Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-22T11:46:47.383Z Has data issue: false hasContentIssue false
  • English
  • Français

The microbiome of the chicken gastrointestinal tract

Published online by Cambridge University Press:  04 July 2012

Carl J. Yeoman ,
Nicholas Chia ,
Patricio Jeraldo ,
Maksim Sipos ,
Nigel D. Goldenfeld  and
Bryan A. White
Carl J. Yeoman
Affiliation:
Department of Animal and Range Sciences, Montana State University, P.O. Box 172900, Bozeman, MT 59717, USA Institute for Genomic Biology, University of Illinois at Urbana-Champaign, 1206 West Gregory Drive, Urbana, IL 61801, USA
Nicholas Chia
Affiliation:
Institute for Genomic Biology, University of Illinois at Urbana-Champaign, 1206 West Gregory Drive, Urbana, IL 61801, USA Loomis Laboratory of Physics, 1110 West Green St., Urbana, IL 61801, USA Center for Individualized Medicine, Mayo Clinic, Rochester, MN 55905, USA
Patricio Jeraldo
Affiliation:
Institute for Genomic Biology, University of Illinois at Urbana-Champaign, 1206 West Gregory Drive, Urbana, IL 61801, USA Loomis Laboratory of Physics, 1110 West Green St., Urbana, IL 61801, USA Center for Individualized Medicine, Mayo Clinic, Rochester, MN 55905, USA
Maksim Sipos
Affiliation:
Institute for Genomic Biology, University of Illinois at Urbana-Champaign, 1206 West Gregory Drive, Urbana, IL 61801, USA Loomis Laboratory of Physics, 1110 West Green St., Urbana, IL 61801, USA
Nigel D. Goldenfeld
Affiliation:
Institute for Genomic Biology, University of Illinois at Urbana-Champaign, 1206 West Gregory Drive, Urbana, IL 61801, USA Loomis Laboratory of Physics, 1110 West Green St., Urbana, IL 61801, USA
Bryan A. White*
Affiliation:
Institute for Genomic Biology, University of Illinois at Urbana-Champaign, 1206 West Gregory Drive, Urbana, IL 61801, USA Department of Animal Sciences, 1207 West Gregory Drive, Urbana, IL 61801, USA
*
*Corresponding author. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The modern molecular biology movement was developed in the 1960s with the conglomeration of biology, chemistry, and physics. Today, molecular biology is an integral part of studies aimed at understanding the evolution and ecology of gastrointestinal microbial communities. Molecular techniques have led to significant gains in our understanding of the chicken gastrointestinal microbiome. New advances, primarily in DNA sequencing technologies, have equipped researchers with the ability to explore these communities at an unprecedented level. A reinvigorated movement in systems biology offers a renewed promise in obtaining a more complete understanding of chicken gastrointestinal microbiome dynamics and their contributions to increasing productivity, food value, security, and safety as well as reducing the public health impact of raising production animals. Here, we contextualize the contributions molecular biology has already made to our understanding of the chicken gastrointestinal microbiome and propose targeted research directions that could further exploit molecular technologies to improve the economy of the poultry industry.

