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Spatial Microbial Composition Along the Gastrointestinal Tract of Captive Attwater’s Prairie Chicken

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Abstract

Gastrointestinal microbiota is increasingly recognized as an important component of individual health, and therefore, our ability to quantify its diversity accurately is central for exploring different ways to improve health. Non-invasive sampling methods, such as cloaca swabs, are often used to measure gastrointestinal microbiota diversity within an individual. However, few studies have addressed to what degree differences exist in microbial community composition along the gastrointestinal tract, and measures obtained from the cloaca may not actually represent the diversity present elsewhere in the gastrointestinal tract. In this study, we systematically characterized the gastrointestinal microbial community of the critically endangered Attwater’s Prairie chicken (Tympanuchus cupido attwateri) by opportunistically sampling four different locations (ileum, cecum, large intestine, and cloaca) along the gastrointestinal tract of eight individuals. Spatial variation of microbial community was observed at different sampling locations within the gastrointestinal tract. The cecum harbored the most diverse and significantly different microbiota from the other locations, while the microbial α- and β-diversities were similar in the ileum, large intestine, and cloaca. The results of this study provide evidence that microbiota diversity can differ depending on sampling location and metric used to quantify diversity. As shown here, non-invasive cloacal sampling strategies may reflect microbiota diversity elsewhere in the gastrointestinal tract, yet caution is warranted when making generalizations in terms of the microbiota diversity correlations when samples are obtained from a single location within the gastrointestinal tract.

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References

  1. Clemente Jose C, Ursell Luke K, Parfrey Laura W, Knight R (2012) The impact of the gut microbiota on human health: an integrative view. Cell 148:1258–1270. doi:10.1016/j.cell.2012.01.035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Clavel T, Desmarchelier C, Haller D, Gérard P, Rohn S, Lepage P, Daniel H (2014) Intestinal microbiota in metabolic diseases. Gut Microbes 5:544–551. doi:10.4161/gmic.29331

    Article  PubMed  Google Scholar 

  3. Dethlefsen L, McFall-Ngai M, Relman D (2007) An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 449:811–818

    Article  CAS  PubMed  Google Scholar 

  4. Gill SR, Pop M, DeBoy RT, Eckburg PB, Turnbaugh PJ, Samuel BS, Gordon JI, Relman DA, Fraser-Liggett CM, Nelson KE (2006) Metagenomic analysis of the human distal gut microbiome. Science 312:1355–1359. doi:10.1126/science.1124234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Ritchie LE, Steiner JM, Suchodolski JS (2008) Assessment of microbial diversity along the feline intestinal tract using 16S rRNA gene analysis. FEMS Microbiol Ecol 66:590–598. doi:10.1111/j.1574-6941.2008.00609.x

    Article  CAS  PubMed  Google Scholar 

  6. Macpherson A, Harris N (2004) Interactions between commensal intestinal bacteria and the immune system. Nat Rev Immunol 4:478–485

    Article  CAS  PubMed  Google Scholar 

  7. Kurokawa K, Itoh T, Kuwahara T, Oshima K, Toh H, Toyoda A, Takami H, Morita H, Sharma VK, Srivastava TP, Taylor TD, Noguchi H, Mori H, Ogura Y, Ehrlich DS, Itoh K, Takagi T, Sakaki Y, Hayashi T, Hattori M (2007) Comparative metagenomics revealed commonly enriched gene sets in human gut microbiomes. DNA Res 14:169–181. doi:10.1093/dnares/dsm018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. 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 69:6816–6824. doi:10.1128/aem.69.11.6816-6824.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Markle JG, Frank DN, Mortin-Toth S, Robertson CE, Feazel LM, Rolle-Kampczyk U, von Bergen M, McCoy KD, Macpherson AJ, Danska JS (2013) Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science 339:1084–1088

    Article  CAS  PubMed  Google Scholar 

  10. Wang M, Ahrné S, Jeppsson B, Molin G (2005) Comparison of bacterial diversity along the human intestinal tract by direct cloning and sequencing of 16S rRNA genes. FEMS Microbiol Ecol 54:219–231. doi:10.1016/j.femsec.2005.03.012

