1887

Abstract

Antibiotics are widely used at sub-lethal concentrations as a feed supplement to enhance poultry productivity. To understand antibiotic-induced temporal changes in the structure and function of gut microbiota of chicken, two flocks were maintained for six weeks on a carbohydrate- and protein-rich diet. The feed in the conventional diet (CD) group was supplemented with sub-lethal doses of chlorotetracycline, virginiamycin and amoxicillin, while the organic diet (OD) had no such addition. Antibiotic-fed birds were more productive, with a lower feed conversion ratio (FCR). Their faecal samples also had higher total heterotrophic bacterial load and antibiotic resistance capability. Deep sequencing of 16S rDNA V1-V2 amplicons revealed as the most dominant phylum at all time points, with the predominant presence of members in the OD group. The productivity indicator, i.e. higher : ratio, particularly in the late growth phase, was more marked in CD amplicon sequences, which was supported by culture-based enumerations on selective media. CD datasets also showed the prevalence of known butyrate-producing genera such as , , , and , which correlates closely with their higher PICRUSt-based predicted ‘glycan biosynthesis and metabolism’-related Kyoto Encyclopedia of Genes and Genomes (KEGG) orthologues. Semi-quantitative end-point PCR targeting of the butyryl-CoA: acetate CoA-transferase gene also confirmed butyrate producers as being late colonizers, particularly in antibiotic-fed birds in both the CD flocks and commercial rearing farms. Thus, antibiotics preferentially enrich bacterial populations, particularly short-chain fatty acid producers that can efficiently metabolize hitherto undigestable feed material such as glycans, thereby increasing the energy budget of the host and its productivity.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000597
2018-02-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/micro/164/2/142.html?itemId=/content/journal/micro/10.1099/mic.0.000597&mimeType=html&fmt=ahah

References

  1. 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 [View Article][PubMed]
    [Google Scholar]
  2. Mohd Shaufi MA, Sieo CC, Chong CW, Gan HM, Ho YW. Deciphering chicken gut microbial dynamics based on high-throughput 16S rRNA metagenomics analyses. Gut Pathog 2015; 7:4 [View Article][PubMed]
    [Google Scholar]
  3. Yeoman CJ, Chia N, Jeraldo P, Sipos M, Goldenfeld ND et al. The microbiome of the chicken gastrointestinal tract. Anim Health Res Rev 2012; 13:89–99 [View Article][PubMed]
    [Google Scholar]
  4. Louis P, Flint HJ. Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiol Lett 2009; 294:1–8 [View Article][PubMed]
    [Google Scholar]
  5. Videnska P, Sedlar K, Lukac M, Faldynova M, Gerzova L et al. Succession and replacement of bacterial populations in the caecum of egg laying hens over their whole life. PLoS One 2014; 9:e115142 [View Article][PubMed]
    [Google Scholar]
  6. Onrust L, Ducatelle R, van Driessche K, de Maesschalck C, Vermeulen K et al. Steering endogenous butyrate production in the intestinal tract of broilers as a tool to improve gut health. Front Vet Sci 2015; 2:75 [View Article][PubMed]
    [Google Scholar]
  7. Stanley D, Hughes RJ, Geier MS, Moore RJ. Bacteria within the gastrointestinal tract microbiota correlated with improved growth and feed conversion: challenges presented for the identification of performance enhancing probiotic bacteria. Front Microbiol 2016; 7:187 [View Article][PubMed]
    [Google Scholar]
  8. Witte W. Medical consequences of antibiotic use in agriculture. Science 1998; 279:996–997 [View Article][PubMed]
    [Google Scholar]
  9. Jukes TH, Williams WL. Nutritional effects of antibiotics. Pharmacol Rev 1953; 5:381–420[PubMed]
    [Google Scholar]
  10. Diarra MS, Silversides FG, Diarrassouba F, Pritchard J, Masson L et al. 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 2007; 73:6566–6576 [View Article][PubMed]