Keywords

16S rRNA genegenomic analysisnutritionreducing pathogen loadantibiotic resistance genesvirulence genes
Type
Review Article
Information
Animal Health Research Reviews , Volume 13 , Issue 1 , June 2012 , pp. 89 - 99
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abro, SH, Renström, LHM, Ullman, K, Belák, S and Baule, C (2012). Characterization and analysis of the full-length genome of a strain of the European QX-like genotype of infectious bronchitis virus. Archives of Virology 157(6): 1211–1215.CrossRefGoogle ScholarPubMed
Ahir, VB, Roy, A, Jhala, MK, Bhanderi, BB, Mathakiya, RA, Bhatt, VD, Padiya, KB, Jakhesara, SJ, Koringa, PG and Joshi, CG (2011). Genome sequence of Pasteurella multocida subsp. Gallicida Anand1_poultry. Journal of Bacteriology 193: 5604.CrossRefGoogle ScholarPubMed
Amann, RI, Ludwig, W and Schleifer, KH (1995). Phylogenetic identification and in situ detection of individual microbial cells without culturing. Microbiological Reviews 59: 143–169.CrossRefGoogle Scholar
Aydin, R, Pariza, MW and Cook, ME (2001). Olive oil prevents the adverse affects of dietary conjugated linoleic acid on chick hatchability and egg quality. Journal of Nutritional Sciences 131: 800–806.Google Scholar
Badinga, L and Greene, ES (2006). Physiological properties of conjugated linoleic acid and implications for human health. Nutrition in Clinical Practice 21: 367–373.CrossRefGoogle ScholarPubMed
Barbosa, T, Zavala, G, Cheng, S and Villegas, P (2007). Full genome sequence and some biological properties of reticuloendotheliosis virus strain APC-566 isolated from endangered Attwater's prairie chickens. Virus Research 124: 68–77.CrossRefGoogle ScholarPubMed
Beckmann, L, Simon, O and Vahjen, W (2006). Isolation and identification of mixed beta-glucan degrading bacteria in the intestine of broiler chickens and partial characterization of respective 1,3-1,4-beta-glucanase activities. Journal of Basic Microbiology 46: 175–185.CrossRefGoogle ScholarPubMed
Carina Audisio, M, Oliver, G and Apella, MC (2000). Protective effect of Enterococcus faecium J96, a potential probiotic strain, on chicks infected with Salmonella pullorum. Journal of Food Production 63: 1333–1337.CrossRefGoogle ScholarPubMed
Chapman, HD, Jeffers, TK and Williams, RB (2010). Forty years of monensin for the control of coccidiosis in poultry. Poultry Science 89: 1788–1801.CrossRefGoogle ScholarPubMed
Cole, JR Jr and Boyd, FM (1967). Fat absorption from the small intestine of gnotobiotic chicks. Applied Microbiology 15(5): 1229–1234.CrossRefGoogle ScholarPubMed
Collignon, P, Powers, JH, Chiller, TM, Aidara-Kane, A and Aarestrup, FM (2009). World Health Organization ranking of antimicrobials according to their importance in human medicine: A critical step for developing risk management strategies for the use of antimicrobials in food production animals. Clinical Infectious Diseases 49: 132–141.CrossRefGoogle ScholarPubMed
Cooper, KK, Cooper, MA, Zuccolo, A, Law, B and Joens, LA (2011). Complete genome sequence of Campylobacter jejuni strain S3. Journal of Bacteriology 193: 1491–1492.CrossRefGoogle ScholarPubMed
D'Costa, VM, King, CE, Kalan, L, Morar, M, Sung, WW, Schwarz, C, Froese, D, Zazula, G, Calmels, F, Debruyne, R, Golding, GB, Poinar, HN and Wright, GD (2011). Antibiotic resistance is ancient. Nature 477: 457–461.CrossRefGoogle ScholarPubMed
Danzeisen, JL, Kim, HB, Isaacson, RE, Tu, ZJ and Johnson, TJ (2011). Modulations of the chicken cecal microbiome and metagenome in response to anticoccidal and growth promoter treatment. PLoS One 6: e27949.CrossRefGoogle Scholar
