting patterns. Environ. Microbiol. 4:634-643. https://doi.org/10.1046/j.1462-2920.2002.00358.x
  13. Fuller, R. 1989. Probiotics in man and animals. J. Appl. Bacteriol. 66:365-378. https://doi.org/10.1111/j.1365-2672.1989.tb05105.x
  14. Guo, X. H., D. F. Li, W. Q. Lu, X. S. Piao, and X. Chen. 2006. Screening of Bacillus strains as potential probiotics and subsequent confirmation of the in vivo effectiveness of Bacillus subtilis MA139 in pigs. Antonie van Leeuwenhoek 90:139-146. https://doi.org/10.1007/s10482-006-9067-9
  15. Holzapfel, W. H., P. Haberer, R. Geisen, J. Bjorkroth, and U. Schillinger. 2001. Taxonomy and important features of probiotic microorganisms in food and nutrition. Am. J. Clin. Nutr. 73(Suppl.):365S-373S.
  16. Hong, H. A., L. H. Duc, and S. M. Cutting. 2005. The use of bacterial spore formers as probiotics. FEMS Microbiol. Rev. 29:813-835. https://doi.org/10.1016/j.femsre.2004.12.001
  17. Hosoi, T., A. Ametani, K. Kiuchi, and S Kaminogawa. 2000. Improved growth and viability of lactobacilli in the presence of Bacillus subtilis (natto), catalase, or subtilisin. Can. J. Microbiol. 46:892-897. https://doi.org/10.1139/w00-070
  18. Jin, L. Z., Y. W. Ho, N. Abdullah, and S. Jalaludin. 1997. Probiotics in poultry: modes of action. Worlds Poult. Sci. J. 53: 351-368. https://doi.org/10.1079/WPS19970028
  19. Krehbiel, C. R., S. R. Rust, G. Zhang, and S. E. Gilliland. 2003. Bacterial direct-fed microbials in ruminant diets: Performance response and mode of action. J. Anim. Sci. 81(E. Suppl. 2): E120-E132.
  20. La Ragione, R. M., G. Casula, S. M. Cutting, and M. J. Woodward. 2001. Bacillus subtilis spores competitively exclude Escherichia coli O78:K80 in poultry. Vet. Microbiol. 79:133-142. https://doi.org/10.1016/S0378-1135(00)00350-3
  21. Lema, M., L. Williams, and D. R. Rao. 2001. Reduction of fecal shedding of enterohemorrhagic Escherichia coli O157:H7 in lambs by feeding microbial feed supplement. Small Rumin. Res. 39:31-39. https://doi.org/10.1016/S0921-4488(00)00168-1
  22. Leser, T. D. and L. Molbak. 2009. Better living through microbial action: the benefits of the mammalian gastrointestinal microbiota on the host. Environ. Microbiol. 11:2194-2206. https://doi.org/10.1111/j.1462-2920.2009.01941.x
  23. Maruta, K., H. Miyazaki, Y. Tadano, S. Masuda, A. Suzuki, H. Takahashi, and M. Takahashi. 1996. Effects of Bacillus subtilis C-3102 intake on fecal flora of sows and on diarrhea and mortality rate of their piglets. Anim. Sci. Technol. 67:403-409.
  24. Medina, B., I. D. Girard, E. Jacotot, and V. Julliand. 2002. Effect of preparation of Saccharomyces cerevisiae on microbial profiles and fermentation patterns in the large intestine of horses fed a high fiber or high starch diet. J. Anim. Sci. 80:2600-2609.
  25. Meyer, P. M., A. Vaz Pires, A. R. Vagadlo, J. M. Correia de Simas, and I. Susin. 2001. Adicao de probiotico ao leite integral ou sucedaneo e desempenho de bezerros da raca holandesa. Scientia Agricola 58:215-221. https://doi.org/10.1590/S0103-90162001000200001
  26. Miettinen, M., J. Vuopio-Varkila, and K. Varkila. 1996. Production of human tumor necrosis factor alpha, interleukin-6, and interleu-kin-10 is induced by lactic acid bacteria. Infect. Immun. 64:5403-5405.
  27. Mohammed, N., N. Ajisaka, Z. A. Lila, K. Hara, K. Mikuni, K. Hara, S. Kanda, and H. Itabashi. 2004. Effect of Japanese horseradish oil on methane production and ruminal fermentation in vitro and in steers. J. Anim. Sci. 82:1839-1846.
  28. Muyzer, G., A. Teske, C. O. Wirsen, and H. W. Jannasch. 1995. Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments. Arch Microbiol. 164:165-172. https://doi.org/10.1007/BF02529967
  29. Ozawa, K., H. Yokota, M. Kimura, and T. Mitsuoka. 1981. Effects of administration of Bacillus subtilis strain BN on intestinal flora of weanling piglets. Nippon Juigaku Zasshi 43:771-775. https://doi.org/10.1292/jvms1939.43.771
  30. Qiao, G. H., A. S. Shan, N. Ma, Q. Q. Ma, and Z. W. Sun. 2010. Effect of supplemental Bacillus cultures on rumen fermentation and milk yield in Chinese Holstein cows. J. Anim. Physiol. Anim. Nutr. 94:429-436.
