International Journal of Bacteriology
Volume 2013 (2013), Article ID 958408, 8 pages
http://dx.doi.org/10.1155/2013/958408
Research Article

Physiological Properties and Salmonella Growth Inhibition of Probiotic Bacillus Strains Isolated from Environmental and Poultry Sources

Department of Poultry Science, University of Arkansas, Fayetteville, AR 72701, USA

Received 15 March 2013; Accepted 10 May 2013

Academic Editor: Ramakrishna Nannapaneni

Copyright © 2013 Anita Menconi et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. H. A. Hong, H. D. Le, and S. M. Cutting, “The use of bacterial spore formers as probiotics,” FEMS Microbiology Reviews, vol. 29, no. 4, pp. 813–835, 2005. View at Publisher · View at Google Scholar · View at Scopus
  2. A. Jadamus, W. Vahjen, K. Schäfer, and O. Simon, “Influence of the probiotic strain Bacillus cereus var. toyoi on the development of enterobacterial growth and on selected parameters of bacterial metabolism in digesta samples of piglets,” Journal of Animal Physiology and Animal Nutrition, vol. 86, no. 1-2, pp. 42–54, 2002. View at Publisher · View at Google Scholar · View at Scopus
  3. H. Kasper, “Protection against gastrointestinal diseases—present facts and future developments,” International Journal of Food Microbiology, vol. 41, no. 2, pp. 127–131, 1998. View at Publisher · View at Google Scholar · View at Scopus
  4. R. D. Sleatorand and C. Hill, “New frontiers in probiotic research,” Letters in Applied Microbiology, vol. 46, pp. 143–147, 2008. View at Google Scholar
  5. R. D. Rolfe, “The role of probiotic cultures in the control of gastrointestinal health,” Journal of Nutrition, vol. 130, pp. 396S–402S, 2000. View at Google Scholar
  6. C. H. Liu, C. H. Chiu, S. W. Wang, and W. Cheng, “Dietary administration of the probiotic, Bacillus subtilis E20, enhances the growth, innate immune responses, and disease resistance of the grouper, Epinephelus coioides,” Fish & Shellfish Immunology, vol. 33, no. 4, pp. 699–706, 2012. View at Google Scholar
  7. K. Kobayashi, “Chemotherapy-induced diarrhea,” Cancer & Chemotherapy, vol. 30, no. 6, pp. 765–771, 2003. View at Google Scholar · View at Scopus
  8. D. M. F. Savarese, G. Savy, L. Vahdat, P. E. Wischmeyer, and B. Corey, “Prevention of chemotheraphy and radiation toxicity with glutamine,” Cancer Treatment Reviews, vol. 29, no. 6, pp. 501–513, 2003. View at Publisher · View at Google Scholar · View at Scopus
  9. C. McGough, C. Baldwin, G. Frost, and H. J. N. Andreyev, “Role of nutritional intervention in patients treated with radiotherapy for pelvic malignancy,” British Journal of Cancer, vol. 90, no. 12, pp. 2278–2287, 2004. View at Google Scholar · View at Scopus
  10. L. M. Noriega, P. van der Auwera, D. Daneau, F. Meunier, and M. Aoun, “Salmonella infections in a cancer center,” Supportive Care in Cancer, vol. 2, no. 2, pp. 116–122, 1994. View at Publisher · View at Google Scholar · View at Scopus
  11. J. Delaloye, G. Merlani, C. Petignat et al., “Nosocomial nontyphoidal salmonellosis after antineoplastic chemotherapy: reactivation of asymptomatic colonization?” European Journal of Clinical Microbiology and Infectious Diseases, vol. 23, no. 10, pp. 751–758, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. E. I. Benchimol and D. R. Mack, “Probiotics in relapsing and chronic diarrhea,” Journal of Pediatric Hematology/Oncology, vol. 26, no. 8, pp. 515–517, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. M. W. Hull and P. L. Beck, “Clostridium difficile—associated colitis,” Canadian Family Physician, vol. 50, pp. 1536–1545, 2004. View at Google Scholar · View at Scopus
  14. D. Czerucka and P. Rampal, “Experimental effects of Saccharomyces boulardii on diarrheal pathogens,” Microbes and Infection, vol. 4, no. 7, pp. 733–739, 2002. View at Publisher · View at Google Scholar · View at Scopus
  15. D. Czerucka, S. Dahan, B. Mograbi, B. Rossi, and P. Rampal, “Saccharomyces boulardii preserves the barrier function and modulates the signal transduction pathway induced in enteropathogenic Escherichia coli-infected T84 cells,” Infection and Immunity, vol. 68, no. 10, pp. 5998–6004, 2000. View at Publisher · View at Google Scholar · View at Scopus
