Change in the ileal bacterial population of Turkeys fed different diets and after infection with Salmonella as determined with denaturing gradient gel electrophoresis of amplified 16S ribosomal DNA

Poultry Science

Volumn 87, Issue 7, 2008, Pages 1415-1427

  Santos Jr , A A ^a   Ferket, P R ^b   Santos, F B O ^b   Nakamura, N ^c   Collier, C ^c  

^a Florida   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Enzyme; Microbial ecology; Nonstarch polysaccharide; Polymerase chain reaction denaturing gradient gel electrophoresis; Turkey

Indexed keywords

AVES; BACTERIA (MICROORGANISMS); MELEAGRIS GALLOPAVO; SALMONELLA; TRITICUM AESTIVUM; ZEA MAYS;

EID: 46249089035     PISSN: 00325791     EISSN: 15253171     Source Type: Journal    
DOI: 10.3382/ps.2006-00462     Document Type: Article

References (77)

1. Akiba, T., and K. Horikoshi. 1988. Xylanases of alkalophilic thermophilic Bacillus. Methods Enzymol. 160:655-659.
2. Amann, R. I., W. Ludwig, and K. H. Schleifer. 1995. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol. Rev. 59:143-169.
3. Andrew, V. K., T. W. Shirkey, R. H. Siggers, M. D. Drew, and B. Laarveld. 2004. Commensal bacteria and intestinal development: Studies using gnotobiotic pigs. Pages 47-59 in Interfacing Immunity, Gut Health and Performance. L. A. Tucker and J. A. Taylor-Pickard, ed. Nottingham University Press, Nottingham, UK.
4. Annison, G. 1993. Corrigendum - The role of wheat non-starch polysaccharides in broiler nutrition. Aust. J. Agric. Res. 44:405-422.
5. Apajalahti, J. H. A., L. K. Sarkilahti, B. R. E. Maki, J. P. Heikkinen, P. H. Nurminen, and W. E. Holben. 1998. Effective recovery of bacterial DNA and percent-guanine-plus-cytosine-based analysis of community structure in the gastrointestinal tract of broiler chickens. Appl. Environ. Microbiol. 64:4084-4088.
6. Bach Knudsen, E. E. 2001. The nutritional significance of "dietary fibre" analysis. Anim. Feed Sci. Technol. 90:3-20.
7. Bach Knudsen, K. E. 1997. Carbohydrate and lignin contents of plant materials used in animal feeding. Anim. Feed Sci. Technol. 67:319-338.
8. Bach Knudsen, K. E., B. B. Jensen, J. O. Andersen, and I. Hansen. 1991. Gastrointestinal implications in pigs of wheat and oat fractions. 2. Microbial activity in the gastrointestinal tract. Br. J. Nutr. 65:233-248.
9. Bach Knudsen, K. E., and H. Jorgensen. 2001. Intestinal degradation of dietary carbohydrates - From birth to maturity. Pages 109-120 in Digestive Physiology of Pigs. J. E. Lindberg and B. Ogle, ed. CABI Publishing, Wallingford, UK.
10. Bartelt, J., A. Jadamus, F. Wiese, E. Swiech, L. Buraczewska, and O. Simon. 2002. Apparent precaecal digestibility of nutrients and level of endogenous nitrogen in digesta of the small intestine of growing pigs as affected by various digesta viscosities. Arch. Anim. Nutr. 56:93-107.
11. Bataillon, M., A. P. N. Cardinali, N. Castillon, and F. Duchiron. 2000. Purification and characterization of a moderately thermostable xylanase from Bacillus sp. strain SPS-0. Enzyme Microb. Technol. 26:187-192.
12. Choct, M., and G. Annison. 1992. Anti-nutritive effect of wheat pentosans in broiler: Roles of viscosity and gut microflora. Br. Poult. Sci. 33:821-834.
