Successional changes in the chicken cecal microbiome during 42 days of growth are independent of organic acid feed additives

BMC Veterinary Research

Volumn 10, Issue 1, 2014, Pages

  Oakley, Brian B ^a,b   Buhr, R Jeff ^a   Ritz, Casey W ^c   Kiepper, Brian H ^c   Berrang, Mark E ^d   Seal, Bruce S ^a   Cox, Nelson A ^a  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

^b WESTERN UNIVERSITY OF HEALTH SCIENCES   (United States)

^c UNIVERSITY OF GEORGIA   (United States)

^d RUSSELL RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACID; FOOD ADDITIVE; FORMIC ACID; FORMIC ACID DERIVATIVE; PROPIONIC ACID; PROPIONIC ACID DERIVATIVE; RNA 16S;

ANIMAL; ANIMAL FOOD; BACTERIUM; CECUM; CHICKEN; CLASSIFICATION; DRUG EFFECTS; GENETICS; GROWTH, DEVELOPMENT AND AGING; MALE; MICROBIOLOGY; MICROFLORA; MOLECULAR GENETICS;

ANIMAL FEED; ANIMALS; BACTERIA; CECUM; CHICKENS; FATTY ACIDS; FOOD ADDITIVES; FORMATES; MALE; MICROBIOTA; MOLECULAR SEQUENCE DATA; PROPIONATES; RNA, RIBOSOMAL, 16S;

EID: 84965082838     PISSN: None     EISSN: 17466148     Source Type: Journal    
DOI: 10.1186/s12917-014-0282-8     Document Type: Article

References (70)