  31. Qin, Z. H., J. P. Cai, and X. H. Ye. 2005. Cloning and phylogenetic analysis of 16S rRNA gene of Bacillus subtilis natto. Chinese J. Microecol. 17:324-326.
  32. Santoso,U., K Tanaka, and S. Ohtani. 1995. Effect of dried Bacillus subtilis culture on growth, body composition and hepatic lipogenic enzyme activity in female broiler chicks. Br. J. Nutr. 74:523-529. https://doi.org/10.1079/BJN19950155
  33. Santoso,U., S. Ohtani, K. Tanaka, and M. Sakaida. 1999. Dried Bacillus subtilis culture reduced ammonia gas release in poultry house. Asian-Aus. J. Anim. Sci. 12:806-809. https://doi.org/10.5713/ajas.1999.806
  34. Scot, E. D., T. R Callaway, R. D Wolcott, S.Yan, M. Trevor, G. H. Robert, and S. E. Thomas. 2008. Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol. 8:125. https://doi.org/10.1186/1471-2180-8-125
  35. Spellerberg, I. F. and P. J. Fedor. 2003. A tribute to Claude Shannon (1916-2001) and a plea for more rigorous use of species richness, species diversity and the 'Shannon-Wiener' Index. Global Ecol. Biogeogr. 12:177-179. https://doi.org/10.1046/j.1466-822X.2003.00015.x
  36. Spiehs, M. J. and V. H. Varel. 2009. Nutrient excretion and odorant production in manure from cattle fed corn wet distillers grains with solubles. J. Anim. Sci. 87:2977-2984. https://doi.org/10.2527/jas.2008-1584
  37. Stefan J. Green. 2005. A guide to denaturing gradient gel electrophoresis. Version 1-Nov 21.
  38. Stephens, T. P., G. H. Longeragan, E. Karunasena, and M. M. Brashears. 2007. Reduction of Escherichia coli O157 and Salmonella in feces and on hides of feedlot cattle using various doses of a direct-fed microbial. J. Food Prot. 70:2386-2391.
  39. Sumi, H. 1997. Antibacterial activity of Bacillus natto-growth inhibition against Eschricchia coli O-157. Biosci. 14:47-50.
  40. Sun, P., J. Q. Wang, and H. T. Zhang. 2010. Effects of Bacillus subtilis natto on performance and immune function of preweaning calves. J. Dairy Sci. 93:5851-5855 https://doi.org/10.3168/jds.2010-3263
  41. Swyers, K. L., A. O. Burk, T. G. Hartsock, E. M. Ungerfeld, and J. L. Shelton. 2008. Effects of direct-fed microbial supplementation on digestibility and fermentation end-products in horses fed low- and high-starch concentrates. J. Anim. Sci. 86:2596-2608. https://doi.org/10.2527/jas.2007-0608
  42. Tannock, G. W. 2001. Molecular assessment of intestinal microflora. Am. J. Clin. Nutr. 73:410-414.
  43. Teo, A.Y. L. and H. M. Tan. 2005. Inhibition of Clostridium perfringens by a novel strain of Bacillus subtilis isolated from the gastrointestinal tracts of healthy chickens. Appl. Environ. Microbiol. 71:4185-4190. https://doi.org/10.1128/AEM.71.8.4185-4190.2005
  44. Teo, A.Y. L. and H. M. Tan. 2006. Effect of Bacillus subtilis PB6 (CloSTAT)on broilers infected with a pathogenic strain of Escherichia coli. J. Appl. Poult. Res. 15:229-235. https://doi.org/10.1093/japr/15.2.229
  45. Timmerman, H. M., L. Mulder, H. Everts, D. C. van Espen, E. van der Wal, G. Klaassen, S. M. G. Rouwers, R. Hartemink, F. M. Rombouts, and A. C. Beynen. 2005. Health and growth of veal calves fed milk replacers with or without probiotics. J. Dairy Sci. 88:2154-2165. https://doi.org/10.3168/jds.S0022-0302(05)72891-5
  46. Walter, J., N. C. Heng, W. P. Hammes, D. M. Loach, G. W. Tannock, and C. Hertel. 2003. Identification of Lactobacillus reuteri genes specifically induced in the mouse gastrointestinal tract. Appl. Environ. Microbiol. 69:2044-2051. https://doi.org/10.1128/AEM.69.4.2044-2051.2003
  47. Wehnes, C. A., K. N. Novak, V. Patskevich, D. R. Shields, J. A. Coalson, Smith, M. E. Davis, and T. G. Rehberger. 2009. Benefits of supplementation of an electrolyte scour treatment with a Bacillus-based direct-fed microbial for calves. Probiotics Antimicrob. Proteins 1:36-44. https://doi.org/10.1007/s12602-008-9004-5
  48. Whitley, N. C., D. Cazac, B. J. Rude, D. Jackson-O'Brien, and S. Parveen. 2009. Use of a commercial probiotic supplement in meat goats. J. Anim. Sci. 87:723-728.
  49. Yu, Z. T. and M. Mark. 2004. Comparisons of different hypervariable regions of rrs genes for Use in fingerprinting of microbial communities by PCR-denaturing gradient gel electrophoresis. Appl. Environ. Microbiol. 70:4800-4806. https://doi.org/10.1128/AEM.70.8.4800-4806.2004

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