13. Collier, C. T., M. R. Smiricky-Tjardes, D. M. Albin, J. E. Wubben, V. M. Gabert, B. Deplancke, D. Bane, D. B. Anderson, and H. R. Gaskins. 2003a. Molecular ecological analysis of porcine ileal microbiota responses to antimicrobial growth promoters. J. Anim. Sci. 81:3035-3045.
14. Collier, C. T., J. D. van der Klis, B. Deplancke, D. B. Anderson, and H. R. Gaskins. 2003b. Effects of tylosin on bacterial mucolysis, Clostridium perfringens colonization, and intestinal barrier function in a chick model of necrotic enteritis. Antimicrob. Agents Chemother. 47:3311-3317.
15. Falk, P. G., L. V. Hooper, T. Midtvedt, and J. I. Gordon. 1998. Creating and maintaining the gastrointestinal ecosystem: What we know and need to know from gnotobiology. Microbiol. Mol. Biol. Rev. 62:1157-1170.
16. Ferket, P. R. 1991. Effect of diet on gut microflora of poultry. Zootechnica 7:44-49.
17. Ferket, P. R., and A. A. Santos Jr. 2005. How nutrition influences gut health and pathogen colonization? Proc. 2nd Alltech's Annual Brazilian Feed Industry Symposium - The Premier Brazilian Meeting for Animal Nutrition, Curitiba, Parana, Brazil. Alltech Inc., Nicholasville, KY.
18. Foucher, A. L. J. L., T. Bongers, L. R. Noble, and M. J. Wilson. 2004. Assessment of nematode biodiversity using DGGE of 18S rDNA following extraction of nematodes from soil. Soil Biol. Biochem. 36:2027-2032.
19. Fraga, M. J., P. P. Ayala, R. Carabano, and J. C. Blas. 1991. Effect of type of fiber on the rate of passage and on the contribution of soft feces to nutrient intake of finishing rabbits. J. Anim. Sci. 69:1566-1574.
20. Fuller, R. 1977. The importance of lactobacilli in maintaining normal microbial balance in the crop. Br. Poult. Sci. 18:85-94.
21. Furr, R. M. 2003. Evaluating theories efficiently: The nuts and bolts of contrast analysis. Understanding Stat. 2:33-67.
22. Gestel, G., P. Besancon, and J. M. Rouanet. 1994. Comparative evaluation of the effects of two different forms of dietary fibre (rice bran vs. wheat bran) on rat colonic mucosa and faecal microflora. Ann. Nutr. Metab. 38:249-256.
23. Hancock, R. E. W., and A. Rozek. 2002. Role of membranes in the activities of antimicrobial cationic peptides. FEMS Microbiol. Lett. 206:143-149.
24. Hentschel, U., M. Steinert, and J. Hacker. 2000. Common molecular mechanisms of symbiosis and pathogenesis. Trends Microbiol. 8:226-231.
25. Hogberg, A. 2003. Cereal non-starch polysaccharides in pig diets: Influence on digestion site, gut environment and microbial populations. PhD Thesis. Swedish Univ. Agric. Sci., Uppsala.
26. Hogberg, A., and J. E. Lindberg. 2004. Influence of cereal nonstarch polysaccharides and enzyme supplementation on digestion site and gut environment in weaned piglets. Anim. Feed Sci. Technol. 116:113-128.
27. Hoj, L., R. A. Olsen, and V. L. Torsvik. 2005. Archaeal communities in high arctic wetlands at Spitsbergen, Norway (79°N) as characterized by 16S rRNA gene fingerprinting. FEMS Microbiol. Ecol. 53:89-101.
28. Hume, M. E., L. F. Kubena, T. S. Edrington, C. J. Donskey, R. W. Moore, S. C. Ricke, and D. J. Nisbet. 2003. Poultry digestive microflora biodiversity as indicated by denaturing gradient gel electrophoresis. Poult. Sci. 82:1100-1107.
29. Ishii, K., and S. Takii. 2003. Comparison of microbial communities in four different composting processes as evaluated by denaturing gradient gel electrophoresis analysis. J. Appl. Microbiol. 95:109-119.