1. Scallan E, Griffin PM, Angulo FJ, Tauxe RV, Hoekstra RM: Foodborne illness acquired in the united states-unspecified agents. Emerg Infect Dis 2011, 17:16-22.
2. Scharff RL: Economic burden from health losses due to foodborne illness in the United States. J Food Prot 2012, 75:123-131.
3. James WO, Brewer RL, Prucha JC, Williams WO Jr, Parham DR: Effects of chlorination of chill water on the bacteriologic profile of raw chicken carcasses and giblets. J Am Vet Med Assoc 1992, 200:60-63.
4. James C, Vincent C, De Andrade Lima TI, James SJ: The primary chilling of poultry carcasses-a review. Int J Refrigeration 2006, 29:847-862.
5. Doyle MP, Erickson MC: Opportunities for mitigating pathogen contamination during on-farm food production. Int J Food Microbiol 2012, 152:54-74.
6. European-Commission: Regulation (EC) No. 1831/2003 of the European Parliament and of the Council on additives for use in animal nutrition. Official Journal of European Union 2003, L 268:29-43.
7. Weber JT, Courvalin P: An emptying quiver: antimicrobial drugs and resistance. Emerg Infect Dis 2005, 11:791-793.
8. Love DC, DavisMF, Bassett A, Gunther A, Nachman KE: Dose imprecision and resistance: Free-choice medicated feeds in industrial food animal production in the United States. Environ Health Perspect 2011, 119:279-283.
9. Seal BS, Lillehoj HS, Donovan DM, Gay CG: Alternatives to antibiotics: a symposium on the challenges and solutions for animal production. Anim Health Res Rev 2013, 14:78-87.
10. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI: An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006, 444:1027-1031.
11. McKenna P, Hoffmann C, Minkah N, Aye PP, Lackner A, Liu ZZ, Lozupone CA, Hamady M, Knight R, Bushman FD: The macaque gut microbiome in health, lentiviral infection, and chronic enterocolitis. PLoS Pathog 2008, 4:E20.
12. Bakken JS, Borody T, Brandt LJ, Brill JV, Demarco DC, Franzos MA, Kelly C, Khoruts A, Louie T, Martinelli LP, Moore TA, Russell G, Surawicz C, Fecal Microbiota T: Treating clostridium difficile infection with fecal microbiota transplantation. Clin Gastroenterol Hepatol 2011, 9:1044-1049.
13. Greenblum S, Turnbaugh PJ, Borenstein E: Metagenomic systems biology of the human gut microbiome reveals topological shifts associated with obesity and inflammatory bowel disease. Proc Natl Acad Sci U S A 2012, 109:594-599.
14. Lawley TD, Clare S, Walker AW, Stares MD, Connor TR, Raisen C, Goulding D, Rad R, Schreiber F, Brandt C, Deakin LJ, Pickard DJ, Duncan SH, Flint HJ, Clark TG, Parkhill J, Dougan G: Targeted restoration of the intestinal microbiota with a simple, defined bacteriotherapy resolves relapsing clostridium difficile disease in mice. PLoS Pathog 2012, 8:e1002995.
15. Knarreborg A, Simon MA, Engberg RM, Jensen BB, Tannock GW: 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 2002, 68:5918-5924.
16. Wise MG, Siragusa GR: 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 2007, 102:1138-1149.
17. Fairchild AS, Smith JL, Idris U, Lu J, Sanchez S, Purvis LB, Hofacre C, Lee MD: Effects of orally administered tetracycline on the intestinal community structure of chickens and on tet determinant carriage by commensal bacteria and Campylobacter jejuni. Appl Environ Microbiol 2005, 71:5865-5872.
18. Danzeisen JL, Kim HB, Isaacson RE, Tu ZJ, Johnson TJ: Modulations of the chicken cecal microbiome and metagenome in response to anticoccidial and growth promoter treatment. PLoS One 2011, 6:e27949.
19. Gong J, Yu H, Liu T, Gill JJ, Chambers JR, Wheatcroft R, Sabour PM: Effects of zinc bacitracin, bird age and access to range on bacterial microbiota in the ileum and caeca of broiler chickens. J Appl Microbiol 2008, 104:1372-1382.
20. Torok VA, Allison GE, Percy NJ, Ophel-Keller K, Hughes RJ: Influence of antimicrobial feed additives on broiler commensal posthatch gut microbiota development and performance. Appl Environ Microbiol 2011, 77:3380-3390.
21. Tillman GE, Haas GJ, Wise MG, Oakley B, Smith MA, Siragusa GR: Chicken intestine microbiota following the administration of lupulone, a hop-based antimicrobial. FEMS Microbiol Ecol 2011, 77:395-403.
22. Sun H, Tang JW, Fang CL, Yao XH, Wu YF, Wang X, Feng J: Molecular analysis of intestinal bacterial microbiota of broiler chickens fed diets containing fermented cottonseed meal. Poult Sci 2013, 92:392-401.
23. Oviedo-Rondon EO, Hume ME, Barbosaa NA, Sakomura NK, Weber G, Wilsone JW: Ileal and caecal microbial populations in broilers given specific essential oil blends and probiotics in two consecutive grow-outs. Avian Biology Research 2010, 3:157-169.
