Microbial Ecology

, Volume 56, Issue 2, pp 322–331

Comparison of the Cecal Microbiota of Domestic and Wild Turkeys

  • Alexandra J Scupham
  • Toni G. Patton
  • Elizabeth Bent
  • Darrell O. Bayles
Original Article

Abstract

The extent to which production methods alter intestinal microbial communities of livestock is currently unknown. As the intestinal microbiota may affect animal health, nutrition, and food safety, a baseline comparison of the cecal communities of domestic and wild turkeys was performed. Oligonucleotide fingerprinting of ribosomal RNA (rRNA) genes (OFRG) of 2,990 16S rRNA clones and dot blot quantification of dominant populations were used to identify the dominant bacterial taxa. Seventy-three percent of all the clones belonged to as yet uncultured genera. However, at a higher phylogenetic level, the OFRG library was composed of 54% Bacteroidetes clones (52% of the domestic library clones, 56% of the wild library clones), 30% Firmicutes clones (33% of the domestic library clones, 32% of the wild library clones), 3% Proteobacteria clones (5% domestic, 2% wild), and 3% Deferribacteres clones (4% domestic, 1% wild). Seven percent of the clones were unidentifiable (6% domestic, 9% wild). Bacteroidetes clones included the genera Alistipes, Prevotella, Megamonas, and Bacteroides. Of the Clostridiales clones, groups IV, IX, and XIV including genera Faecalibacterium, Megasphaera, Phascolarctobacterium, and Papillibacter were predominant. Lactobacillus, Enterococcus, and Streptococcus bacilli were also identified. β- δ- and γ-proteobacterial genera included Acinetobacter, Sutterella, and Escherichia. Deferribacteres clones showed high similarity to Mucispirillum schaedleri. Statistical comparison of the domestic and wild turkey clone libraries indicated similar levels of community richness and evenness despite the fact that the two libraries shared only 30% of the total clone operational taxonomic units. Together these results indicate that although high level taxonomic community structure is similar, high-density turkey production causes considerable divergence of the genera found in the ceca of commercial birds from those of their wild counterparts.

Supplementary material

248_2007_9349_MOESM1_ESM.doc (19 kb)
ESMDendrogram of the 2407 domestic and wild turkey clones and 39 control clones. The dendrogram was created using greedy clique partitioning of the oligonucleotide fingerprinting of rRNA genes (OFRG) fingerprints for each clone. Taxonomy for the labeled clones was determined by sequence analysis of the clone and RDP II classification of the sequence. Clone taxa appended with an asterisk (*) indicate taxonomy was determined by comparison of the fingerprint to theoretical fingerprints generated from GenBank sequence data (DOC 19 kb)