    Article  CAS  PubMed  Google Scholar 

  11. Yeoman CJ, Chia N, Jeraldo P, Sipos M, Goldenfeld ND, White BA (2012) The microbiome of the chicken gastrointestinal tract. Anim Health Res Rev 13:89–99

    Article  PubMed  Google Scholar 

  12. van der Wielen PWJJ, Keuzenkamp DA, Lipman LJA, van Knapen F, Biesterveld S (2002) Spatial and temporal variation of the intestinal bacterial community in commercially raised broiler chickens during growth. Microb Ecol 44:286–293. doi:10.1007/s00248-002-2015-y

    Article  PubMed  Google Scholar 

  13. Su H, McKelvey J, Rollins D, Zhang M, Brightsmith DJ, Derr J, Zhang S (2014) Cultivable bacterial microbiota of northern bobwhite (Colinus virginianus): a new reservoir of antimicrobial resistance? PLoS One 9:e99826. doi:10.1371/journal.pone.0099826

    Article  PubMed  PubMed Central  Google Scholar 

  14. Pryde SE, Richardson AJ, Stewart CS, Flint HJ (1999) Molecular analysis of the microbial diversity present in the colonic wall, colonic lumen, and cecal lumen of a pig. Appl Environ Microbiol 65:5372–5377

    CAS  PubMed  PubMed Central  Google Scholar 

  15. McLelland J (1989) Anatomy of the avian cecum. J Exp Zool 252:2–9. doi:10.1002/jez.1402520503

    Article  Google Scholar 

  16. Gelis S (2006) Evaluating and treating the gastrointestinal system. Spix Publishing, Inc., Palm Beach

    Google Scholar 

  17. Barnes EM, Mead GC, Barnum DA, Harry EG (1972) 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 13:311–326

    Article  CAS  PubMed  Google Scholar 

  18. Salanitro JP, Fairchilds IG, Zgornicki YD (1974) Isolation, culture characteristics, and identification of anaerobic bacteria from the chicken cecum. Appl Microbiol 27:678–687

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Ruiz-RodrÍGuez M, Lucas FS, Heeb P, Soler JJ (2009) Differences in intestinal microbiota between avian brood parasites and their hosts. Biol J Linn Soc 96:406–414. doi:10.1111/j.1095-8312.2008.01127.x

    Article  Google Scholar 

  20. Ezenwa VO, Gerardo NM, Inouye DW, Medina M, Xavier JB (2012) Animal behavior and the microbiome. Science 338:198–199

    Article  CAS  PubMed  Google Scholar 

  21. Ruiz-Rodríguez M, Soler JJ, Lucas FS, Heeb P, José Palacios M, Martín-Gálvez D, De Neve L, Pérez-Contreras T, Martínez JG, Soler M (2009) Bacterial diversity at the cloaca relates to an immune response in magpie Pica pica and to body condition of great spotted cuckoo Clamator glandarius nestlings. J Avian Biol 40:42–48. doi:10.1111/j.1600-048X.2008.04471.x

    Article  Google Scholar 

  22. van Dongen WF, White J, Brandl H, Moodley Y, Merkling T, Leclaire S, Blanchard P, Danchin E, Hatch S, Wagner R (2013) Age-related differences in the cloacal microbiota of a wild bird species. BMC Ecol 13:11

    Article  PubMed  PubMed Central  Google Scholar 

  23. Leticia Mirón AM, Rocha-Ramírez V, Belda-Ferre P, Cabrera-Rubio R, Folch-Mallol J, Cardénas-Vázquez R, DeLuna A, Lilia Hernández A, Maya-Elizarrarás E, and Schondube JE (2014) Gut bacterial diversity of the house sparrow (Passer domesticus) inferred by 16S rRNA sequence analysis. Metagenomics 3

  24. Morrow ME, Rossignol TA, Silvy NJ (2004) Federal listing of prairie grouse: lessons from the Attwater’s prairie-chicken. Wildl Soc Bull 32:112–118. doi:10.2193/0091-7648(2004)32[112:FLOPGL]2.0.CO;2

    Article  Google Scholar 

  25. Caporaso J, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci 108:4516–4522

    Article  CAS  PubMed  Google Scholar 

  26. 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 (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. doi:10.1128/aem.01541-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. doi:10.1093/bioinformatics/btr381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267. doi:10.1128/aem.00062-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Shannon CE, Weaver W (1949) The mathematical theory of communication. University of Illinois Press, Urbana

