Influence of antimicrobial feed additives on broiler commensal posthatch gut microbiota development and performance

Applied and Environmental Microbiology

Volumn 77, Issue 10, 2011, Pages 3380-3390

  Torok, Valeria A ^a,b   Allison, Gwen E ^c   Percy, Nigel J ^a   Ophel Keller, Kathy ^a   Hughes, Robert J ^b,d  

^a Plant Research Centre   (Australia)

^b UNIVERSITY OF NEW ENGLAND   (Australia)

^c AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^d SOUTH AUSTRALIAN RESEARCH AND DEVELOPMENT INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AGE-RELATED; ANTI-MICROBIAL AGENT; BACTERIAL COMMUNITY; BACTERIAL SPECIES; DIETARY TREATMENTS; DOMAIN LEVELS; ENTEROBACTERIACEAE; FEED ADDITIVES; LACTOBACILLUS REUTERI; MICROBIAL COLONIZATION; MICROBIAL COMMUNITIES; MICROBIOTAS; OPERATIONAL TAXONOMIC UNITS; POULTRY PRODUCTION; TERMINAL RESTRICTION FRAGMENT LENGTH POLYMORPHISMS;

BACTERIOLOGY; NUTRITION;

BACTERIA;

ANTIINFECTIVE AGENT; AVILAMYCIN; BACITRACIN; BACTERIAL DNA; BAMBERMYCIN; DNA; OLIGOSACCHARIDE; RIBOSOME DNA; RNA 16S;

ALCOHOL; ANTIMICROBIAL ACTIVITY; BACTERIUM; COLONIZATION; DIET; FRAGMENTATION; FUNCTIONAL MORPHOLOGY; IDENTIFICATION KEY; IDENTIFICATION METHOD; MICROBIAL COMMUNITY; PERFORMANCE ASSESSMENT; POLYMORPHISM; POULTRY; TAXONOMY;

ANIMAL; ARTICLE; BACTERIUM; BIODIVERSITY; CHEMISTRY; CHICKEN; CLASSIFICATION; CLUSTER ANALYSIS; DENATURING GRADIENT GEL ELECTROPHORESIS; DIET; DNA FINGERPRINTING; DNA SEQUENCE; DRUG EFFECT; GASTROINTESTINAL TRACT; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; RESTRICTION FRAGMENT LENGTH POLYMORPHISM;

ANIMALS; ANTI-INFECTIVE AGENTS; BACITRACIN; BACTERIA; BAMBERMYCINS; BIODIVERSITY; CHICKENS; CLUSTER ANALYSIS; DENATURING GRADIENT GEL ELECTROPHORESIS; DIET; DNA; DNA FINGERPRINTING; DNA, BACTERIAL; DNA, RIBOSOMAL; GASTROINTESTINAL TRACT; MOLECULAR SEQUENCE DATA; OLIGOSACCHARIDES; PHYLOGENY; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA;

AVES; BACTERIA (MICROORGANISMS); CLOSTRIDIALES; ENTEROBACTERIACEAE; LACHNOSPIRACEAE; LACTOBACILLUS CRISPATUS; LACTOBACILLUS JOHNSONII; LACTOBACILLUS REUTERI; OTUS; OXALOBACTERACEAE; SUBDOLIGRANULUM; UNCLASSIFIED CLOSTRIDIALES; UNIDENTIFIED BACTERIUM;

EID: 79958187253     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02300-10     Document Type: Article

References (65)