30. + intraepithelial lymphocyte distribution by dietary fiber in the rat large intestine. Exp. Biol. Med. 227:1017-1021.
31. Ishizuka, S., S. Tanaka, H. Xu, and H. Hara. 2004. Fermentable dietary fiber potentiates the localization of immune cells in the rat large intestinal crypts. Exp. Biol. Med. 229:876-884.
32. Joerger, R. D. 2003. Alternatives to antibiotics: Bacteriocins, antimicrobial peptides and bacteriophages. Poult. Sci. 82:640-647.
33. Kass, M. L., P. J. Van Soest, and W. G. Pond. 1980. Utilization of dietary fiber alfalfa by growing swine. II. Volatile fatty acid concentrations in and disappearance from the gastrointestinal tract. J. Anim. Sci. 50:192-197.
34. Kirk, J. L., L. A. Beaudette, M. Hart, P. Moutoglis, J. N. Klironomos, H. Lee, and T. Trevors. 2004. Methods of studying soil microbial diversity. J. Microbiol. Methods 58:169-188.
35. Konstantinov, S. R., W. Y. Zhu, B. A. Williams, S. Tamminga, W. M. Vos, and A. D. L. Akkermans. 2003. Effect of fermentable carbohydrates on piglet faecal bacterial communities as revealed by denaturing gradient gel electrophoresis analysis of 16S ribosomal DNA. FEMS Microbiol. Ecol. 43:225-235.
36. Lan, Y. 2004. Gastrointestinal health benefits of soy water-soluble carbohydrates in young broiler chickens. PhD Thesis. Wageningen University, Wageningen, the Netherlands.
37. Lane, D. J., B. Pace, G. J. Olsen, D. A. Stahl, M. L. Sogin, and N. R. Pace. 1985. Rapid determination of 16S ribosomal RNA sequences for phylogenetic analysis. Proc. Natl. Acad. Sci. USA 82:6955-6959.
38. Langhout, D. J., J. B. Schutte, J. de Jong, H. Sloetjes, M. W. A. Verstegen, and S. Tamminga. 2000. Effect of viscosity on digestion of nutrients in conventional and germ-free chicks. Br. J. Nutr. 83:533-540.
39. Le Blay, G., H. M. Bottiere, and C. Cherubt. 1999. Prolonged intake of fructo-oligosaccharides induces a short-term elevation in lactic acid-producing bacteria and a persistent increase in cecal butyrate in rats. J. Nutr. 129:2231-2235.
40. Leser, T. D., R. H. Lindecrona, T. K. Jensen, B. B. Jensen, and K. Möller. 2000. Changes in bacterial community structure in the colon of pigs fed different experimental diets and after infection with Brachyspira hyodysenteriae. Appl. Environ. Microbiol. 66:3290-3296.
41. Liu, W. T., and D. A. Stahl. 2002. Molecular approaches for the measurement of density, diversity, and phylogeny. Pages 114-134 in Manual of Environmental Microbiology. 2nd rev. ed. C. J. Hurst, R. L. Crawford, G. R. Knudsen, M. J. McInerney, and L. D. Stetzenbach, ed. ASM Press, Washington, DC.
42. Magurran, A. 1988. Ecological Diversity and Its Measurement. Princeton University Press, Princeton, NJ.
43. McCracken, V. J., J. M. Simpson, R. I. Mackie, and H. R. Gaskins. 2001. Molecular ecological analysis of dietary and antibiotic-induced alterations of the mouse intestinal microbiota. J. Nutr. 131:1862-1870.
44. Minamida, K., I. N. Sujaya, A. Tamura, N. Shigematsu, T. Sone, A. Yokota, K. Asano, Y. Benno, and F. Tomita. 2004. The effects of di-D- fructofuranose-1,2′:2,3′-dianhydride (DFA III) administration on human intestinal microbiota. J. Biosci. Bioeng. 98:244-250.