Dethlefsen, L, Huse, S, Sogin, ML and Relman, DA (2008). The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biology 6: e280.CrossRefGoogle Scholar
Dhawi, AA, Elazomi, A, Jones, MA, Lovell, MA, Li, H, Emes, RD and Barrow, PA (2011). Adaptation to the chicken intestine in Salmonella enteritidis PT4 studied by transcriptional analysis. Veterinary Microbiology 153: 198–204.CrossRefGoogle Scholar
Dhiman, TR, Nam, S and Ure, AL (2005). Factors affecting conjugated linoleic acid content in milk and meat. Critical Reviews in Food Science and Nutrition 45: 463–482.CrossRefGoogle ScholarPubMed
Diel, DG, Susta, L, Cardenas Garcia, S, Killian, ML, Brown, CC, Miller, PJ, and Afonso, CL (2012). Complete genome and clinicopathological characterization of a virulent Newcastle disease virus isolate from South America. Journal of Clinical Microbiology 50: 378–387.CrossRefGoogle ScholarPubMed
Donohoe, DR, Garge, N, Zhang, X, Sun, W, O'Connell, TM, Bunger, MK and Bultman, SJ (2011). The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metabolism 13: 489–490.CrossRefGoogle ScholarPubMed
Dunkley, KD, Dunkley, CS, Njongmeta, NL, Callaway, TR, Hume, ME, Kubena, LF, Nisbet, DJ and Ricke, SC (2007). Comparison of in vitro fermentation and molecular microbial profiles of high-fiber feed substrates incubated with chicken cecal inocula. Poultry Science 86: 801–810.CrossRefGoogle ScholarPubMed
Feng, Y, Xu, HF, Li, QH, Zhang, SY, Wang, CX, Zhu, DL, Cao, FL, Li, YG, Johnston, RN, Zhou, J, Liu, GR and Liu, SL (2012). Complete genome sequence of Salmonella enterica serovar pullorum RKS5078. Journal of Bacteriology 194: 744.CrossRefGoogle ScholarPubMed
Flint, HJ and Bayer, EA (2008). Plant cell wall breakdown by anaerobic microorganisms from the mammalian digestive tract. Annals of the New York Academy of Sciences 1125: 280–288.CrossRefGoogle ScholarPubMed
Fukata, T, Hadate, Y, Baba, E and Arakawa, A (1991). Influence of bacteria on Clostridium prefringens infections in young chickens. Avian Diseases 35: 224–227.CrossRefGoogle Scholar
Gipp, E, Hlahla, D, Didelot, X, Kops, F, Maurischat, S, Tedin, K, Alter, T, Ellerbroek, L, Schreiber, K, Schomburg, D, Janssen, T, Batholomäus, P, Hofreuter, D, Woltemate, S, Uhr, M, Brenneke, B, Grüning, P, Gerlach, G, Wieler, L, Suerbaum, S and Josenhans, C (2011). Closely related Campylobacter jejuni strains from different sources reveal a generalist rather than a specialist lifestyle. BMC Genomics 12: 584.Google Scholar
Glenn, LM, Englen, MD, Lindsey, RL, Frank, JF, Turpin, JE, Berrang, ME, Meinersmann, RJ, Fedorka-Cray, PJ and Frye, JG (2012). Analysis of antimicrobial resistance genes detected in multiple-drug-resistant Escherichia coli isolates from broiler chicken carcasses. Microbial Drug Resistance. In press.CrossRefGoogle ScholarPubMed
Gong, J, Forster, RJ, Yu, H, Chambers, JR, Sabour, PM, Wheatcroft, R and Chen, S (2002). Diversity and phylogenetic analysis of bacteria in the mucosa of chicken ceca and comparison with bacteria in the cecal lumen. FEMS Microbiology Letters. 208: 1–7.CrossRefGoogle ScholarPubMed
Gong, J, Si, W, Forster, RJ, Huang, R, Hai, Y, Yulong, Y, Yang, C and Han, Y (2007). 16S rRNA gene-based analysis of mucosa-associated bacterial community and phylogeny in the chicken gastrointestinal tracts: from crops to ceca. FEMS Microbial Ecology 59: 147–157.CrossRefGoogle ScholarPubMed