1. 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.
2. Angelakis, E., and D. Raoult. 2010. The increase of Lactobacillus species in the gut flora of newborn broiler chicks and ducks is associated with weight gain. PLoS One 5:1-5.
3. Apajalahti, J., A. Kettunen, and H. Graham. 2004. Characteristics of the gastrointestinal microbial communities, with special reference to the chicken. Worlds Poult. Sci. J. 60:223-232.
4. Bjerrum, L., et al. 2006. Microbial community composition of the ileum and cecum of broiler chickens as revealed by molecular and cellular-based techniques. Poult. Sci. 85:1151-1164.
5. Bolder, N., J. Wagenaar, F. Putirulan, K. Veldman, and M. Sommer. 1999. The effect of flavophospholipol (Flavomycin) and salinomycin sodium (Sacox) on the excretion of Clostridium perfringens, Salmonella enteritidis and Campylobacter jejuni in broilers after experimental infection. Poult. Sci. 78: 1681-1689.
6. Bonfield, J. K., and R. Staden. 1996. Experiment files and their application during large-scale sequencing projects. DNA Seq. 6:109-117.
7. Bray, J. R., and K. R. Curtis. 1957. An ordination of the upland forest communities of southern Wisconsin. Ecol. Monogr. 27:325-349.
8. Butaye, P., L. A. Devriese, and F. Haesebrouck. 2003. Antimicrobial growth promoters used in animal feed: effects of less well known antibiotics on gram-positive bacteria. Clin. Microbiol. Rev. 16:175-188.
9. Clarke, K. R. 1993. Non-parametric multivariate analyses of changes in community structure. Aust. J. Ecol. 18:117-143.
10. Cole, J. R., et al. 2009. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37:D141-D145.
11. Diarra, M., et al. 2007. Impact of feed supplementation with antimicrobial agents on growth performance of broiler chickens, Clostridium perfringens and Enterococcus counts, and antibiotic resistance phenotypes and distribution of antimicrobial resistance determinants in Escherichia coli isolates. Appl. Environ. Microbiol. 73:6566-6576.
12. Dumonceaux, T. J., J. E. Hill, S. M. Hemmingsen, and A. G. Van Kessel. 2006. Characterization of intestinal microbiota and response to dietary virginiamycin supplementation in the broiler chicken. Appl. Environ. Microbiol. 72:2815-2823.
13. Egert, M., A. A. De Graaf, H. Smidt, W. M. De Vos, and K. Venema. 2006. Beyond diversity: functional microbiomics of the human colon. Trends Microbiol. 14:86-91.
14. Engberg, R. M., M. S. Hedemann, T. D. Leser, and B. B. Jensen. 2000. Effect of zinc bacitracin and salinomycin on intestinal microflora and performance of broilers. Poult. Sci. 79:1311-1319.
15. Feighner, S. D., and M. P. Dashkevicz. 1987. Subtherapeutic levels of antibiotics in poultry feed and their effects on weight gain, feed efficiency, and bacterial cholyltaurine hydrolase activity. Appl. Environ. Microbiol. 53:331-336.
16. Fernández-Rubio, C., et al. 2009. Butyric acid-based feed additives help protect broiler chickens from Salmonella Enteritidis infection. Poult. Sci. 88:943-948.
17. Frei, A., D. Goldenberger, and M. Teuber. 2001. Antimicrobial susceptibility of intestinal bacteria from Swiss poultry flocks before the ban of antimicrobial growth promoters. Syst. Appl. Microbiol. 24:116-121.
18. Garcia, V., P. Catala-Gregori, F. Hernandez, M. D. Megias, and J. Madrid. 2007. Effect of formic acid and plant extracts on growth, nutrient digestibility, intestine mucosa morphology and meat yield of broilers. J. Appl. Poult. Res. 16:555-562.
19. Geier, M. S., et al. 2010. Comparison of alternatives to in-feed antimicrobials for the prevention of clinical necrotic enteritis. J. Appl. Microbiol. 109:1329-1338.
20. Geier, M. S., V. A. Torok, G. E. Allison, K. Ophel-Keller, and R. J. Hughes. 2009. Indigestible carbohydrates alter the intestinal microbiota but do not influence the performance of broiler chickens. J. Appl. Microbiol. 106:1540-1548.
21. Gong, J., et al. 2008. Effects of zinc bacitracin, bird age and access to range on bacterial microbiota in the ileum and caeca of broiler chickens. J. Appl. Microbiol. 104:1372-1382.