45. Montagne, L., J. R. Pluske, and D. J. Hampson. 2003. A review of interactions between dietary fibre and the intestinal mucosa, and their consequences on digestive health in young non-ruminant animals. Anim. Feed Sci. Technol. 108:95-117.
46. Muyzer, G. 1999. DGGE/TGGE a method for identifying genes from natural ecosystems. Curr. Opin. Microbiol. 2:317-322.
47. Muyzer, G., T. Brinkhoff, U. Nbel, C. Santegoeds, H. Schäfer, and H. Wawer. 1998. Denaturant gradient gel electrophoresis in microbial ecology. Pages 1-27 in Molecular Microbial Ecology Manual. Vol. 3.4.4. A. Akkermans, J. D. van Elsas, and F. de Bruijn, ed. Kluwer Academic Publishers, Boston, MA.
48. Muyzer, G., E. C. de Wall, and A. G. Uitterlinden. 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 59:695-700.
49. Muyzer, G., and K. Smalla. 1998. Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie Leeuwenhoek 73:127-141.
50. NRC. 1994. Nutrient Requirements of Poultry. 9th rev. ed. Natl. Acad. Press, Washington, DC.
51. Nousiainen, J., and J. Setala. 1998. Lactic acid bacteria as animal probiotics. Pages 437-473 in Lactic Acid Bacteria: Microbiology and Functional Aspects. S. Salminen and A. Wright ed. Marcel Dekker, New York, NY.
52. Palys, T., L. K. Nakamura, and F. M. Cohan. 1997. Discovery and classification of ecological diversity in the bacterial world: The role of DNA sequence data. Int. J. Syst. Bacteriol. 47:1145-1156.
53. Raskin, L., W. Capman, R. Sharp, L. Poulsen, and D. Stahl. 1997. Molecular ecology of gastrointestinal ecosystems. Pages 243-298 in Gastrointestinal Microbiology. Vol 2. R. I. Mackie, B. A. White, and R. E. Isaacson, ed. Chapman and Hall, New York, NY.
54. Rastall, R. A., G. R. Gibson, H. S. Gill, F. Guarner, T. R. Klaenhammer, B. Pot, G. Reid, I. R. Rowland, and M. E. Sanders. 2005. Modulation of the microbial ecology of the human colon by probiotics, prebiotics and synbiotics to enhance human health: An overview of enabling science and potential applications. FEMS Microbiol. Ecol. 52:145-152.
55. Rastall, R. A., and V. Maitin. 2002. Prebiotics and synbiotics: Towards the next generation. Curr. Opin. Biotechnol. 13:490-496.
56. Remus, J. 2003. Control strategies for Salmonella in swine discussed. Feedstuffs 75:14-16.
57. Roberfroid, M. B., F. Bornet, C. Bouley, and J. H. Cummings. 1995. Colonic microflora: Nutrition and health: Summary and conclusions of an International Life Sciences Institute (ILSI) workshop held in Barcelona, Spain. Nutr. Rev. 53:127-130.
58. Santos, F. B. O., X. Li, J. B. Payne, and B. W. Sheldon. 2005. Estimation of most probable number Salmonella populations on commercial North Carolina turkey farms. J. Appl. Poult. Res. 14:700-708.
59. SAS Institute. 1996. SAS/STAT User's Guide, Version 6. 4th ed. Vol. 2. SAS Proprietary Software Release 6.12. SAS Institute Inc., Cary, NC.
60. Shannon, C. E., and W. Weaver. 1949. The Mathematical Theory of Communication. Univ. Illinois Press, Urbana.
61. Simon, O., W. Vahjen, and D. Taras. 2004. Interaction of nutrition with intestinal microbial communities. Pages 33-46 in Interfacing Immunity, Gut Health and Performance, L. A. Tucker and J. A. Taylor-Pickard, ed. Nottingham University Press, Nottingham, UK.