References

  1. 1.
    Amann R, Ludwig W (2000) Ribosomal RNA-targeted nucleic acid probes for studies in microbial ecology. FEMS Microbiol Rev 24:555–565PubMedCrossRefGoogle Scholar
  2. 2.
    Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA (1990) Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56:1919–1925PubMedGoogle Scholar
  3. 3.
    Amann RI, Krumholz L, Stahl DA (1990) Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J Bacteriol 172:762–770PubMedGoogle Scholar
  4. 4.
    Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ, Weightman AJ (2005) At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies. Appl Environ Microbiol 71:7724–7736PubMedCrossRefGoogle Scholar
  5. 5.
    Barnes EM (1979) The intestinal microflora of poultry and game birds during life and after storage. Address of the president of the Society for Applied Bacteriology delivered at a meeting of the society on 10 January 1979. J Appl Bacteriol 46:407–419PubMedGoogle Scholar
  6. 6.
    Barnes EM, Impey CS, Stevens BJ (1979) Factors affecting the incidence and anti-salmonella activity of the anaerobic caecal flora of the young chick. J Hyg (Lond) 82:263–283Google Scholar
  7. 7.
    Benno Y, Endo K, Suzuki K, Mitsuoka T, Namioka S (1985) Use of nonprotein nitrogen in pigs: effects of dietary urea on the intestinal microflora. Am J Vet Res 46:959–962PubMedGoogle Scholar
  8. 8.
    Bent E, Yin B, Figueroa A, Ye X, Fu Q, Liu Z, Chrobak M, Jeske D, Jiang T, Borneman J (2006) Development of a 9,6000 clone array for oligonucleotide fingerprinting of rRNA genes: utilization to compare four different soil DNA extraction methods. J Microbiol Methods 67:171–180PubMedCrossRefGoogle Scholar
  9. 9.
    Bielke LR, Elwood AL, Donoghue DJ, Donoghue AM, Newberry LA, Neighbor NK, Hargis BM (2003) Approach for selection of individual enteric bacteria for competitive exclusion in turkey poults. Poult Sci 82:1378–1382PubMedGoogle Scholar
  10. 10.
    Boom R, Sol CJ, Salimans MM, Jansen CL, Wertheim-van Dillen PM, van der Noordaa J (1990) Rapid and simple method for purification of nucleic acids. J Clin Microbiol 28:495–503PubMedGoogle Scholar
  11. 11.
    Borneman J, Chrobak M, Della Vedova G, Figueroa A, Jiang T (2001) Probe selection algorithms with applications in the analysis of microbial communities. Bioinformatics 17 Suppl 1:S39–S48PubMedGoogle Scholar
  12. 12.
    Coates JD, Cole KA, Michaelidou U, Patrick J, McInerney MJ, Achenbach LA (2005) Biological control of hog waste odor through stimulated microbial Fe(III) reduction. Appl Environ Microbiol 71:4728–4735PubMedCrossRefGoogle Scholar
  13. 13.
    Cole JR, Chai B, Farris RJ, Wang Q, Kulam SA, McGarrell DM, Garrity GM, Tiedje JM (2005) The Ribosomal Database Project (RDP-II): sequences and tools for high-throughput rRNA analysis. Nucleic Acids Res 33:D294–D296PubMedCrossRefGoogle Scholar
  14. 14.
    Collins MD, Lawson PA, Willems A, Cordoba JJ, Fernandez-Garayzabal J, Garcia P, Cai J, Hippe H, Farrow JA (1994) The phylogeny of the genus Clostridium: proposal of five new genera and eleven new species combinations. Int J Syst Bacteriol 44:812–826PubMedCrossRefGoogle Scholar
  15. 15.
    Dore J, Sghir A, Hannequart-Gramet G, Corthier G, Pochart P (1998) Design and evaluation of a 16S rRNA-targeted oligonucleotide probe for specific detection and quantitation of human faecal Bacteroides populations. Syst Appl Microbiol 21:65–71PubMedGoogle Scholar
  16. 16.
    Duncan SH, Hold GL, Harmsen HJ, Stewart CS, Flint HJ (2002) Growth requirements and fermentation products of Fusobacterium prausnitzii, and a proposal to reclassify it as Faecalibacterium prausnitzii gen. nov., comb. nov. Int J Syst Evol Microbiol 52:2141–2146PubMedCrossRefGoogle Scholar
  17. 17.
    Engberg J, On SL, Harrington CS, Gerner-Smidt P (2000) Prevalence of Campylobacter, Arcobacter, Helicobacter, and Sutterella spp. in human fecal samples as estimated by a reevaluation of isolation methods for Campylobacters. J Clin Microbiol 38:286–291PubMedGoogle Scholar
  18. 18.