22. Gong, J., et al. 2007. 16S rRNA gene-based analysis of mucosa-associated bacterial community and phylogeny in the chicken gastrointestinal tracts; from crops to ceca. FEMS Microbiol. Ecol. 59:147-157.
23. Guan, L. L., et al. 2003. Detection and identification of Lactobacillus species in crops of broilers of different ages by using PCR-denaturing gradient gel electrophoresis and amplified ribosomal DNA restriction analysis. Appl. Environ. Microbiol. 69:6750-6757.
24. Guban, J., D. Korver, G. Allison, and G. Tannock. 2006. Relationship of dietary antimicrobial drug administration with broiler performance, decreased population levels of Lactobacillus salivarius, and reduced bile salt deconjugation in the ileum of broiler chickens. Poult. Sci. 85:2186-2194.
25. Gunal, M., G. Yayli, O. Kaya, N. Karahan, and O. Sulak. 2006. The effects of antibiotic growth promoter, probiotic or organic acid supplementation on performance, intestinal microflora and tissue of broilers. Int. J. Poult. Sci. 5:149-155.
26. Harrow, S., V. Ravindran, R. Butler, J. Marshall, and G. Tannock. 2007. Real-time quantitative PCR measurement of ileal Lactobacillus salivarius populations from broiler chickens to determine the influence of farming practices. Appl. Environ. Microbiol. 73:7123-7127.
27. Hilmi, H. T. A., A. Surakka, J. Apajalahti, and P. E. Saris. 2007. Identification of the most abundant Lactobacillus species in the crop of 1- and 5-week-old broiler chickens. Appl. Environ. Microbiol. 73:7867-7873.
28. Hume, M. E., et al. 2003. Poultry digestive microflora biodiversity as indicated by denaturing gradient gel electrophoresis. Poult. Sci. 82:1100-1107.
29. Kaplan, C. W., and C. L. Kitts. 2003. Variation between observed and true terminal restriction fragment length is dependent on true TRF length and purine content. J. Microbiol. Methods. 54:121-125.
30. Kent, A. D., D. J. Smith, B. J. Benson, and E. W. Triplett. 2003. Web-based phylogenetic assignment tool for analysis of terminal restriction fragment length polymorphism profiles of microbial communities. Appl. Environ. Microbiol. 69:6768-6776.
31. Klasing, K. C. 2007. Nutrition and the immune system. Br. Poult. Sci. 48:525-537.
32. 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.
33. Lane, D. J. 1991. 16S/23S rRNA sequencing, p. 115-175. In E. Stackebrandt and M. Goodfellow (ed.), Nucleic acid techniques in bacterial systematics. John Wiley & Sons, Inc., Hoboken, NJ.
34. Lu, J., J. S. Domingo, and O. C. Shanks. 2007. Identification of chickenspecific fecal microbial sequences using a metagenomic approach. Water Res. 41:3561-3574.
35. Lu, J., et al. 2003. Diversity and succession of the intestinal bacterial communities of the maturing broiler chicken. Appl. Environ. Microbiol. 69:6816-6824.
36. Lund, M., L. Bjerrum, and K. Pedersen. 2010. Quantification of Faecalibacterium prausnitzii- and Subdoligranulum variabile-like bacteria in the cecum of chickens by real-time PCR. Poult. Sci. 89:1217-1224.
37. 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.
38. Mountzouris, K. C., et al. 2010. Effects of probiotic inclusion levels in broiler nutrition on growth performance, nutrient digestibility, plasma immunoglobulins, and cecal microflora composition. Poult. Sci. 89:58-67.
39. Mountzouris, K. C., et al. 2007. Evaluation of the efficacy of a probiotic containing Lactobacillus, Bifidobacterium, Enterococcus, and Pediococcus strains in promoting broiler performance and modulating cecal microflora compositions and metabolic activities. Poult. Sci. 86:309-317.
40. 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.
41. Niewold, T. 2007. The nonantibiotic anti-inflammatory effect of antimicrobial growth promoters, the real mode of action? A hypothesis. Poult. Sci. 86: 605-609.
42. Noy, Y., and D. Sklan. 1997. Posthatch development in poultry. J. Appl. Poult. Res. 6:344-354.