    [Google Scholar]
  11. Moore PR, Evenson A, Luckey TD, McCoy E, Elvehjem CA. Use of sulfasuxidine, streptothricin, and streptomycin in nutritional studies with the chick. J Biol Chem 1946; 165:437–441[PubMed]
    [Google Scholar]
  12. Jukes TH, Stokstad ELR, Taylor RR, Cunha TJ, Edwards HM et al. Growth-promoting effect of aureomycin on pigs. Arch Biochem 1950; 26:324–325[PubMed]
    [Google Scholar]
  13. Barton MD. Antibiotic use in animal feed and its impact on human healt. Nutr Res Rev 2000; 13:279–299 [View Article][PubMed]
    [Google Scholar]
  14. Quercia S, Candela M, Giuliani C, Turroni S, Luiselli D et al. From lifetime to evolution: timescales of human gut microbiota adaptation. Front Microbiol 2014; 5:587 [View Article][PubMed]
    [Google Scholar]
  15. MacFarlane S, MacFarlane GT. Regulation of short-chain fatty acid production. Proc Nutr Soc 2003; 62:67–72 [View Article][PubMed]
    [Google Scholar]
  16. Boyen F, Haesebrouck F, Vanparys A, Volf J, Mahu M et al. Coated fatty acids alter virulence properties of Salmonella Typhimurium and decrease intestinal colonization of pigs. Vet Microbiol 2008; 132:319–327 [View Article][PubMed]
    [Google Scholar]
  17. Barnes EM, Mead GC, Barnum DA, Harry EG. 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 1972; 13:311–326 [View Article][PubMed]
    [Google Scholar]
  18. Salanitro JP, Fairchilds IG, Zgornicki YD. Isolation, culture characteristics, and identification of anaerobic bacteria from the chicken cecum. Appl Microbiol 1974; 27:678–687[PubMed]
    [Google Scholar]
  19. Butaye P, Devriese LA, Haesebrouck F. Antimicrobial growth promoters used in animal feed: effects of less well known antibiotics on gram-positive bacteria. Clin Microbiol Rev 2003; 16:175–188 [View Article][PubMed]
    [Google Scholar]
  20. Apajalahti J, Kettunen A, Graham H. Characteristics of the gastrointestinal microbial communities, with special reference to the chicken. Worlds Poult Sci J 2004; 60:223–232 [View Article]
    [Google Scholar]
  21. Zhou W, Wang Y, Lin J. Functional cloning and characterization of antibiotic resistance genes from the chicken gut microbiome. Appl Environ Microbiol 2012; 78:3028–3032 [View Article][PubMed]
    [Google Scholar]
  22. Marshall BM, Ochieng DJ, Levy SB. Commensals: underappreciated reservoir of antibiotic resistance. Microbe Magazine 2009; 4:231–238 [View Article]
    [Google Scholar]
  23. Wei S, Morrison M, Yu Z. Bacterial census of poultry intestinal microbiome. Poult Sci 2013; 92:671–683 [View Article][PubMed]
    [Google Scholar]
  24. Ismail Y, Mahendran V, Octavia S, Day AS, Riordan SM et al. Investigation of the enteric pathogenic potential of oral Campylobacter concisus strains isolated from patients with inflammatory bowel disease. PLoS One 2012; 7:e38217 [View Article][PubMed]
    [Google Scholar]
  25. Mandal S, van Treuren W, White RA, Eggesbø M, Knight R et al. Analysis of composition of microbiomes: a novel method for studying microbial composition. Microb Ecol Health Dis 2015; 26:27663 [View Article][PubMed]
    [Google Scholar]
  26. Kohl KD, Skopec MM, Dearing MD. Captivity results in disparate loss of gut microbial diversity in closely related hosts. Conserv Physiol 2014; 2:cou009 [View Article][PubMed]
    [Google Scholar]
  27. Mancabelli L, Ferrario C, Milani C, Mangifesta M, Turroni F et al. Insights into the biodiversity of the gut microbiota of broiler chickens. Environ Microbiol 2016; 18:4727–4738 [View Article][PubMed]
    [Google Scholar]
  28. Baker GC, Smith JJ, Cowan DA. Review and re-analysis of domain-specific 16S primers. J Microbiol Methods 2003; 55:541–555 [View Article][PubMed]
    [Google Scholar]
  29. Salipante SJ, Sengupta DJ, Rosenthal C, Costa G, Spangler J et al. Rapid 16S rRNA next-generation sequencing of polymicrobial clinical samples for diagnosis of complex bacterial infections. PLoS One 2013; 8:e65226 [View Article][PubMed]
    [Google Scholar]