Gronow, S, Held, B, Lucas, S, Lapidus, A, Del Rio, TG, Nolan, M, Tice, H, Deshpande, S, Cheng, JF, Pitluck, S, Liolios, K, Pagani, I, Ivanova, N, Mavromatis, K, Pati, A, Tapia, R, Han, C, Goodwin, L, Chen, A, Palaniappen, K, Land, M, Hauser, L, Chang, YJ, Jefferies, CD, Brambilla, EM, Rohde, M, Göker, M, Detter, JC, Woyke, T, Bristow, J, Markowitz, V, Hugenholtz, P, Krypides, NC, Klenk, HP and Eisen, JA (2011). Complete genome sequence of Bacteroides salanitronis type strain (BL78). Standards in Genomic Science 4: 191–199.CrossRefGoogle ScholarPubMed
Gustafson, RH and Bowen, RE (1997). Antibiotic use in animal agriculture. Journal of Applied Microbiology 83: 531–541.CrossRefGoogle ScholarPubMed
Gyles, CL (2008). Antimicrobial resistance in selected bacteria from poultry. Animal Health Research Reviews 9: 149–158.CrossRefGoogle ScholarPubMed
Hai, Y, Zhou, T, Gong, J, Young, C, Su, X, Li, XZ, Zhu, H, Tsao, R and Yang, R (2010). Isolation of deoxynivalenol-transforming bacteria from the chicken intestines using the approach of PCR-DGGE guided microbial selection. BMC Microbiology 10: 182.Google Scholar
Ham, JS, Kim, HW, Seol, KH, Jang, A, Jeong, SG, Oh, MH, Kim, DH, Kang, DK, Kim, GB and Cha, CJ (2011). Genome sequence of Lactobacillus salivarius NIAS840, isolated from chicken intestine. Journal of Bacteriology 193: 5551–5552.CrossRefGoogle ScholarPubMed
Harvey, PC, Watson, M, Hulme, S, Jones, MA, Lovell, M, Berchieri, A Jr, Young, J, Bumstead, N and Barrow, P (2011). Salmonella enterica serovar typhimurium colonizing the lumen of the chicken intestine grows slowly and upregulates a unique set of virulence and metabolism genes. Infection and Immunity 79: 4105–4121.CrossRefGoogle ScholarPubMed
Higgins, CH (1898). Notes upon an epidemic of fowl cholera and upon the comparative production of acid by allied bacteria. Journal of Experimental Medicine 3: 651–668.CrossRefGoogle ScholarPubMed
Hudault, S, Bewa, H, Bridonneau, C and Raibaud, P (1985). Efficiency of various bacterial suspensions derived from cecal floras of conventional chickens in reducing the population level of Salmonella typhimurium in gnotobiotic mice and chicken intestines. Canadian Journal of Microbiology 31: 832–838.CrossRefGoogle ScholarPubMed
Hughes, VM and Datta, N (1983). Conjugative plasmids in bacteria of the ‘pre-antibiotic’ era. Nature 302: 725–726.CrossRefGoogle ScholarPubMed
Huse, SM, Dethlefsen, L, Huber, JA, Mark Welch, D, Relman, DA and Sogin, ML (2008). Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genetics 4: e1000255.CrossRefGoogle ScholarPubMed
Jeurissen, SH, Janse, EM, van Rooijen, N and Claassen, E (1998). Inadequate anti-polysaccharide antibody responses in the chicken. Immunobiology 198: 385–395.CrossRefGoogle ScholarPubMed
Jin, LZ, Ho, YW, Abdullah, N, Ali, MA and Jalaludin, S (1996). Antagonistic effects of intestinal Lactobacillus isolates on pathogens of chickens. Letters in Applied Microbiology 23: 67–71.CrossRefGoogle Scholar
Johnson, TJ, Fernandez-Alarcon, C, Bojesen, AM, Nolan, LK, Trampel, DW and Seemann, T (2011). Complete genome sequence of Gallibacterium anatis strain UMN179, isolated from a laying hen with peritonitis. Journal of Bacteriology 193: 3676–3677.CrossRefGoogle ScholarPubMed
Johnson, TJ, Kariyawasam, S, Wannemuehler, Y, Mangiamele, P, Johnson, SJ, Doetkott, C, Skyberg, JA, Lynne, AM, Johnson, JR and Nolan, LK (2007). The genome sequence of avian pathogenic Escherichia coli strain O1:K1:H7 shares strong similarities with human extraintestinal pathogenic E. coli genomes. Journal of Bacteriology 189: 3228–3236.CrossRefGoogle ScholarPubMed