43. Owens, B., L. C. M. A. Tucker, and K. J. McCracken. 2008. Effects of different feed additives alone or in combination on broiler performance, gut microflora and ileal histology. Br. Poult. Sci. 49:202-212.
44. Pedroso, A. A., et al. 2006. Intestinal bacterial community and growth performance of chickens fed diets containing antibiotics. Poult. Sci. 85:747-752.
45. Pedroso, A. A., F. F. M. Menten, and M. R. Lambais. 2005. The structure of bacterial community in the intestine of newly hatched chicks. J. Appl. Poult. Res. 14:232-237.
46. Pfaller, M. 2006. Flavophospholipol use in animals: positive implications for antimicrobial resistance based on its microbiologic properties. Diagn. Microbiol. Infect. Dis. 56:115-121.
47. Promega. 2007. Technical manual TM042. Promega, Madison, WI.
48. Rada, V., J. Janesova, M. Marounek, and K. Vorisek. 1991. Susceptibility of chicken intestinal lactobacilli to antimicrobial compounds. Acta Vet. Brno 60:339-343.
49. Rehman, H. U., W. Vanhjen, W. A. Awad, and J. Zentek. 2007. Indigenous bacteria and bacterial metabolic products in the gastrointestinal tract of broiler chickens. Arch. Anim. Nutr. 61:319-335.
50. Sarmah, A. K., M. T. Meyer, and A. B. A. Boxall. 2006. A global perspective on the use, sale, exposure pathways, occurrence, fate and effects of veterinary antibiotics (VAs) in the environment. Chemosphere. 65:725-759.
51. Shira, E. B., D. Sklan, and A. Friedman. 2005. Impaired immune responses in broiler hatchling hindgut following delayed access to feed. Vet. Immunol. Immunopathol. 105:33-45.
52. Snedecor, G. W., and W. G. Cochran. 1980. Statistical methods, 7th ed. Iowa State University Press, Ames, IA.
53. Stirling, G. R., et al. 2004. Combining an initial risk assessment process with DNA assays to improve prediction of soilborne diseases caused by root-knot nematode (Meloidogyne spp.) and Fusarium oxysporum f. sp. lycopersici in the Queensland tomato industry. Aust. Plant Pathol. 33:285-293.
54. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-1599.
55. Tamura, K., M. Nei, and S. Kumar. 2004. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc. Natl. Acad. Sci. U. S. A. 101:11030-11035.
56. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
57. Torok, V. A., K. Ophel-Keller, M. Loo, and R. J. Hughes. 2008. Application of methods for identifying broiler chicken gut bacterial species linked with increased energy metabolism. Appl. Environ. Microbiol. 74:783-791.
58. Torok, V. A., et al. 2007. Environment and age: impact on poultry gut microflora. Aust. Poult. Sci. Symp. 19:149-152.
59. van der Wielen, P. W. J. J., D. A. Keuzenkamp, L. J. A. 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.
60. Walter, J., et al. 2001. Detection of Lactobacillus, Pediococcus, Leuconostoc, and Weissella species in human feces by using group-specific PCR primers and denaturing gradient gel electrophoresis. Appl. Environ. Microbiol. 67: 2578-2585.
61. Widmer, F., M. Hartmann, B. Frey, and R. Kolliker. 2006. A novel strategy to extract specific phylogenetic sequence information from community TRFLP. J. Microbiol. Methods. 66:512-520.
62. Wise, M., and G. Siragusa. 2007. Quantitative analysis of the intestinal bacterial community in one- to three-week-old commercially reared broiler chickens fed conventional or antibiotic-free vegetable-based diets. J. Appl. Microbiol. 102:1138-1149.
63. Yin, Y., et al. 2010. Exposure of different bacterial inocula to newborn chicken affects gut microbiota development and ileum gene expression. ISME J. 4:367-376.
64. Zhou, H., et al. 2007. Appropriate chicken sample size for identifying the composition of broiler intestinal microbiota affected by dietary antibiotics, using the polymerase chain reaction-denaturing gradient gel electrophoresis technique. Poult. Sci. 86:2541-2549.
65. Zhu, X. Y., and R. D. Joerger. 2003. Composition of microbiota in content and mucus from ceca of broiler chickens as measured by fluorescent in situ hybridization with group-specific, 16S rRNA-targeted oligonucleotide probes. Poult. Sci. 82:1242-1249.