  30. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010; 7:335–336 [View Article][PubMed]
    [Google Scholar]
  31. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010; 26:2460–2461 [View Article][PubMed]
    [Google Scholar]
  32. Andrews S. 2010; FastQC A quality control tool for high throughput sequence data. Available online at http://www.bioinformatics.babraham.ac.uk/projects/fastqc/
  33. Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 2013; 10:996–998 [View Article][PubMed]
    [Google Scholar]
  34. Desantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 2006; 72:5069–5072 [View Article][PubMed]
    [Google Scholar]
  35. Caporaso JG, Bittinger K, Bushman FD, Desantis TZ, Andersen GL et al. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 2010; 26:266–267 [View Article][PubMed]
    [Google Scholar]
  36. Lozupone C, Knight R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 2005; 71:8228–8235 [View Article][PubMed]
    [Google Scholar]
  37. Langille MG, Zaneveld J, Caporaso JG, Mcdonald D, Knights D et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 2013; 31:814–821 [View Article][PubMed]
    [Google Scholar]
  38. Parks DH, Tyson GW, Hugenholtz P, Beiko RG. STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 2014; 30:3123–3124 [View Article][PubMed]
    [Google Scholar]
  39. Miquel S, Martín R, Bridonneau C, Robert V, Sokol H et al. Ecology and metabolism of the beneficial intestinal commensal bacterium Faecalibacterium prausnitzii. Gut Microbes 2014; 5:146–151 [View Article][PubMed]
    [Google Scholar]
  40. Stanley D, Denman SE, Hughes RJ, Geier MS, Crowley TM et al. Intestinal microbiota associated with differential feed conversion efficiency in chickens. Appl Microbiol Biotechnol 2012; 96:1361–1369 [View Article][PubMed]
    [Google Scholar]
  41. Aminov RI. A brief history of the antibiotic era: lessons learned and challenges for the future. Front Microbiol 2010; 1:134 [View Article][PubMed]
    [Google Scholar]
  42. Kilonzo-Nthenge A, Nahashon SN, Chen F, Adefope N. Prevalence and antimicrobial resistance of pathogenic bacteria in chicken and guinea fowl. Poult Sci 2008; 87:1841–1848 [View Article][PubMed]
    [Google Scholar]
  43. Sekelja M, Rud I, Knutsen SH, Denstadli V, Westereng B et al. Abrupt temporal fluctuations in the chicken fecal microbiota are explained by its gastrointestinal origin. Appl Environ Microbiol 2012; 78:2941–2948 [View Article][PubMed]
    [Google Scholar]
  44. Yildirim S, Yeoman CJ, Sipos M, Torralba M, Wilson BA et al. Characterization of the fecal microbiome from non-human wild primates reveals species specific microbial communities. PLoS One 2010; 5:e13963 [View Article][PubMed]
    [Google Scholar]
  45. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature 2006; 444:1022–1023 [View Article][PubMed]
    [Google Scholar]
  46. Handl S, Dowd SE, Garcia-Mazcorro JF, Steiner JM, Suchodolski JS. Massive parallel 16S rRNA gene pyrosequencing reveals highly diverse fecal bacterial and fungal communities in healthy dogs and cats. FEMS Microbiol Ecol 2011; 76:301–310 [View Article][PubMed]
    [Google Scholar]
  47. 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 [View Article][PubMed]
    [Google Scholar]
  48. Huys G, Vanhoutte T, Joossens M, Mahious AS, de Brandt E et al. Coamplification of eukaryotic DNA with 16S rRNA gene-based PCR primers: possible consequences for population fingerprinting of complex microbial communities. Curr Microbiol 2008; 56:553–557 [View Article][PubMed]
    [Google Scholar]
  49. Rivas R, Velázquez E, Zurdo-Piñeiro JL, Mateos PF, Martínez Molina E. Identification of microorganisms by PCR amplification and sequencing of a universal amplified ribosomal region present in both prokaryotes and eukaryotes. J Microbiol Methods 2004; 56:413–426 [View Article][PubMed]
    [Google Scholar]
  50. Milani C, Hevia A, Foroni E, Duranti S, Turroni F et al. Assessing the fecal microbiota: an optimized ion torrent 16S rRNA gene-based analysis protocol. PLoS One 2013; 8:e68739 [View Article][PubMed]