    Franks AH, Harmsen HJ, Raangs GC, Jansen GJ, Schut F, Welling GW (1998) Variations of bacterial populations in human feces measured by fluorescent in situ hybridization with group-specific 16S rRNA-targeted oligonucleotide probes. Appl Environ Microbiol 64:3336–3345PubMedGoogle Scholar
  19. 19.
    Gophna U, Sommerfeld K, Gophna S, Doolittle WF, Veldhuyzen van Zanten SJ (2006) Differences between tissue-associated intestinal microfloras of patients with Crohn’s disease and ulcerative colitis. J Clin Microbiol 44:4136–4141PubMedCrossRefGoogle Scholar
  20. 20.
    Hanssen I (1979) A comparison of the microbiological conditions in the small intestine and caeca of wild and captive willow grouse (Lagopus lagopus lagopus). Acta Vet Scand 20:365–371PubMedGoogle Scholar
  21. 21.
    Hooper LV, Wong MH, Thelin A, Hansson L, Falk PG, Gordon JI (2001) Molecular analysis of commensal host-microbial relationships in the intestine. Science 291:881–884PubMedCrossRefGoogle Scholar
  22. 22.
    Hughes JB, Bohannan BJM (2004) Application of ecological diversity statistics in microbial ecology. In: Kowalchuk GA, de Bruijn FJ, Head IM, Akkermans ADL, van Elsasz JD (eds) Molecular microbial ecology manual, vol. 2, 2nd ed. Kluwer Academic Press, The Netherlands, pp 1321–1344Google Scholar
  23. 23.
    Hume ME, Kubena LF, Edrington TS, Donskey CJ, Moore RW, Ricke SC, Nisbet DJ (2003) Poultry digestive microflora biodiversity as indicated by denaturing gradient gel electrophoresis. Poult Sci 82:1100–1107PubMedGoogle Scholar
  24. 24.
    Hutter G, Schlagenhauf U, Valenza G, Horn M, Burgemeister S, Claus H, Vogel U (2003) Molecular analysis of bacteria in periodontitis: evaluation of clone libraries, novel phylotypes and putative pathogens. Microbiology 149:67–75PubMedCrossRefGoogle Scholar
  25. 25.
    Jampachaisri K, Valinsky L, Borneman J, Press SJ (2005) Classification of oligonucleotide fingerprints: application for microbial community and gene expression analyses. Bioinformatics 21:3122–3130PubMedCrossRefGoogle Scholar
  26. 26.
    Jernberg C, Lofmark S, Edlund C, Jansson JK (2007) Long-term ecological impacts of antibiotic administration on the human intestinal microbiota. The International Society for Microbial Ecology Journal 1:56–66Google Scholar
  27. 27.
    Jousimies-Somer H (1997) Recently described clinically important anaerobic bacteria: taxonomic aspects and update. Clin Infect Dis 25 Suppl 2:S78–S87PubMedGoogle Scholar
  28. 28.
    Krause DO, Smith WJ, Conlan LL, Gough JM, Williamson MA, McSweeney CS (2003) Diet influences the ecology of lactic acid bacteria and Escherichia coli along the digestive tract of cattle: neural networks and 16S rDNA. Microbiol 149:57–65CrossRefGoogle Scholar
  29. 29.
    Lane DJ (1991) 16S/23S rRNA Sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175Google Scholar
  30. 30.
    Lu J, Idris U, Harmon B, Hofacre C, Maurer JJ, Lee MD (2003) Diversity and succession of the intestinal bacterial community of the maturing broiler chicken. Appl Environ Microbiol 69:6816–6824PubMedCrossRefGoogle Scholar
  31. 31.
    Miroshnichenko ML, Bonch-Osmolovskaya EA (2006) Recent developments in the thermophilic microbiology of deep-sea hydrothermal vents. Extremophiles 10:85–96PubMedCrossRefGoogle Scholar
  32. 32.
    Morotomi M, Nagai F, Sakon H (2007) Taxonomic note: genus Megamonas should be placed in the lineage of Firmicutes; Clostridia; Clostridiales; Acidaminococcaceae; Megamonas. Int J Syst Evol Microbiol 57:1673–1674PubMedCrossRefGoogle Scholar
  33. 33.
    Nurmi E, Rantala M (1973) New aspects of Salmonella infection in broiler production. Nature 241:210–211PubMedCrossRefGoogle Scholar
  34. 34.
    Pace NR, Stahl D, Lane DJ, Olsen GJ (1986) The analysis of natural microbial populations by ribosomal RNA sequences. Adv Microb Ecol 9:51–55Google Scholar
  35. 35.
    Raskin L, Stromley JM, Rittmann BE, Stahl DA (1994) Group-specific 16S rRNA hybridization probes to describe natural communities of methanogens. Appl Environ Microbiol 60:1232–1240PubMedGoogle Scholar
  36. 36.