62. Simpson, J. M., V. J. McCracken, H. R. Gaskins, and R. I. Mackie. 2000. Denaturing gradient gel electrophoresis analysis of 16S rDNA amplicons to monitor changes in fecal bacterial populations of weaning pigs after introduction of Lactobacillus reuteri strain MM53. Appl. Environ. Microbiol. 66:4705-4711.
63. Simpson, J. M., V. J. McCracken, B. A. White, H. R. Gaskins, and R. I. Mackie. 1999. Application of denaturant gradient gel electrophoresis for the analysis of the porcine gastrointestinal microbiota. J. Microbiol. Methods 36:167-179.
64. Sneath, P. H., and R. R. Sokal. 1973. Numerical Taxonomy: The Principles and Practice of Numerical Classification. W. H. Freeman and Company, San Francisco, CA.
65. Suau, A., R. Bonnet, M. Sutren, J. J. Godon, G. R. Gibson, M. D. Collins, and J. Dore. 1999. Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Appl. Environ. Microbiol. 65:4799-4807.
66. Svihus, B. 2001. Research note: A consistent low starch digestibility observed in pelleted broiler chicken diets containing high levels of different wheat varieties. Anim. Feed Sci. Technol. 92:45-49.
67. Torsvik, V., F. L. Daae, R. A. Sandaa, and L. Ovreas. 1998. Novel techniques for analyzing microbial diversity in natural and perturbed environments. J. Biotechnol. 64:53-62.
68. Trowell, H., D. A. T. Southgate, T. M. S. Wolever, A. R. Leeds, M. A. Gussell, and D. J. A. Jenkins. 1976. Dietary fiber redefined. Lancet 1:967.
69. Tsai, Y. L., and B. H. Olsen. 1992. Rapid method for separation of bacterial DNA from humic substances in sediments for polymerase chain reaction. Appl. Environ. Microbiol. 58:2292-2295.
70. Uchino, F., and T. Nakane. 1981. A thermostable xylanase from a thermophilic acidophilic Bacillus sp. Agric. Biol. Chem. 45:1121-1127.
71. Van Laere, K. M. J., M. Bosveld, H. A. Schols, G. Beldman, and A. G. J. Voragen. 1997. Fermentative degradation of plant cell wall derived oligosaccharides by intestinal bacteria. Pages 37-46 in Proc. Int. Symp. Non-digestable Oligosaccharides: Healthy Food for the Colon. R. Hartemink, ed. Wageningen Graduate School VLAG, Wageningen, the Netherlands.
72. Vaughan, E. E., F. Schut, H. G. H. J. Helig, E. G. W. M. de Vos, and A. D. L. Akkermans. 2000. A molecular view of the intestinal ecosystem. Curr. Issues Intest. Microbiol. 1:1-12.
73. Waters, S. M., C. F. Duffy, and R. F. G. Power. 2005. PCR-DGGE analysis of caecal microflora of Natustat™ supplemented turkeys challenged with Histomonas meleagridis. Int. J. Poult. Sci. 4:620-627.
74. Wilson, K. H., and R. B. Blitchington. 1996. Human colonic biota studied by ribosomal DNA sequence analysis. Appl. Environ. Microbiol. 62:2273-2278.
75. Wise, A., A. K. Mallet, and I. R. Rowland. 1986. Effect of mixtures of dietary fibers on the enzyme activity of the rat caecal microflora. Toxicology 38:241-248.
76. Yan, S. S., and J. M. Gilbert. 2004. Antimicrobial drug delivery in food animals and microbial food safety concerns: an overview of in vitro and in vivo factors potentially affecting the animal gut microflora. Adv. Drug Deliv. Rev. 56:1497-1521.
77. Zoetendal, E. G., A. D. L. Akkermans, and W. M. De Vos. 1998. Temperature gradient gel electrophoresis analysis of 16S rRNA from human fecal samples reveals stable and host-specific communities of active bacteria. Appl. Environ. Microbiol. 64:3854-3859.