Diversity and Succession of the Intestinal Bacterial Community of the Maturing Broiler Chicken

Applied and Environmental Microbiology

Volumn 69, Issue 11, 2003, Pages 6816-6824

  Lu, Jiangrang ^a   Idris, Umelaalim ^a   Harmon, Barry ^a   Hofacre, Charles ^a   Maurer, John J ^a,b   Lee, Margie D ^a,b  

^a UNIVERSITY OF GEORGIA   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL FLORAS;

BACTERIA; BIODIVERSITY; COMPOSITION;

MICROBIOLOGY;

RNA 16S;

ARTICLE; CECUM; CHICKEN; CLOSTRIDIUM; COMMUNITY STRUCTURE; ENTEROCOCCUS; FUSOBACTERIUM; GENE SEQUENCE; ILEUM; INTESTINE FLORA; LACTOBACILLUS; MATURATION; NONHUMAN; NUCLEOTIDE SEQUENCE; SEQUENCE ANALYSIS; STATISTICAL ANALYSIS; STREPTOCOCCUS;

ANIMAL FEED; ANIMALS; BACTERIA; CECUM; CHICKENS; DNA, BACTERIAL; DNA, RIBOSOMAL; ECOSYSTEM; ILEUM; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA;

AVES; BACTERIA (MICROORGANISMS); BACTEROIDES; CLOSTRIDIACEAE; CLOSTRIDIUM; ENTEROCOCCUS; FUSOBACTERIUM; GALLUS GALLUS; LACTOBACILLUS; NEGIBACTERIA; POSIBACTERIA; STREPTOCOCCUS; ZEA MAYS;

EID: 0242489005     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.69.11.6816-6824.2003     Document Type: Article

References (62)