    Robertson BR, O’Rourke JL, Neilan BA, Vandamme P, On SL, Fox JG, Lee A (2005) Mucispirillum schaedleri gen. nov., sp. nov., a spiral-shaped bacterium colonizing the mucus layer of the gastrointestinal tract of laboratory rodents. Int J Syst Evol Microbiol 55:1199–1204PubMedCrossRefGoogle Scholar
  37. 37.
    Salanitro JP, Blake IG, Muirhead PA (1974) Studies on the cecal microflora of commercial broiler chickens. Appl Microbiol 28:439–447PubMedGoogle Scholar
  38. 38.
    Schales K, Gerlach H, Kosters J (1993) Investigations on the aerobic flora and Clostridium perfringens in fecal specimens from free-living and captive capercaillies (Tetrao urogallus L., 1758). Zentralbl Veterinarmed B 40:469–477PubMedGoogle Scholar
  39. 39.
    Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1506PubMedCrossRefGoogle Scholar
  40. 40.
    Schloss PD, Handelsman J (2006) Introducing SONS, a tool for operational taxonomic unit-based comparisons of microbial community memberships and structures. Appl Environ Microbiol 72:6773–6779PubMedCrossRefGoogle Scholar
  41. 41.
    Scupham AJ (2007) Succession in the intestinal microbiota of preadolescent turkeys. FEMS Microbiol Ecol 60:136–147PubMedCrossRefGoogle Scholar
  42. 42.
    Sghir A, Gramet G, Suau A, Rochet V, Pochart P, Dore J (2000) Quantification of bacterial groups within human fecal flora by oligonucleotide probe hybridization. Appl Environ Microbiol 66:2263–2266PubMedCrossRefGoogle Scholar
  43. 43.
    Souza MR, Moreira JL, Barbosa FH, Cerqueira MM, Nunes AC, Nicoli JR (2007) Influence of intensive and extensive breeding on lactic acid bacteria isolated from Gallus gallus domesticus ceca. Vet Microbiol 120:142–150PubMedCrossRefGoogle Scholar
  44. 44.
    Stern NJ, Svetoch EA, Eruslanov BV, Perelygin VV, Mitsevich EV, Mitsevich IP, Pokhilenko VD, Levchuk VP, Svetoch OE, Seal BS (2006) Isolation of a Lactobacillus salivarius strain and purification of its bacteriocin, which is inhibitory to Campylobacter jejuni in the chicken gastrointestinal system. Antimicrob Agents Chemother 50:3111–3116PubMedCrossRefGoogle Scholar
  45. 45.
    Suau A, Rochet V, Sghir A, Gramet G, Brewaeys S, Sutren M, Rigottier-Gois L, Dore J (2001) Fusobacterium prausnitzii and related species represent a dominant group within the human fecal flora. Syst Appl Microbiol 24:139–145PubMedCrossRefGoogle Scholar
  46. 46.
    Valinsky L, Scupham AJ, Della Vedova J, Liu Z, Figuerosa A, Jampachaisri K, Yin B, Press J, Jiang T, Borneman J (2004) Oligonucleotide Fingerprinting of Ribosomal RNA Genes (OFRG). In Kowalchuk GA, de Bruijn FJ, Head IM, Akkermans ADL, van Elsas JD (eds) Molecular microbial ecology methods, vol. 1, 2nd ed. Kluwer Academic Press, The Netherlands, pp 569–585Google Scholar
  47. 47.
    Walker AW, Duncan SH, McWilliam Leitch EC, Child MW, Flint HJ (2005) pH and peptide supply can radically alter bacterial populations and short-chain fatty acid ratios within microbial communities from the human colon. Appl Environ Microbiol 71:3692–3700PubMedCrossRefGoogle Scholar
  48. 48.
    Wong JM, de Souza R, Kendall CW, Emam A, Jenkins DJ (2006) Colonic health: fermentation and short chain fatty acids. J Clin Gastroenterol 40:235–243PubMedCrossRefGoogle Scholar
  49. 49.
    Woodmansey EJ (2007) Intestinal bacteria and ageing. J Appl Microbiol 102:1178–1186PubMedCrossRefGoogle Scholar
  50. 50.
    Yue JC, Clayton MK (2005) A similarity measure based on species proportions. Commun Stat 34:2123–2131CrossRefGoogle Scholar
  51. 51.
    Yue JC, Clayton MK, Lin FC (2001) A nonparametric estimator of species overlap. Biometrics 57:743–749PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Alexandra J Scupham
    • 1
  • Toni G. Patton
    • 1
  • Elizabeth Bent
    • 2
  • Darrell O. Bayles
    • 3
  1. 1.Pre-Harvest Food Safety and Enteric Diseases Research Unit, National Animal Disease Center, Agricultural Research ServiceUS Department of AgricultureAmesUSA
  2. 2.Department of Plant PathologyUniversity of CaliforniaRiversideUSA
  3. 3.Bacterial Diseases of Livestock Research Unit, National Animal Disease Center, Agricultural Research ServiceUS Department of AgricultureAmesUSA

Personalised recommendations