Different antibiotic growth promoters induce specific changes in the cecal microbiota membership of broiler chicken

PLoS ONE

Volumn 12, Issue 2, 2017, Pages

  Costa, Marcio C ^a,b,c   Bessegatto, Jose A ^a,b   Alfieri, Amauri A ^a,b   Weese, J Scott ^a,b   Filho, João A B ^a,b   Oba, Alexandre ^a,b  

^a STATE UNIVERSITY OF LONDRINA   (Brazil)

^b UNIVERSITY OF GUELPH   (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; AVILAMYCIN; BACITRACIN ZINC; ENRAMYCIN; HALQUINOL; UNCLASSIFIED DRUG; VIRGINIAMYCIN; ANTIINFECTIVE AGENT; BACITRACIN; CLOXIQUINE; FOOD ADDITIVE; OLIGOSACCHARIDE; PEPTIDE;

ANALYSIS OF MOLECULAR VARIANCE; ANALYSIS OF VARIANCE; ANALYTIC METHOD; ARTICLE; BACTERIAL STRAIN; CECUM; CLOSTRIDIUM; CONTROLLED STUDY; DISCRIMINANT ANALYSIS; DNA EXTRACTION; FIRMICUTES; HIGH THROUGHPUT SEQUENCING; MICROFLORA; NONHUMAN; PARSIMONY ANALYSIS; PEPTOSTREPTOCOCCACEAE; PRINCIPAL COORDINATE ANALYSIS; RNA SEQUENCE; SPECIES RICHNESS; TAXONOMY; ANIMAL; ANIMAL FOOD; BACTERIUM; CHICKEN; CLASSIFICATION; DRUG EFFECTS; GENETIC VARIATION; GROWTH, DEVELOPMENT AND AGING; INTESTINE FLORA; MICROBIOLOGY; PRINCIPAL COMPONENT ANALYSIS; RANDOMIZATION; RIBOTYPING;

ANIMAL FEED; ANIMALS; ANTI-BACTERIAL AGENTS; BACITRACIN; BACTERIA; CECUM; CHICKENS; CHLOROQUINOLINOLS; FOOD ADDITIVES; GASTROINTESTINAL MICROBIOME; GENETIC VARIATION; OLIGOSACCHARIDES; PEPTIDES; PRINCIPAL COMPONENT ANALYSIS; RANDOM ALLOCATION; RIBOTYPING; VIRGINIAMYCIN;

EID: 85013324826     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0171642     Document Type: Article

References (38)