Johnson, TJ, Logue, CM, Wannemuehler, Y, Kariyawasam, S, Doetkott, C, DebRoy, C, White, DG and Nolan, LK (2009). Examination of the source and extended virulence genotypes of Escherichia coli contaminating retail poultry meat. Foodborne Pathogens and Disease 6: 657–667.CrossRefGoogle ScholarPubMed
Johnson, TJ, Wannemuehler, Y, Johnson, SJ, Stell, AL, Doetkott, C, Johnson, JR, Kim, KS, Spanjaard, L and Nolan, LK (2008). Comparison of extraintestinal pathogenic Escherichia coli strains from human and avian sources reveals a mixed subset representing potential zoonotic pathogens. Applied and Environmental Microbiology 74: 7043–7050.CrossRefGoogle ScholarPubMed
Kimura, N, Mimura, F, Nishida, S and Kobayashi, A (1976). Studies on the relationship between intestinal flora and cecal coccidiosis in chicken. Poultry Science 55: 1375–1383.CrossRefGoogle ScholarPubMed
Ladely, SR, Harrison, MA, Fedorka-Cray, PJ, Berrang, ME, Englen, MD and Meinersmann, RJ (2007). Development of macrolide-resistant Campylobacter in broilers administered subtherapeutic or therapeutic concentrations of tylosin. Journal of Food Protection 70: 1945–1951.CrossRefGoogle ScholarPubMed
Lee, JH, Shin, H and Ryu, S (2012). Complete genome sequence of Salmonellla enterica serovar typhimurium bacteriophage SPN3UB. Journal of Virology 86: 3404–3405.CrossRefGoogle ScholarPubMed
Ley, RE, Hamady, M, Lozuone, C, Turnbaugh, PJ, Ramey, RR, Bircher, JS, Schlegel, ML, Tucker, TA, Schrenzel, MD, Knight, R and Gordon, JI (2008). Evolution of mammals and their gut microbes. Science 320: 1647–1651.CrossRefGoogle ScholarPubMed
Linde, AM, Munir, M, Zohari, S, Stáhl, K, Baule, C, Renström, L and Berg, M (2010). Complete genome characterization of a Newcastle disease virus isolated during an outbreak in Sweden in 1997. Virus Genes 41: 165–173.CrossRefGoogle ScholarPubMed
Lowder, BV, Guinane, CM, Ben Zakour, NL, Weinert, LA, Conway-Morris, A, Cartwright, RA, Simpson, AJ, Rambaut, A, Nübel, U and Fitzgerald, JR (2009). Recent human-to-poultry host jump, adaptation, and pandemic spread of Staphylococcus aureus. Proceedings of the National Academy of Science USA 106: 19545–19550.CrossRefGoogle ScholarPubMed
McCubbin, DR, Apelberg, BJ, Roe, S and Divita, F (2002). Livestock ammonia management and particulate-related health benefits. Environmental Science and Technology 36: 1141–1146.CrossRefGoogle ScholarPubMed
McNeil, NI (1984). The contribution of the large intestine to energy supplies in man. American Journal of Clinical Nutrition 39: 338–342.Google ScholarPubMed
Morishita, Y and Mitsuoka, T (1976). Microorganisms responsible for controlling the populations of Escherichia coli and enterococcus and the consistency of cecal contents in the chicken. Japanese Journal of Microbiology 20: 197–202.CrossRefGoogle ScholarPubMed
Morris, SC (2003). Life's Solution: Inevitable Humans in a Lonely Universe. Cambridge, United Kingdom: Cambridge University Press.CrossRefGoogle Scholar
Ojala, T, Kuparinen, V, Koskinen, JP, Alatalo, E, Holm, L, Auvinen, P, Edelman, S, Westerlund-Wikström, B, Korhonen, TK, Paulin, L and Kankainen, M (2010). Genome sequence of Lactobacillus crispatus ST1. Journal of Bacteriology 192: 3547–3548.CrossRefGoogle ScholarPubMed
Okulewicz, A and Zlotorzycka, J (1985). Connections between Ascaridia galli and the bacterial flora in the intestine of hens. Angewandte Parasitology 26: 151–155.Google ScholarPubMed
Palmquist, DL, Lock, AL, Shingfield, KJ and Bauman, DE (2005). Biosynthesis of conjugated linoleic acid in ruminants and humans. Advanced Food Nutrition Research 50: 179–217.CrossRefGoogle ScholarPubMed