24. Geier MS, Torok VA, Allison GE, Ophel-Keller K, Gibson RA, Munday C, Hughes RJ: Dietary omega-3 polyunsaturated fatty acid does not influence the intestinal microbial communities of broiler chickens. Poult Sci 2009, 88:2399-2405.
25. Bjerrum L, Pedersen K, Engberg RM: The influence of whole wheat feeding on Salmonella infection and gut flora composition in broilers. Avian Dis 2005, 49:9-15.
26. Stanley D, Hughes RJ, Moore RJ: Microbiota of the chicken gastrointestinal tract: influence on health, productivity and disease. Appl Microbiol Biotechnol 2014, 98:4301-4310.
27. Videnska P, Sisak F, Havlickova H, Faldynova M, Rychlik I: Influence of Salmonella enterica serovar Enteritidis infection on the composition of chicken cecal microbiota. BMC Vet Res 2013, 9:Article number 140.
28. Singh KM, Shah TM, Reddy B, Deshpande S, Rank DN, Joshi CG: Taxonomic and gene-centric metagenomics of the fecal microbiome of low and high feed conversion ratio (FCR) broilers. J Appl Genet 2014, 55:145-154.
29. Sergeant MJ, Constantinidou C, Cogan TA, Bedford MR, Penn CW, Pallen MJ: Extensive microbial and functional diversity within the chicken cecal microbiome. PLoS One 2014, 9:e91941.
30. van der Wielen PW, Keuzenkamp DA, Lipman LJ, Van Knapen F, Biesterveld S: Spatial and temporal variation of the intestinal bacterial community in commercially raised broiler chickens during growth. Microb Ecol 2002, 44:286-293.
31. Sekelja M, Rud I, Knutsen SH, Denstadli V, Westereng B, Naes T, Rudi K: Abrupt temporal fluctuations in the chicken fecal microbiota are explained by its gastrointestinal origin. Appl Environ Microbiol 2012, 78:2941-2948.
32. Hume ME, Kubena LF, Edrington TS, Donskey CJ, Moore RW, Ricke SC, Nisbet DJ: Poultry digestive microflora biodiversity as indicated by denaturing gradient gel electrophoresis. Poult Sci 2003, 82:1100-1107.
33. Lu J, Idris U, Harmon B, Hofacre C, Maurer JJ, Lee MD: Diversity and succession of the intestinal bacterial community of the maturing broiler chicken. Appl Environ Microbiol 2003, 69:6816-6824.
34. Eren AM, Sogin ML, Morrison HG, Vineis JH, Fisher JC, Newton RJ, McLellan SL: A single genus in the gut microbiome reflects host preference and specificity. ISME J 2014. doi:10.1038/ismej.2014.97.
35. Biddle A, Stewart L, Blanchard J, Leschine S: Untangling the genetic basis of fibrolytic specialization by lachnospiraceae and ruminococcaceae in diverse gut communities. Diversity 2013, 5:627-640.
36. Donohoe DR, Garge N, Zhang X, Sun W, O'Connell TM, Bunger MK, Bultman SJ: The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab 2011, 13:517-526.
37. Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermudez-Humaran LG, Gratadoux JJ, Blugeon S, Bridonneau C, Furet JP, Corthier G, Grangette C, Vasquez N, Pochart P, Trugnan G, Thomas G, Blottiere HM, Dore J, Marteau P, Seksik P, Langella P: Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci U S A 2008, 105:16731-16736.
38. Duncan SH, Hold GL, Barcenilla A, Stewart CS, Flint HJ: Roseburia intestinalis sp. nov., a novel saccharolytic, butyrate-producing bacterium from human faeces. Int J Syst Evol Microbiol 2002, 52:1615-1620.
39. Luo YH, Peng HW, Wright ADG, Bai SP, Ding XM, Zeng QF, Li H, Zheng P, Su ZW, Cui RY, Zhang KY: Broilers fed dietary vitamins harbor higher diversity of cecal bacteria and higher ratio of Clostridium, Faecalibacterium, and Lactobacillus than broilers with no dietary vitamins revealed by 16S rRNA gene clone libraries. Poult Sci 2013, 92:2358-2366.
40. Lee GH, Kumar S, Lee JH, Chang DH, Kim DS, Choi SH, Rhee MS, Lee DW, Yoon MH, Kim BC: Genome sequence of Oscillibacter ruminantium strain GH1, isolated from rumen of Korean native cattle. J Bacteriol 2012, 194:6362.
41. Katano Y, Fujinami S, Kawakoshi A, Nakazawa H, Oji S, Iino T, Oguchi A, Ankai A, Fukui S, Terui Y, Kamata S, Harada T, Tanikawa S, Suzuki K, Fujita N: Complete genome sequence of Oscillibacter valericigenes Sjm18-20 T (=NBRC 101213 T). Stand Genomic Sci 2012, 6:406-414.
42. Rehman HU, Vahjen W, Awad WA, Zentek J: Indigenous bacteria and bacterial metabolic products in the gastrointestinal tract of broiler chickens. Arch Anim Nutr 2007, 61:319-335.
43. Fogel GB, Collins CR, Li J, Brunk CF: Prokaryotic genome size and SSU rDNA copy number: estimation of microbial relative abundance from a mixed population. Microb Ecol 1999, 38:93-113.
44. Apajalahti JHA, Särkilahti LK, Mäki BRE, Pekka Heikkinen J, Nurminen PH, Holben WE: Effective recovery of bacterial DNA and percent-guanine-plus-cytosinebased analysis of community structure in the gastrointestinal tract of broiler chickens. Appl Environ Microbiol 1998, 64:4084-4088.
45. Claassen S, Du Toit E, Kaba M, Moodley C, Zar HJ, Nicol MP: A comparison of the efficiency of five different commercial DNA extraction kits for extraction of DNA from faecal samples. J Microbiol Methods 2013, 94:103-110.