1. Alroy, J., V. Goyal, N. W. Lukacs, R. L. Taylor, R. G. Strout, H. D. Ward, and M. E. A. Pereira. 1989. Glycoconjugates of the intestinal epithelium of the domestic fowl (Gallus domesticus): a lectin histochemistry study. Histochem. J. 21:187-193.
2. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
3. 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.
4. Apajalahti, J. H. A., A. Kettunen, M. R. Bedford, and W. E. Holben. 2001. Percent G+C profiling accurately reveals diet-related differences in the gastrointestinal microbial community of broiler chickens. Appl. Environ. Microbiol. 67:5656-5667.
5. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struh. 1993. Current protocols in molecular biology. John Wiley and Sons, Inc., New York, N.Y.
6. Barnes, E. M., G. C. Mead, D. A. Barnum, and E. G. Harry. 1972. The intestinal flora of the chicken in the period 2 to 6 weeks of age, with particular reference to the anaerobic bacteria. Br. Poult. Sci. 13:311-326.
7. Barnes, E. M., and C. S. Impey. 1972. Some properties of the nonsporing anaerobes from poultry caeca. J. Appl. Bacteriol. 35:241-251.
8. Barnes, E. M. 1979. The intestinal microflora of poultry and game birds during life and after storage. J. Appl. Bacteriol. 46:407-419.
9. Barnes, H. J., and W. B. Gross. 1997. Colibacillosis, p. 131-142. In B. W. Calnek, H. J. Barnes, C. W. Beard, L. R. McDougald, and Y. M. Saif (ed.), Diseases of poultry, 10th ed. Iowa State University Press, Ames, Iowa.
10. Buchan, A., M. Alber, and R. E. Hodson. 2001. Strain-specific differentiation of environmental Escherichia coli isolates via denaturing gradient gel electrophoresis (DGGE) analysis of the 16S-23S intergenic spacer region. FEMS Microbiol. Ecol. 35:313-321.
11. Chandler, D. P., J. K. Fredrickson, and F. J. Brockman. 1997. Effect of PCR template concentration on the composition and distribution of total community 16S rDNA clone libraries. Mol. Ecol. 6:475-482.
12. Depalneke, B., K. R. Hristova, H. A. Oakley, V. J. McCracken, R. Aminov, R. I. Mackie, and H. R. Gaskins. 2000. Molecular ecological analysis of the succession and diversity of sulfate-reducing bacteria in the mouse gastrointestinal tract. Appl. Environ. Microbiol. 66:2166-2174.
13. Drasar, B. S., and P. A. Barrow. 1985. Intestinal microbiology, p. 19-42. American Society for Microbiology, Washington, D.C.
14. Falk, P. G., L. V. Hooper, T. Midtvedt, and J. I. Gordon. 2000. Creating and maintaining the gastrointestinal ecosystem: what we know and need to know from gnotobiology. Microbiol. Mol. Biol. Rev. 62:1157-1170.
15. Farrelly, V., F. A. Rainey, and E. Stackebrandt. 1995. Effect of genome size and rrn gene copy number on PCR amplification of 16S rRNA genes from a mixture of bacterial species. Appl. Environ. Microbiol. 61:2798-2801.
16. Field, K. G., A. E. Bernhard, and T. J. Brodeur. 2003. Molecular approaches to microbiological monitoring: fecal source detection. Environ. Monit. Assess. 81:313-326.
17. Finken, M. D., and D. P. Wages. 1997. Necrotic enteritis, p. 261-267. In B. W. Calnek, H. J. Barnes, C. W. Beard, L. R. McDougald, and Y. M. Saif (ed.), Diseases of poultry, 10th ed. Iowa State University Press, Ames, Iowa.
18. George, B. A., C. L. Quarles, and D. J. Fagerberg. 1982. Virginiamycin effects on controlling necrotic enteritis infection in chickens. Poult. Sci. 61:447-450.
19. Gong, J., R. J. Forster, H. Yu, J. R. Chambers, P. M. Sabour, R. Wheateroft, and S. Chen. 2002. Diversity and phylogenetic analysis of bacteria in the mucosa of chicken ceca and comparison with bacteria in the cecal lumen. FEMS Microbiol. Lett. 208:1-7.
20. Good, I. J. 1953. The population frequencies of species and the estimation of population parameters. Biometrika 40:237-264.
21. Guan, S., R. Xu, S. Chen, J. Odumeru, and C. Gyles. 2002. Development of a procedure for discriminating among Escherichia coli isolates from animal and human sources. Appl. Environ. Microbiol. 68:2690-2698.