Panda, AK, Rama Rao, SV, Raju, MVLN and Shyam Sunder, G (2009). Effect of butyric acid on performance, gastrointestinal tract health and carcass characteristics in broiler chickens. Asian-Australian Journal of Animal Science 22: 1026–1031.CrossRefGoogle Scholar
Pearson, BM, Gaskin, DJ, Segers, RP, Wells, JM, Nuijten, PJ and van Vliet, AH (2007). The complete genome sequence of Campylobacter jejuni strain 81116 (NCTC11828). Journal of Bacteriology 189: 8402–8403.CrossRefGoogle ScholarPubMed
Price, LB, Stegger, M, Hasman, H, Aziz, M, Larsen, J, Andersen, PS, Pearson, T, Waters, AE, Foster, JT, Schupp, J, Gillece, J, Driebe, E, Liu, CM, Springer, B, Zdovc, I, Battisti, A, Franco, A, Zmudzki, J, Schwarz, S, Butaye, P, Jouy, E, Pomba, C, Porrero, MC, Ruimy, R, Smith, TC, Robinson, DA, Weese, JC, Arriola, CS, Yu, F, Laurent, F, Keim, P, Skov, R and Aarestrup, FM (2012). Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. mBio 3: e00305–e00311.CrossRefGoogle ScholarPubMed
Qiu, X, Sun, Q, Wu, S, Dong, L, Hu, S, Meng, C, Wu, Y and Liu, X (2011). Entire genome sequence analysis of genotype IX Newcastle disease viruses reveals their early-genotype phylogenetic position and recent-genotype genome size. Virology Journal 8: 117.CrossRefGoogle ScholarPubMed
Qu, A, Brulc, JM, Wilson, MK, Law, BF, Theoret, JR, Joens, LA, Konkel, ME, Angly, F, Dinsdale, EA, Edwards, RA, Nelson, KE and White, BA (2008). Comparative metagenomics reveals host-specific metavirulomes and horizontal gene transfer elements in the chicken cecum microbiome. PLoS One 3: e2945.CrossRefGoogle ScholarPubMed
Rehman, HU, Vahjen, W, Awad, WA and Zentek, J (2007). Indigenous bacteria and bacterial metabolic products in the gastrointestinal tract of broiler chickens. Archives of Animal Nutrition 61: 319–335.CrossRefGoogle ScholarPubMed
Rodriguez-Valera, F, Martin-Cuadrado, A, Rodriguez-Brito, B, Pasic, L, Thingstad, TF, Rohwer, F and Mira, A (2009). Explaining microbial population genomics through phage predation. Nature Reviews Microbiology 7: 828–836.CrossRefGoogle ScholarPubMed
Saengkerdsub, S, Anderson, RC, Wilkinson, HH, Kim, WK, Nisbet, DJ and Ricke, SC (2007a). Identification and quantification of methanogenic archaea in adult chicken ceca. Applied and Environmental Microbiology 73: 353–356.CrossRefGoogle ScholarPubMed
Saengkerdsub, S, Herrera, P, Woodward, CL, Anderson, RC, Nisbet, DJ and Ricke, SC (2007b). Detection of methane and quantification of methanogenic archaea in faeces from young broiler chickens using real-time PCR. Letters in Applied Microbiology 45: 629–634.CrossRefGoogle ScholarPubMed
Salanitro, JP, Blake, IG and Muirhead, PA (1974). Studies on the cecal microflora of commercial broiler chickens. Applied Microbiology 28: 439–447.CrossRefGoogle ScholarPubMed
Schoeni, JL and Wong, AC (1994). Inhibition of Campylobacter jejuni colonization in chicks by defined competitive exclusion bacteria. Applied and Environmental Microbiology 60: 1191–1197.CrossRefGoogle ScholarPubMed
Schultsz, C and Geerlings, S (2012). Plasmid-mediated resistance in Enterobacteriaceae: changing landscape and implications for therapy. Drugs 72: 1–16.CrossRefGoogle ScholarPubMed
Shakouri, MD, Lji, PA, Mikkelsen, LL and Cowieson, AJ (2009). Intestinal function and gut microflora of broiler chickens as influenced by cereal grains and microbial enzyme supplementation. Animal Physiology and Animal Nutrition 93: 647–658.CrossRefGoogle ScholarPubMed