46. Oakley BB, Morales CA, Line J, Berrang ME, Meinersmann RJ, Tillman GE, Wise MG, Siragusa GR, Hiett KL, Seal BS: The poultry-associated microbiome: network analysis and farm-to-fork characterizations. PLoS One 2013, 8:e57190.
47. Izquierdo JA, Sizova MV, Lynd LR: Diversity of bacteria and glycosyl hydrolase family 48 genes in cellulolytic consortia enriched from thermophilic biocompost. Appl Environ Microbiol 2010, 76:3545-3553.
48. Stanley D, Geier MS, Denman SE, Haring VR, Crowley TM, Hughes RJ, Moore RJ: Identification of chicken intestinal microbiota correlated with the efficiency of energy extraction from feed. Vet Microbiol 2013, 164:85-92.
49. Smedley JG, Fisher DJ, Sayeed S, Chakrabarti G, McClane BA: The Enteric Toxins of Clostridium Perfringens. In Reviews of Physiology, Biochemistry and Pharmacology, Volume 152. Berlin: Springer Verlag; 2004:183-204.
50. Sawires YS, Songer JG: Clostridium perfringens: insight into virulence evolution and population structure. Anaerobe 2006, 12:23-43.
51. Van Immerseel F, De Buck J, Pasmans F, Huyghebaert G, Haesebrouck F, Ducatelle R: Clostridium perfringens in poultry: an emerging threat for animal and public health. Avian Pathol 2004, 33:537-549.
52. Qu A, Brulc JM, Wilson MK, Law BF, Theoret JR, Joens LA, Konkel ME, Angly F, Dinsdale EA, Edwards RA, Nelson KE, White BA: Comparative metagenomics reveals host specific metavirulomes and horizontal gene transfer elements in the chicken cecum microbiome. PLoS One 2008, 3:e2945.
53. Windisch W, Schedle K, Plitzner C, Kroismayr A: Use of phytogenic products as feed additives for swine and poultry. J AnimSci 2008, 86:E140-E148.
54. Vandeplas S, Dubois Dauphin R, Beckers Y, Thonart P, Théwis A: Salmonella in chicken: current and developing strategies to reduce contamination at farm level. J Food Prot 2010, 73:774-785.
55. Ricke SC, Kundinger MM, Miller DR, Keeton JT: Alternatives to antibiotics: chemical and physical antimicrobial interventions and foodborne pathogen response. Poult Sci 2005, 84:667-675.
56. Over KF, Hettiarachchy N, Johnson MG, Davis B: Effect of organic acids and plant extracts on Escherichia coli O157:H7, Listeria monocytogenes, and Salmonella Typhimurium in broth culture model and chicken meat systems. J Food Sci 2009, 74:M515-M521.
57. Heres L, Engel B, Urlings HAP, Wagenaar JA, Van Knapen F: Effect of acidified feed on susceptibility of broiler chickens to intestinal infection by Campylobacter and Salmonella. Vet Microbiol 2004, 99:259-267.
58. Van Immerseel F, Russell JB, Flythe MD, Gantois I, Timbermont L, Pasmans F, Haesebrouck F, Ducatelle R: The use of organic acids to combat salmonella in poultry: a mechanistic explanation of the efficacy. Avian Pathol 2006, 35:182-188.
59. Griffiths RI, Whiteley AS, O'Donnell AG, Bailey MJ: Rapid method for coextraction of DNA and RNA from natural environments for analysis of ribosomal DNA-and rRNA-based microbial community composition. Appl Environ Microbiol 2000, 66:5488-5491.
60. Rinttila T, Kassinen A, Malinen E, Krogius L, Palva A: Development of an extensive set of 16S rDNA-targeted primers for quantification of pathogenic and indigenous bacteria in faecal samples by real-time PCR. J Appl Microbiol 2004, 97:1166-1177.
61. Oakley BB, Morales CA, Line JE, Seal BS, Hiett KL: Application of high-throughput sequencing to measure the performance of commonly used selective cultivation methods for the foodborne pathogen Campylobacter. FEMS Microbiol Ecol 2012, 79:327-336.
62. Blankenberg D, Gordon A, Von Kuster G, Coraor N, Taylor J, Nekrutenko A: Manipulation of FASTQ data with galaxy. Bioinformatics 2010, 26:1783-1785.
63. Oakley BB, Carbonero F, Dowd SE, Hawkins RJ, Purdy KJ: Contrasting patterns of niche partitioning between two anaerobic terminal oxidizers of organic matter. ISME J 2012, 6:905-914.
64. Schloss PD, Gevers D, Westcott SL: Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 2011, 6:e27310.
65. Edgar RC: Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010, 26:2460-2461.
66. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF: Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 2009, 75:7537-7541.
67. Wang Q, Garrity GM, Tiedje JM, Cole JR: Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 2007, 73:5261-5267.
68. R DCT: R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2013.
69. Oksanen J., Blanchet FG, Kindt R, Legendre P, O'Hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Wagner H (2010): vegan: Community Ecology Package. R package version 1.17-4.
70. McArdle BH, Anderson MJ: Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 2001, 82:290-297.