  16. N. K. Lee, J. S. Park, E. Park, and H. D. Paik, “Adherence and anticarcinogenic effects of Bacillus polyfermenticus SCD in the large intestine,” Letters in Applied Microbiology, vol. 44, no. 3, pp. 274–278, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. S. V. Malkov, V. V. Markelov, G. Y. Polozov, B. I. Barabanschikov, A. Y. Kozhevnikov, and M. V. Trushin, “Significant delay of lethal outcome in cancer patients due to peroral administration of Bacillus oligonitrophilus KU-1,” TheScientificWorldJournal, vol. 6, pp. 2177–2187, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. E. Park, G. I. Jeon, J. S. Park, and H. D. Paik, “A probiotic strain of Bacillus polyfermenticus reduces DMH induced precancerous lesions in F344 male rat,” Biological and Pharmaceutical Bulletin, vol. 30, no. 3, pp. 569–574, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. L. O'Mahony, M. Feeney, S. O'Halloran et al., “Probiotic impact on microbial flora, inflammation and tumour development in IL-10 knockout mice,” Alimentary Pharmacology and Therapeutics, vol. 15, no. 8, pp. 1219–1225, 2001. View at Publisher · View at Google Scholar · View at Scopus
  20. M. C. Urdaci, P. Bressollier, and I. Pinchuk, “Bacillus clausii probiotic strains: antimicrobial and immunomodulatory activities,” Journal of clinical gastroenterology, vol. 38, no. 6, pp. S86–S90, 2004. View at Google Scholar · View at Scopus
  21. T. M. Barbosa, C. R. Serra, R. M. La Ragione, M. J. Woodward, and A. O. Henriques, “Screening for Bacillus isolates in the broiler gastrointestinal tract,” Applied and Environmental Microbiology, vol. 71, no. 2, pp. 968–978, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. L. H. Duc, H. A. Hong, T. M. Barbosa, A. O. Henriques, and S. M. Cutting, “Characterization of Bacillus probiotics available for human use,” Applied and Environmental Microbiology, vol. 70, no. 4, pp. 2161–2171, 2004. View at Publisher · View at Google Scholar · View at Scopus
  23. P. Permpoonpattana, H. A. Hong, R. Khaneja, and S. M. Cutting, “Evaluation of Bacillus subtilis strains as probiotics and their potential as a food ingredient,” Beneficial Microbes, vol. 3, no. 2, pp. 127–135, 2012. View at Google Scholar
  24. L. H. Duc, H. A. Hong, and S. M. Cutting, “Germination of the spore in the gastrointestinal tract provides a novel route for heterologous antigen delivery,” Vaccine, vol. 21, no. 27–30, pp. 4215–4224, 2003. View at Publisher · View at Google Scholar · View at Scopus
  25. L. H. Duc, H. A. Hong, N. Fairweather, E. Ricca, and S. M. Cutting, “Bacterial spores as vaccine vehicles,” Infection and Immunity, vol. 71, no. 5, pp. 2810–2818, 2003. View at Publisher · View at Google Scholar · View at Scopus
  26. T. T. Hoa, L. H. Duc, R. Isticato et al., “Fate and dissemination of Bacillus subtilis spores in a murine model,” Applied and Environmental Microbiology, vol. 67, no. 9, pp. 3819–3823, 2001. View at Publisher · View at Google Scholar · View at Scopus
  27. G. Casula and S. M. Cutting, “Bacillus probiotics: spore germination in the gastrointestinal tract,” Applied and Environmental Microbiology, vol. 68, no. 5, pp. 2344–2352, 2002. View at Publisher · View at Google Scholar · View at Scopus
  28. R. E. Wolfenden, N. R. Pumford, M. J. Morgan et al., “Evaluation of a screening and selection method for bacillus isolates for use as effective direct-fed microbials in commercial poultry,” International Journal of Poultry Science, vol. 9, no. 4, pp. 317–323, 2010. View at Google Scholar · View at Scopus
  29. S. E. Gilliland, T. E. Staley, and L. J. Bush, “Importance of bile tolerance of Lactobacillus acidophilus used as a dietary adjunct,” Journal of dairy science, vol. 67, no. 12, pp. 3045–3051, 1984. View at Google Scholar · View at Scopus
  30. G. Tellez, C. E. Dean, D. E. Corrier, J. R. Deloach, L. Jaeger, and B. M. Hargis, “Effect of dietary lactose on cecal morphology, pH, organic acids, and Salmonella enteritidis organ invasion in Leghorn chicks,” Poultry Science, vol. 72, no. 4, pp. 636–642, 1993. View at Google Scholar · View at Scopus