    Google Scholar 

  30. Chao A (1984) Nonparametric estimation of the number of classes in a population. Scand J Stat 11:265–270

    Google Scholar 

  31. Chazdon RL, Colwell RK, Denslow JS, Guariguata MR (1998) Statistical methods for estimating species richness of woody regeneration in primary and secondary rain forests of Northeastern Costa Rica. In: Dallmeier F, Comiskey JA (eds) Forest biodiversity research, monitoring and modeling: conceptual background and old world case studies. Parthenon Publishing, Paris, France., pp 285–309

    Google Scholar 

  32. Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235. doi:10.1128/aem.71.12.8228-8235.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143. doi:10.1111/j.1442-9993.1993.tb00438.x

    Article  Google Scholar 

  34. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc Ser B (Stat Method) 57:289–300. doi:10.2307/2346101

    Google Scholar 

  35. Choi JH, Kim GB, Cha CJ (2014) Spatial heterogeneity and stability of bacterial community in the gastrointestinal tracts of broiler chickens. Poult Sci 93:1942–1950. doi:10.3382/ps.2014-03974

    Article  CAS  PubMed  Google Scholar 

  36. Rehman HU, Vahjen W, Awad WA, Zentek J (2007) Indigenous bacteria and bacterial metabolic products in the gastrointestinal tract of broiler chickens. Arch Anim Nutr 61:319–335. doi:10.1080/17450390701556817

    Article  PubMed  Google Scholar 

  37. Dillon RJ, Vennard CT, Buckling A, Charnley AK (2005) Diversity of locust gut bacteria protects against pathogen invasion. Ecol Lett 8:1291–1298. doi:10.1111/j.1461-0248.2005.00828.x

    Article  Google Scholar 

  38. Girvan MS, Campbell CD, Killham K, Prosser JI, Glover LA (2005) Bacterial diversity promotes community stability and functional resilience after perturbation. Environ Microbiol 7:301–313. doi:10.1111/j.1462-2920.2005.00695.x

    Article  CAS  PubMed  Google Scholar 

  39. Ussery H (2011) The small-scale poultry flock: an all-natural approach to raising chickens and other fowl for home and market growers. Chelsea Green Publishing, Chelsea

    Google Scholar 

  40. Stewart R, Rambo TB (2000) Cloacal microbes in house sparrows. Condor 102:679–684. doi:10.1650/0010-5422(2000)102[0679:CMIHS]2.0.CO;2

    Article  Google Scholar 

  41. White J, Mirleau P, Danchin E, Mulard H, Hatch SA, Heeb P, Wagner RH (2010) Sexually transmitted bacteria affect female cloacal assemblages in a wild bird. Ecol Lett 13:1515–1524. doi:10.1111/j.1461-0248.2010.01542.x

    Article  PubMed  PubMed Central  Google Scholar 

  42. van der Hoeven-Hangoor E, van der Vossen JMBM, Schuren FHJ, Verstegen MWA, de Oliveira JE, Montijn RC, Hendriks WH (2013) Ileal microbiota composition of broilers fed various commercial diet compositions. Poult Sci 92:2713–2723. doi:10.3382/ps.2013-03017

    Article  PubMed  Google Scholar 

  43. Ruiz-de-Castañda R, Vela AI, Lobato E, Briones V, Moreno J (2011) Prevalence of potentially pathogenic culturable bacteria on eggshells and in cloacae of female Pied Flycatchers in a temperate habitat in central Spain. J Field Ornithol 82:215–224

    Article  Google Scholar 

  44. Shawkey MD, Firestone MK, Brodie EL, Beissinger SR (2009) Avian incubation inhibits growth and diversification of bacterial assemblages on eggs. PLoS One 4:e4522. doi:10.1371/journal.pone.0004522

    Article  PubMed  PubMed Central  Google Scholar 

  45. Mead GC (1989) Microbes of the avian cecum: types present and substrates utilized. J Exp Zool Suppl 3:48–54

    Article  CAS  PubMed  Google Scholar 

  46. Kohl K (2012) Diversity and function of the avian gut microbiota. J Comp Physiol B 182:591–602. doi:10.1007/s00360-012-0645-z