    [Google Scholar]
  51. Wu GD, Lewis JD, Hoffmann C, Chen YY, Knight R et al. Sampling and pyrosequencing methods for characterizing bacterial communities in the human gut using 16S sequence tags. BMC Microbiol 2010; 10:206 [View Article][PubMed]
    [Google Scholar]
  52. Abdallah Ismail N, Ragab SH, Abd Elbaky A, Shoeib AR, Alhosary Y et al. Frequency of Firmicutes and Bacteroidetes in gut microbiota in obese and normal weight Egyptian children and adults. Arch Med Sci 2011; 7:501–507 [View Article][PubMed]
    [Google Scholar]
  53. Pérez-Cobas AE, Gosalbes MJ, Friedrichs A, Knecht H, Artacho A et al. Gut microbiota disturbance during antibiotic therapy: a multi-omic approach. Gut 2013; 62:1591–1601 [View Article][PubMed]
    [Google Scholar]
  54. Sergeant MJ, Constantinidou C, Cogan TA, Bedford MR, Penn CW et al. Extensive microbial and functional diversity within the chicken cecal microbiome. PLoS One 2014; 9:e91941 [View Article][PubMed]
    [Google Scholar]
  55. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A et al. A core gut microbiome in obese and lean twins. Nature 2009; 457:480–484 [View Article][PubMed]
    [Google Scholar]
  56. Cotta MA, Whitehead TR, Zeltwanger RL. Isolation, characterization and comparison of bacteria from swine faeces and manure storage pits. Environ Microbiol 2003; 5:737–745 [View Article][PubMed]
    [Google Scholar]
  57. Creevey CJ, Kelly WJ, Henderson G, Leahy SC. Determining the culturability of the rumen bacterial microbiome. Microb Biotechnol 2014; 7:467–479 [View Article][PubMed]
    [Google Scholar]
  58. Kim BS, Kim JN, Cerniglia CE. In vitro culture conditions for maintaining a complex population of human gastrointestinal tract microbiota. J Biomed Biotechnol 2011; 2011:1–10 [View Article][PubMed]
    [Google Scholar]
  59. Vital M, Gao J, Rizzo M, Harrison T, Tiedje JM. Diet is a major factor governing the fecal butyrate-producing community structure across Mammalia, Aves and Reptilia. Isme J 2015; 9:832–843 [View Article][PubMed]
    [Google Scholar]
  60. Kameyama K, Itoh K. Intestinal colonization by a Lachnospiraceae bacterium contributes to the development of diabetes in obese mice. Microbes Environ 2014; 29:427–430 [View Article][PubMed]
    [Google Scholar]
  61. 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 [View Article]
    [Google Scholar]
  62. Rinttila T, Apajalahti J. Intestinal microbiota and metabolites–Implications for broiler chicken health and performance1. J Appl Poult Res 2013; 22:647–658 [View Article]
    [Google Scholar]
  63. Peris-Bondia F, Latorre A, Artacho A, Moya A, D'Auria G. The active human gut microbiota differs from the total microbiota. PLoS One 2011; 6:e22448 [View Article][PubMed]
    [Google Scholar]
  64. Zhu XY, Zhong T, Pandya Y, Joerger RD. 16S rRNA-based analysis of microbiota from the cecum of broiler chickens. Appl Environ Microbiol 2002; 68:124–137 [View Article][PubMed]
    [Google Scholar]
  65. Koropatkin NM, Cameron EA, Martens EC. How glycan metabolism shapes the human gut microbiota. Nat Rev Microbiol 2012; 10:323–335 [View Article][PubMed]
    [Google Scholar]
  66. Koh A, de Vadder F, Kovatcheva-Datchary P, Bäckhed F. From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell 2016; 165:1332–1345 [View Article][PubMed]
    [Google Scholar]
  67. Foditsch C, Santos TM, Teixeira AG, Pereira RV, Dias JM et al. Isolation and characterization of Faecalibacterium prausnitzii from calves and piglets. PLoS One 2014; 9:e116465 [View Article][PubMed]
    [Google Scholar]
  68. Fåk F, Bäckhed F. Lactobacillus reuteri prevents diet-induced obesity, but not atherosclerosis, in a strain dependent fashion in Apoe-/- mice. PLoS One 2012; 7:e46837 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000597
Loading
/content/journal/micro/10.1099/mic.0.000597
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error