  31. SAS Institute Inc. 2002-2003, Version 9.1, Carey, NC, USA.
  32. J. Zar, Biostatistical Analysis, Prentice-Hall, 2nd edition, 1984.
  33. N. A. Logan and R. C. W. Berkeley, “Identification of Bacillus strains using the API system,” Journal of General Microbiology, vol. 130, no. 7, pp. 1871–1882, 1984. View at Google Scholar · View at Scopus
  34. R. D. Wagner, D. D. Paine, and C. E. Cerniglia, “Phenotypic and genotypic characterization of competitive exclusion products for use in poultry,” Journal of Applied Microbiology, vol. 94, no. 6, pp. 1098–1107, 2003. View at Publisher · View at Google Scholar · View at Scopus
  35. R. Havenaar, B. T. Brink, and J. H. J. Huis Veld, “Selection of strains for probiotic use,” in Probiotics, the Scientific Basis, R. Fuller, Ed., vol. 1, pp. 209–224, Chapman and Hall, London, UK, 1992. View at Google Scholar
  36. S. M. Kristoffersen, S. Ravnum, N. J. Tourasse, O. A. Økstad, A. B. Kolstø, and W. Davies, “Low concentrations of bile salts induce stress responses and reduce motility in Bacillus cereus ATCC 14570,” Journal of Bacteriology, vol. 189, no. 14, pp. 5302–5313, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. D. Bakari, N. L. Tatsadjieu, A. Mbawala, and C. M. Mbofung, “Assessment of physiological properties of some lactic acid bacteria isolated from the intestine of chickens use as probiotics and antimicrobial agents against enteropathogenic bacteria,” Innovative Romanian Food Biotechnology, vol. 8, pp. 33–40, 2011. View at Google Scholar
  38. M. Begley, C. G. M. Gahan, and C. Hill, “The interaction between bacteria and bile,” FEMS Microbiology Reviews, vol. 29, no. 4, pp. 625–651, 2005. View at Publisher · View at Google Scholar · View at Scopus
  39. S. B. Hernández, I. Cota, A. Ducret, L. Aussel, and J. Casadesús, “Adaptation and preadaptation of Salmonella enterica to bile,” PLoS Genetics, vol. 8, no. 1, pp. 1–15, 2012. View at Google Scholar
  40. M. Du Toit, C. M. A. P. Franz, L. M. T. Dicks et al., “Characterisation and selection of probiotic lactobacilli for a preliminary minipig feeding trial and their effect on serum cholesterol levels, faeces pH and faeces moisture content,” International Journal of Food Microbiology, vol. 40, no. 1-2, pp. 93–104, 1998. View at Publisher · View at Google Scholar · View at Scopus
  41. H. Tanaka, K. Doesburg, T. Iwasaki, and I. Mierau, “Screening of lactic acid bacteria for bile salt hydrolase activity,” Journal of Dairy Science, vol. 82, no. 12, pp. 2530–2535, 1999. View at Google Scholar · View at Scopus
  42. C. Dunne, L. O'Mahony, L. Murphy et al., “In vitro selection criteria for probiotic bacteria of human origin: correlation with in vivo findings,” American Journal of Clinical Nutrition, vol. 73, no. 2, pp. 386S–392S, 2001. View at Google Scholar · View at Scopus
  43. A. C. Ouwehand, S. Salminen, and E. Isolauri, “Probiotics: an overview of beneficial effects,” Antonie van Leeuwenhoek, vol. 82, no. 1–4, pp. 279–289, 2002. View at Publisher · View at Google Scholar · View at Scopus
  44. C. Ibourahema, R. D. Dauphin, D. Jacqueline, and P. Thonart, “Characterization of lactic acid bacteria isolated from poultry farms in Senegal,” African Journal of Biotechnology, vol. 7, no. 12, pp. 2006–2012, 2008. View at Google Scholar · View at Scopus