22. Heilig, H. G., E. G. Zoetendal, E. E. Vaughan, P. Marteau, A. D. Akkermans, and W. M. de Vos. 2002. Molecular diversity of Lactobacillus spp. and other lactic acid bacteria in the human intestine as determined by specific amplification of 16S ribosomal DNA. Appl. Environ. Microbiol. 68:114-123.
23. Hill, M. J. 1982. Gut flora associated diseases in man. J. Vet. Med. 33(Suppl.):32-36.
24. Hofacre, C. L., D. G. White, J. J. Maurer, C. Morales, C. Lobsinger, C. R. Hudson, and S. G. Thayer. 2001. Antibiotic resistant bacteria in rendered animal products. Avian Dis. 45:953-961.
25. Hooper, L. V., M. H. Wong, A. Thelin, L. Hansson, P. G. Falk, and J. I. Gordon. 2001. Molecular analysis of commensal host-microbial relationships in the intestine. Science 291:881-884.
26. Kimura, N., F. Mimura, S. Nishida, and A. Kobayashi. 1976. Studies on the relationship between intestinal flora and cecal coccidiosis in chicken. Poult. Sci. 55:1375-1383.
27. Knarreborg, A., M. A. Simon, R. M. Engberg, B. B. Jensen, and G. W. Tannock. 2002. Effects of dietary fat source and subtherapeutic levels of antibiotic on the bacterial community in the ileum of broiler chickens at various ages. Appl. Environ. Microbiol. 68:5918-5924.
28. Koopman, J. P., H. M. Kennis, A. M. Stadhouders, and H. De Boer. 1983. Some aspects of the gastrointestinal microflora of germfree mice associated with cultured microfloras. Lab. Anim. 17:188-195.
29. Leblond, F., H. Boureau, and P. Bourliquix. 1997. The cloning of sialidase genes from Clostridium indolis and Clostridium coleatum. Clin. Infect. Dis. 25(Suppl. 2):S156-S157.
30. Long, J. R. 1973. Necrotic enteritis in broiler chickens. I. A review of the literature and prevalence of the disease in Ontario. Can. J. Comp. Med. 37:302-308.
31. Lu, J., S. Sanchez, C. Hofacre, J. J. Maurer, B. G. Harmon, and M. D. Lee. 2003. Evaluation of broiler litter with reference to the microbial composition as assessed by using 16S rDNA and functional gene markers. Appl. Environ. Microbiol. 69:901-908.
32. McCaig, A. E., L. A. Glover, and J. I. Prosser. 1999. Molecular analysis of bacterial community structure and diversity in unimproved and improved upland grass pastures. Appl. Environ. Microbiol. 65:1721-1730.
33. Mead, G. C., and B. W. Adams. 1975. Some observations on the caecal microflora of the chick during the first two weeks of life. Br. Poult. Sci. 16:169-176.
34. Mead, G. C. 1989. Microbes of the avian cecum: types present and substrates utilized. J. Exp. Zool. 3(Suppl.):48-54.
35. Mead, G. C. 2000. Prospects for competitive exclusion treatment to control salmonellas and other foodborne pathogens in poultry. Vet. J. 159:111-123.
36. Meslin, J. C., N. Fontaine, and C. Andrieux. 1999. Variation of mucin distribution in the rat intestine, caecum and colon: effect of the bacterial flora. Comp. Biochem. Physiol. A 123:235-239.
37. Metchnikoff, E. 1903. Prolongation of life. G. Putnam's Sons, New York, N.Y.
38. Moore, P. A., A. Evenson, T. D. Luckey, E. McCoy, C. A. Elvehjem, and E. B. Hart. 1946. Use of sulfasuxidine, streptothricin, and streptomycin in nutritional studies with the chick. J. Biol. Chem. 165:437-441.
39. Netherwood, T., H. J. Gilbert, D. S. Parker, and A. G. O'Donnell. 1999. Probiotics shown to change bacterial community structure in the avian gastrointestinal tract. Appl. Environ. Microbiol. 65:5134-5138.
40. Ohkuma, M., and T. Kudo. 1996. Phylogenetic diversity of the intestinal bacterial community in the termite Reticulitermes speratus. Appl. Environ. Microbiol. 62:461-468.
41. Pearson, W. R. 1990. Rapid and sensitive sequence comparison with FASTP and FASTA. Methods Enzymol. 183:63-98.
42. Pryde, S. E., S. H. Duncan, G. L. Hold, C. S. Stewart, and H. J. Flint. 2002. The microbiology of butyrate formation in the human colon. FEMS Microbiol. Lett. 217:133-139.