Simon, O, Männer, K, Schäfer, K, Sagredos, A and Eder, K (2000). Effects of conjugated linoleic acids on protein to fat proportions, fatty acids, and plasma lipids in broilers. European Journal of Lipid Science and Technology 102: 402–410.3.0.CO;2-T>CrossRefGoogle Scholar
Soerjadi-Liem, AS, Snoeyenbos, GH and Weinack, OM (1984). Comparative studies on competitive exclusion of three isolates of Campylobacter fetus subsp. Jejuni in chickens by native gut microflora. Avian Diseases 28: 139–146.CrossRefGoogle ScholarPubMed
Stokstad, ELR and Jukes, TH (1950). Further observations on the animal protein factor. Proceedings of the Society of Experimental Biology and Medicine 73: 523–528.CrossRefGoogle Scholar
Swann, MM (1969). Report: Joint committee on the use of antibiotics in animal husbandry and veterinary medicine. London, UK: HMSO.Google Scholar
Thaller, MC, Migliore, L, Marquez, C, Tapia, W, Cedeño, V, Rossolini, GM and Gentile, G (2010). Tracking acquired antibiotic resistance in commensal bacteria of Galápagos Land Iguanas: no man, no resistance. PLoS ONE 5: e8989.CrossRefGoogle ScholarPubMed
Thomson, NR, Clayton, DJ, Windhorst, D, Vernikos, G, Davidson, S, Churcher, C, Quail, M, Stevens, M, Jones, MA, Watson, M, Barron, A, Layton, A, Pickard, D, Kingsley, RA, Bignell, A, Clark, L, Harris, B, Ormond, D, Abdellah, Z, Brooks, K, Cherevach, I, Chillingworth, T, Woodward, J, Norberczak, H, Lord, A, Arrowsmith, C, Jagels, K, Moule, S, Mungall, K, Sanders, M, Whitehead, S, Chabalgoity, JA, Maskell, D, Humphrey, T, Roberts, M, Barrow, PA, Dougan, D and Parkhill, J (2008). Comparative genome analysis of Salmonella enteritidis PT4 and Salmonella gallinarum 287/91 provides insight into evolutionary and host adaptation pathways. Genome Research 18: 1624–1637.CrossRefGoogle ScholarPubMed
Topping, DL and Clifton, PM (2001). Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiological Reviews 81: 1031–1064.CrossRefGoogle ScholarPubMed
Toth, TE and Siegel, PB (1986). Cellular defense of the avian respiratory tract: paucity of free-residing macrophages in the normal chicken. Avian Diseases 30: 67–75.CrossRefGoogle ScholarPubMed
Turnbaugh, PJ, Hamady, M, Yatsunenko, T, Cantarel, BL, Duncan, A, Ley, RE, Sogin, ML, Jones, WJ, Roe, BA, Affourtit, JP, Egholm, M, Henrissat, B, Heath, AC, Knight, R and Gordon, JI (2008). A core gut microbiome in obese and lean twins. Nature 457: 480–484.CrossRefGoogle ScholarPubMed
Volozhantsev, NV, Verevkin, VV, Bannov, VA, Krasilnikova, VM, Myakinina, VP, Zhilenkov, EL, Svetoch, EA, Stern, NJ, Oakley, BB and Seal, BS (2011). The genome sequence and proteome of bacteriophage ΦCPV1 virulent for Clostridium perfringens. Virus Research 155: 433–439.CrossRefGoogle ScholarPubMed
Wong, JM, de Souza, R, Kendall, CW, Emam, A and Jenkins, DJ (2006). Colonic health: fermentation and short chain fatty acids. Journal of Clinical Gastroenterology 40: 235–243.CrossRefGoogle ScholarPubMed
Xin, H, Gates, RS, Green, AR, Mitloehner, FM, Moore, PA Jr and Wathes, CM (2011). Environmental impacts and sustainability of egg production systems. Poultry Science 90: 263–277.CrossRefGoogle ScholarPubMed
Yeoman, CJ, Chia, N, Yildirim, S, Berg Miller, ME, Stumpf, R, Leigh, SR, Kent, A, Nelson, KE, White, BA and Wilson, BA (2011). Towards an evolutionary model of animal-associated microbiomes. Entropy 13: 570–594.CrossRefGoogle Scholar
Zhou, W, Wang, Y and Lin, J (2012). Functional cloning and characterization of antibiotic resistance genes from the chicken gut microbiome. Applied and Environmental Microbiology 78: 3028–3032.CrossRefGoogle ScholarPubMed