  45. P. M. Bennett, “Plasmid encoded antibiotic resistance: acquisition and transfer of antibiotic resistance genes in bacteria,” British Journal of Pharmacology, vol. 153, no. 1, pp. S347–S357, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. J. B. Dodgson and M. N. Romanov, “Use of chicken models for the analysis of human disease,” Current Protocols in Human Genetics, vol. 15, unit 15.5, pp. 15.5.1–15.5.12, 2004. View at Publisher · View at Google Scholar · View at Scopus
  47. R. M. La Ragione and M. J. Woodward, “Competitive exclusion by Bacillus subtilis spores of Salmonella enterica serotype Enteritidis and Clostridium perfringens in young chickens,” Veterinary Microbiology, vol. 94, no. 3, pp. 245–256, 2003. View at Publisher · View at Google Scholar · View at Scopus
  48. B. Vilà, A. Fontgibell, I. Badiola et al., “Reduction of Salmonella enterica var. Enteritidis colonization and invasion by Bacillus cereus var. toyoi inclusion in poultry feeds,” Poultry Science, vol. 88, no. 5, pp. 975–979, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. J. A. Patterson and K. M. Burkholder, “Application of prebiotics and probiotics in poultry production,” Poultry Science, vol. 82, no. 4, pp. 627–631, 2003. View at Google Scholar · View at Scopus
  50. T. D. Leser, A. Knarreborg, and J. Worm, “Germination and outgrowth of Bacillus subtilis and Bacillus licheniformis spores in the gastrointestinal tract of pigs,” Journal of Applied Microbiology, vol. 104, no. 4, pp. 1025–1033, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. S. C. Ng, A. L. Hart, M. A. Kamm, A. J. Stagg, and S. C. Knight, “Mechanisms of action of probiotics: recent advances,” Inflammatory Bowel Diseases, vol. 15, no. 2, pp. 300–310, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. P. Rupa and Y. Mine, “Recent advances in the role of probiotics in human inflammation and gut health,” Journal of Agricultural and Food Chemistry, vol. 60, pp. 8249–8256, 2012. View at Google Scholar
  53. S. C. Corr, Y. Li, C. U. Riedel, P. W. O’Toole, C. Hill, and C. G. M. Gahan, “Bacteriocin production as a mechanism for the antiinfective activity of Lactobacillus salivarius UCC118,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, pp. 7617–7621, 2007. View at Google Scholar
  54. A. Anadón, M. R. Martinez-Larranaga, and M. Aranzazu Martinez, “Probiotics for animal nutrition in the european union regulation and safety assessment,” Regulatory Toxicology and Pharmacology, vol. 45, no. 1, pp. 91–95, 2006. View at Google Scholar
  55. H. A. Hong, J. M. Huang, R. Khaneja, L. V. Hiep, M. C. Urdaci, and S. M. Cutting, “The safety of Bacillus subtilis and Bacillus indicus as food probiotics,” Journal of Applied Microbiology, vol. 105, no. 2, pp. 510–520, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. C. A. McNulty, P. Boyle, T. Nichols, P. Clappison, and P. Davey, “The public's attitudes to and compliance with antibiotics,” The Journal of Antimicrobial Chemotherapy, vol. 60, supplement 1, pp. i63–i68, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. I. G. Osipova, N. A. Makhailova, I. B. Sorokulova, E. A. Vasil'eva, and A. A. Gaiderov, “Spore probiotics,” Zhurnal Mikrobiologii Epidemiologii i Immunobiologii, vol. 3, no. 3, pp. 113–119, 2003. View at Google Scholar · View at Scopus
  58. P. Williams, “Bacillus subtilis: a shocking message from a probiotic,” Cell Host and Microbe, vol. 1, no. 4, pp. 248–249, 2007. View at Publisher · View at Google Scholar · View at Scopus
  59. W. A. M. Wolken, J. Tramper, and M. J. Van Der Werf, “What can spores do for us?” Trends in Biotechnology, vol. 21, no. 8, pp. 338–345, 2003. View at Publisher · View at Google Scholar · View at Scopus