43. Pryde, S. E., A. J. Richardson, C. S. Stewart, and H. J. Flint. 1999. Molecular analysis of the microbial diversity present in the colonic wall, colonic lumen, and cecal lumen of a pig. Appl. Environ. Microbiol. 65:5372-5377.
44. Rolfe, R. D. 2000. The role of probiotic cultures in the control of gastrointestinal health. J. Nutr. 130(Suppl.):396S-402S.
45. Roos, S., and H. Jonsson. 2002. A high-molecular-mass cell-surface protein from Lactobacillus reuteri 1063 adheres to mucus components. Microbiology 148:433-442.
46. Salanitro, J. P., I. G. Fairchilds, and Y. D. Zgornicki. 1974. Isolation, culture characteristics, and identification of anaerobic bacteria from the chicken cecum. Appl. Microbiol. 27:678-687.
47. Shane, S. M. 1997. Campylobacteriosis, p. 235-246. In B. W. Calnek, H. J. Barnes, C. W. Beard, L. R. McDougald, and Y. M. Saif (ed.), Diseases of poultry, 10th ed. Iowa State University Press, Ames, Iowa.
48. Shimizu, T., K. Ohtani, H. Hirakawa, K. Ohshima, A. Yamashita, T. Shiba, N. Ogasawara, M. Hattori, S. Kuhara, and H. Hayashi. 2002. Complete genome sequence of Clostridium perfringens, an anaerobic flesh-eater. Proc. Natl. Acad. Sci. USA 99:99-1001.
49. Singleton, D. R., M. A. Furlong, S. L. Rathbun, and W. B. Whitman. 2001. Quantitative comparisons of 16S rRNA gene sequence libraries from environmental samples. Appl. Environ. Microbiol. 67:4374-4376.
50. Skeeles, J. K. 1997. Staphylococcosis, p. 247-254. In B. W. Calnek, H. J. Barnes, C. W. Beard, L. R. McDougald, and Y. M. Saif (ed.), Diseases of poultry, 10th ed. Iowa State University Press, Ames, Iowa.
51. Snel, J., P. P. Heinen, H. J. Blok, R. J. Carman, A. J. Duncan, P. C. Allen, and M. D. Collins. 1995. Comparison of 16S rRNA sequences of segmented filamentous bacteria isolated from mice, rats, and chickens and proposal of "Candidatus arthromitus." Int. J. Syst. Bacteriol. 45:780-782.
52. Stokstad, E. L. R., J. H. Jukes, J. Pierce, A. C. Page, and A. L. Franklin. 1949. The multiple nature of the animal protein factor. J. Biol. Chem. 180:647-654.
53. Suau, A., R. Bonnet, M. Sutren, J. Godon, G. R. Gibson, M. D. Collins, and J. Dore. 1999. Direct analysis of gene encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Appl. Environ. Microbiol. 65:4799-4807.
54. Suzuki, M. T., and S. J. Giovannoni. 1996. Bias caused by template annealing in the amplification mixtures of 16S rRNA genes by PCR. Appl. Environ. Microbiol. 62:625-630.
55. Torrallardona, D., C. I. Harris, and M. F. Fuller. 2003. Pigs' gastrointestinal microflora provide them with essential amino acids. J. Nutr. 133:1127-1131.
56. Umesaki, Y., H. Setoyama, S. Matsumoto, A. Imaoka, and K. Itoh. 1999. Differential roles of segmented filamentous bacteria and clostridia in development of the intestinal immune system. Infect. Immun. 67:3504-3511.
57. van der Wielen, P. W., D. A. Keuzenkamp, L. J. Lipman, F. van Knapen, and S. Biesterveld. 2002. Spatial and temporal variation of the intestinal bacterial community in commercially raised broiler chickens during growth. Microb. Ecol. 44:286-293.
58. Wang, R. F., W. W. Cao, and C. E. Cerniglia. 1996. PCR detection and quantitation of predominant anaerobic bacteria in human and animal fecal samples. Appl. Environ. Microbiol. 62:1242-1247.
59. Wheeler, A. L., P. G. Hartel, D. G. Godfrey, J. L. Hill, and W. I. Segars. 2002. Potential of Enterococcus faecalis as a human fecal indicator for microbial source tracking. J. Environ. Qual. 31:1286-1293.
60. Wilson, K. H., and R. B. Blitchington. 1996. Human colonic biota studied by ribosomal DNA sequence analysis. Appl. Environ. Microbiol. 62:2273-2278.
61. Ye, H. Q., D. H. Mallonee, J. E. Wells, I. Bjorkhem, and P. B. Hylemon. 1999. The bile acid-inducible baiF gene from Eubacterium sp. strain VPI 12708 encodes a bile acid-coenzyme A hydrolase. J. Lipid Res. 40:17-23.
62. Zhu, X. Y., T. Zhong, Y. Pandya, and R. D. Joerger. 2002. 16S rRNA-based analysis of microbiota from the cecum of broiler chickens. Appl. Environ. Microbiol. 68:124-137.