    Article  PubMed  Google Scholar 

  47. Józefiak D, Rutkowski A, Martin SA (2004) Carbohydrate fermentation in the avian ceca: a review. Anim Feed Sci Technol 113:1–15. doi:10.1016/j.anifeedsci.2003.09.007

    Article  Google Scholar 

  48. Waite DW, Taylor MW (2014) Characterizing the avian gut microbiota: membership, driving influences, and potential function. Front Microbiol 5:223. doi:10.3389/fmicb.2014.00223

    Article  PubMed  PubMed Central  Google Scholar 

  49. Yang J (2012) Influence of dietary fibers and whole grains on fecal microbiota during in vitro fermentation. Thesis, the University of Nebraska

  50. Dethlefsen L, Relman DA (2011) Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc Natl Acad Sci 108:4554–4561. doi:10.1073/pnas.1000087107

    Article  CAS  PubMed  Google Scholar 

  51. Ridlon JM, Kang D-J, Hylemon PB (2006) Bile salt biotransformations by human intestinal bacteria. J Lipid Res 47:241–259. doi:10.1194/jlr.R500013-JLR200

    Article  CAS  PubMed  Google Scholar 

  52. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, Mende DR, Li J, Xu J, Li S, Li D, Cao J, Wang B, Liang H, Zheng H, Xie Y, Tap J, Lepage P, Bertalan M, Batto J-M, Hansen T, Le Paslier D, Linneberg A, Nielsen HB, Pelletier E, Renault P, Sicheritz-Ponten T, Turner K, Zhu H, Yu C, Li S, Jian M, Zhou Y, Li Y, Zhang X, Li S, Qin N, Yang H, Wang J, Brunak S, Dore J, Guarner F, Kristiansen K, Pedersen O, Parkhill J, Weissenbach J, Bork P, Ehrlich SD, Wang J (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59–65. doi:10.1038/nature08821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Kita K, Ken IR, Akamine C, Kawada W, Shimura Y, Inamoto T (2014) Influence of propolis residue on the bacterial flora in the cecum of Nanbu Kashiwa. J Poult Sci 51:275–280. doi:10.2141/jpsa.0130137

    Article  CAS  Google Scholar 

  54. Dewhirst FE, Paster BJ, Tzellas N, Coleman B, Downes J, Spratt DA, Wade WG (2001) Characterization of novel human oral isolates and cloned 16S rDNA sequences that fall in the family Coriobacteriaceae: description of olsenella gen. nov., reclassification of Lactobacillus uli as Olsenella uli comb. nov. and description of Olsenella profusa sp. nov. Int J Syst Evol Microbiol 51:1797–1804. doi:10.1099/00207713-51-5-1797

    Article  CAS  PubMed  Google Scholar 

  55. Apajalahti JHA, Kettunen A, Bedford MR, Holben WE (2001) Percent G+C profiling accurately reveals diet-related differences in the gastrointestinal microbial community of broiler chickens. Appl Environ Microbiol 67:5656–5667. doi:10.1128/aem.67.12.5656-5667.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Oakley BB, Lillehoj HS, Kogut MH, Kim WK, Maurer JJ, Pedroso A, Lee MD, Collett SR, Johnson TJ, Cox NA (2014) The chicken gastrointestinal microbiome. FEMS Microbiol Lett 360:100–112. doi:10.1111/1574-6968.12608

    Article  CAS  PubMed  Google Scholar 

  57. Mizrahi-Man O, Davenport ER, Gilad Y (2013) Taxonomic classification of bacterial 16S rRNA genes using short sequencing reads: evaluation of effective study designs. PLoS One 8:e53608. doi:10.1371/journal.pone.0053608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We thank Susan Hammerly for early discussions concerning the feasibility of this study and Shannon Nodolf, DVM, for conducting the sampling. This work was supported by the National Science Foundation (DEB 0948787) to JAJ and U.S. Fish and Wildlife Service to JAJ.

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Correspondence to Jeff A. Johnson or Michael S. Allen.

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Zhang, Y., Simon, S.E., Johnson, J.A. et al. Spatial Microbial Composition Along the Gastrointestinal Tract of Captive Attwater’s Prairie Chicken. Microb Ecol 73, 966–977 (2017). https://doi.org/10.1007/s00248-016-0870-1

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