1. Castanon JIR. History of the use of antibiotic as growth promoters in European poultry feeds. Poult Sci. 2007; 86: 2466-2471. doi: 10.3382/ps.2007-00249 PMID: 17954599
2. Stutz MW, Lawton GC. Effects of diet and antimicrobials on growth, feed efficiency, intestinal Clostridium perfringens, and ileal weight of broiler chicks. Poult Sci. 1984; 63: 2036-2042. PMID: 6093090
3. Fasina YO, Newman MM, Stough JM, Liles MR. Effect of Clostridium perfringens infection and antibiotic administration on microbiota in the small intestine of broiler chickens. Poult Sci. 2015.
4. Cox LM, Yamanishi S, Sohn J, Alekseyenko AV, Leung JM, Cho I, et al. Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell. 2014; 158: 705-721. doi: 10.1016/j.cell.2014.05.052 PMID: 25126780
5. Han GG, Kim EB, Lee J, Lee J-Y, Jin G, Park J, et al. Relationship between the microbiota in different sections of the gastrointestinal tract, and the body weight of broiler chickens. Springerplus. 2016; 5: 911. doi: 10.1186/s40064-016-2604-8 PMID: 27386355
6. Latorre JD, Hernandez-Velasco X, Wolfenden RE, Vicente JL, Wolfenden AD, Menconi A, et al. Evaluation and Selection of Bacillus Species Based on Enzyme Production, Antimicrobial Activity, and Biofilm Synthesis as Direct-Fed Microbial Candidates for Poultry. Front Vet Sci. 2016; 3: 95. doi: 10.3389/fvets. 2016.00095 PMID: 27812526
7. Singh KM, Shah T, Deshpande S, Jakhesara SJ, Koringa PG, Rank DN, et al. High through put 16S rRNA gene-based pyrosequencing analysis of the fecal microbiota of high FCR and low FCR broiler growers. Mol Biol Rep. 2012; 39: 10595-10602. doi: 10.1007/s11033-012-1947-7 PMID: 23053958
8. Maron DF, Smith TJS, Nachman KE. Restrictions on antimicrobial use in food animal production: an international regulatory and economic survey. Global Health. 2013; 9: 48. doi: 10.1186/1744-8603-9-48 PMID: 24131666
9. Miller M. The White House Forum on Antibiotic Stewardship impacts labs across the U.S. MLO Med Lab Obs. 2015; 47: 28.
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. doi: 10.1038/ nature05414 PMID: 17183312
11. Yegani M, Korver DR. Factors affecting intestinal health in poultry. Poult Sci. 2008; 87: 2052-2063. doi: 10.3382/ps.2008-00091 PMID: 18809868
12. Costa MC, Stampfli HR, Arroyo LG, Allen-Vercoe E, Gomes RG, Weese JS. Changes in the equine fecal microbiota associated with the use of systemic antimicrobial drugs. BMC Veterinary Research. 2015; 11: 19. doi: 10.1186/s12917-015-0335-7 PMID: 25644524
13. Patterson JA, Burkholder KM. Application of prebiotics and probiotics in poultry production. Poult Sci. 2003; 82: 627-631. PMID: 12710484
14. 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. doi: 10.1080/ 17450390701556817 PMID: 18030916
15. 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. doi: 10.1371/ journal.pone.0091941 PMID: 24657972
16. Stanley D, Denman SE, Hughes RJ, Geier MS, Crowley TM, Chen H, et al. Intestinal microbiota associated with differential feed conversion efficiency in chickens. Appl Microbiol Biotechnol. 2012; 96: 1361-1369. doi: 10.1007/s00253-011-3847-5 PMID: 22249719
17. Pourabedin M, Guan L, Zhao X. Xylo-oligosaccharides and virginiamycin differentially modulate gut microbial composition in chickens. Microbiome. 2015; 3: 15. doi: 10.1186/s40168-015-0079-4 PMID: 25874109
18. Dumonceaux TJ, Hill JE, Hemmingsen SM, Van Kessel AG. Characterization of intestinal microbiota and response to dietary virginiamycin supplementation in the broiler chicken. Applied and Environmental Microbiology. 2006; 72: 2815-2823. doi: 10.1128/AEM.72.4.2815-2823.2006 PMID: 16597987
19. Lu J, Hofacre C, Smith F, Lee MD. Effects of feed additives on the development on the ileal bacterial community of the broiler chicken. Animal. 2008; 2: 669-676. doi: 10.1017/S1751731108001894 PMID: 22443592
20. Wise MG, Siragusa GR. Quantitative analysis of the intestinal bacterial community in one- to threeweek-old commercially reared broiler chickens fed conventional or antibiotic-free vegetable-based diets. Journal of Applied Microbiology. 2007; 102: 1138-1149. doi: 10.1111/j.1365-2672.2006.03153.x PMID: 17381758
21. Neumann AP, Suen G. Differences in major bacterial populations in the intestines of mature broilers after feeding virginiamycin or bacitracin methylene disalicylate. Journal of Applied Microbiology. 2015.
22. Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Research. 2013; 41: e1-e1. doi: 10.1093/nar/gks808 PMID: 22933715
23. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a Dual-Index Sequencing Strategy and Curation Pipeline for Analyzing Amplicon Sequence Data on the MiSeq Illumina Sequencing Platform. Applied and Environmental Microbiology. 2013; 79: 5112-5120. doi: 10. 1128/AEM.01043-13 PMID: 23793624
24. Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, et al. Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucleic Acids Research. 2014; 42: D633-42. doi: 10.1093/nar/ gkt1244 PMID: 24288368
25. Costa MC, Arroyo LG, Allen-Vercoe E, Stampfli HR, Kim PT, Sturgeon A, et al. Comparison of the fecal microbiota of healthy horses and horses with colitis by high throughput sequencing of the V3-V5 region of the 16S rRNA gene. PLoS ONE. 2012; 7: e41484. doi: 10.1371/journal.pone.0041484 PMID: 22859989
26. Dufrene M, Legendre P. Species assemblages and indicator species: The need for a flexible asymmetrical approach. Ecol Monogr 1997; 67: 345-66.
27. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011; 12: R60. doi: 10.1186/gb-2011-12-6-r60 PMID: 21702898
28. Videnska P, Faldynova M, Juricova H, Babak V, Sisak F, Havlickova H, et al. Chicken faecal microbiota and disturbances induced by single or repeated therapy with tetracycline and streptomycin. BMC Veterinary Research. 2013; 9: 30. doi: 10.1186/1746-6148-9-30 PMID: 23406343
29. Torok VA, Hughes RJ, Mikkelsen LL, Perez-Maldonado R, Balding K, MacAlpine R, et al. Identification and characterization of potential performance-related gut microbiotas in broiler chickens across various feeding trials. Applied and Environmental Microbiology. 2011; 77: 5868-5878. doi: 10.1128/AEM. 00165-11 PMID: 21742925
30. Pedroso AA, Menten JFM, Lambais MR, Racanicci AMC, Longo FA, Sorbara JOB. Intestinal bacterial community and growth performance of chickens fed diets containing antibiotics. Poult Sci. 2006; 85: 747-752. PMID: 16615359
31. 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. doi: 10.1371/journal.pone.0027949 PMID: 22114729
32. Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A. 2005; 102: 11070-11075. doi: 10.1073/pnas.0504978102 PMID: 16033867
33. Jami E, White BA, Mizrahi I. Potential role of the bovine rumen microbiome in modulating milk composition and feed efficiency. PLoS ONE. 2014; 9: e85423. doi: 10.1371/journal.pone.0085423 PMID: 24465556
34. Mancabelli L, Ferrario C, Milani C, Mangifesta M, Turroni F, Duranti S, et al. Insights into the biodiversity of the gut microbiota of broiler chickens. Environ Microbiol. 2016.
35. Wei S, Morrison M, Yu Z. Bacterial census of poultry intestinal microbiome. Poult Sci. 2013; 92: 671-683. doi: 10.3382/ps.2012-02822 PMID: 23436518
36. Reed S, Neuman H, Moscovich S, Glahn RP, Koren O, Tako E. Chronic Zinc Deficiency Alters Chick Gut Microbiota Composition and Function. Nutrients. 2015; 7: 9768-9784. doi: 10.3390/nu7125497 PMID: 26633470
37. Gong J, Si W, Forster RJ, Huang R, Yu H, Yin Y, et al. 16S rRNA gene-based analysis of mucosa-associated bacterial community and phylogeny in the chicken gastrointestinal tracts: from crops to ceca. FEMS Microbiol Ecol. 2007; 59: 147-157. doi: 10.1111/j.1574-6941.2006.00193.x PMID: 17233749
38. Polansky O, Sekelova Z, Faldynova M, Sebkova A, Sisak F, Rychlik I. Important Metabolic Pathways and Biological Processes Expressed by Chicken Cecal Microbiota. Applied and Environmental Microbiology. 2015; 82: 1569-1576. doi: 10.1128/AEM.03473-15 PMID: 26712550