Characterization of the cecal microbiome composition of Wenchang chickens before and after fattening

Autoři: Zhen Tan aff001;  Lilong Luo aff001;  Xiaozhe Wang aff001;  Qiong Wen aff001;  Lu Zhou aff001;  Kebang Wu aff001
Působiště autorů: Laboratory of Tropical Animal Breeding, Reproduction and Nutrition, College of Animal Science and Technology, Institute of Tropical Agriculture and Forestry, Hainan University, Haikou, P.R. China aff001
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article


The cecum of poultry harbors a complex and dynamic microbial community which plays important roles in preventing pathogen colonization, detoxifying harmful substances, nutrient processing, and harvesting of the ingestion. Understanding and optimizing microbial communities could help improve agricultural productivity. In this study, we analyzed the composition and function of cecal microbiota of Wenchang chicken (a native breed of Bantam) before and after fattening, using high throughput sequencing technology. High-throughput sequencing of the 16S rRNA genes V3-V4 hypervariable regions was used to characterize and compare the cecal microbiota of Wenchang chicken before fattening (free-range in hill) and after fattening (cage raising). Sixteen phyla were shared by the 20 samples. Firmicutes and Bacteroidetes were the top two abundant phyla being 80% of the total microbiota. Samples of chickens prior to fattening were more dispersed than those after fattening. Twenty four microbes could be considered as biomarkers and 3 phyla revealed differences by variance analysis which could distinguish the two groups. Cecal microbiota in the before fattening group had higher abundance of functions involved in digestive system and biosynthesis of other secondary metabolites. The composition and function of cecal microbiota in Wenchang chicken before and after fattening under the two feeding modes, free range in hillside and cage raising, were found to be different. These results can be attributed to the differences in feeding modes and growth stages. In-depth study on the functions and interactions of intestinal microbiota can help us in developing strategies for raising Wenchang chickens and provide valuable information for the study of microbiota in the chicken gut.

Klíčová slova:

Carbohydrate metabolism – Cecum – Fats – Gastrointestinal tract – Gut bacteria – Chickens – Livestock – Microbiome


1. Park SJ, Kim J, Lee JS, Rhee SK, Kim H. Characterization of the fecal microbiome in different swine groups by high-throughput sequencing. Anaerobe. 2014;28:157–62. doi: 10.1016/j.anaerobe.2014.06.002 24954845.

2. DuPont HL. The growing threat of foodborne bacterial enteropathogens of animal origin. Clinical infectious diseases: an official publication of the Infectious Diseases Society of America. 2007;45(10):1353–61. doi: 10.1086/522662 17968835.

3. Yeoman CJ, Chia N, Jeraldo P, Sipos M, Goldenfeld ND, White BA. The microbiome of the chicken gastrointestinal tract. Animal health research reviews. 2012;13(1):89–99. doi: 10.1017/S1466252312000138 22853945.

4. Borda-Molina D, Seifert J, Camarinha-Silva A. Current Perspectives of the Chicken Gastrointestinal Tract and Its Microbiome. Computational and structural biotechnology journal. 2018;16:131–9. doi: 10.1016/j.csbj.2018.03.002 30026889; PubMed Central PMCID: PMC6047366.

5. Ocejo M, Oporto B, Hurtado A. 16S rRNA amplicon sequencing characterization of caecal microbiome composition of broilers and free-range slow-growing chickens throughout their productive lifespan. Sci Rep. 2019;9(1):2506. doi: 10.1038/s41598-019-39323-x 30792439; PubMed Central PMCID: PMC6385345.

6. Svihus B, Choct M, Classen HL. Function and nutritional roles of the avian caeca: a review. World Poultry Sci J. 2013;69(2):249–63. doi: 10.1017/S0043933913000287 WOS:000321059500002.

7. 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(7122):1027–31. doi: 10.1038/nature05414 17183312.

8. Videnska P, Sedlar K, Lukac M, Faldynova M, Gerzova L, Cejkova D, et al. Succession and Replacement of Bacterial Populations in the Caecum of Egg Laying Hens over Their Whole Life. Plos One. 2014;9(12). ARTN e115142 doi: 10.1371/journal.pone.0115142 WOS:000346375400075. 25501990

9. Kubasova T, Kollarcikova M, Crhanova M, Karasova D, Cejkova D, Sebkova A, et al. Contact with adult hen affects development of caecal microbiota in newly hatched chicks. Plos One. 2019;14(3). ARTN e0212446 doi: 10.1371/journal.pone.0212446 WOS:000460372100034. 30840648

10. 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(3). ARTN e91941 doi: 10.1371/journal.pone.0091941 WOS:000333355300046. 24657972

11. Stanley D, Geier MS, Chen H, Hughes RJ, Moore RJ. Comparison of fecal and cecal microbiotas reveals qualitative similarities but quantitative differences. Bmc Microbiol. 2015;15. ARTN 51 doi: 10.1186/s12866-015-0388-6 WOS:000353191500001. 25887695

12. Ahir VB, Koringa PG, Bhatt VD, Ramani UV, Tripathi AK, Singh KM, et al. Metagenomic analysis of poultry gut microbes. Indian Journal of Poultry Science. 2010;45(2):111–4.

13. Stanley D, Geier MS, Denman SE, Haring VR, Crowley TM, Hughes RJ, et al. Identification of chicken intestinal microbiota correlated with the efficiency of energy extraction from feed. Vet Microbiol. 2013;164(1–2):85–92. doi: 10.1016/j.vetmic.2013.01.030 23434185.

14. Wen C, Yan W, Sun C, Ji C, Zhou Q, Zhang D, et al. The gut microbiota is largely independent of host genetics in regulating fat deposition in chickens. The ISME Journal. 2019. doi: 10.1038/s41396-019-0367-2 30728470

15. Fanatico AC, Pillai PB, Emmert JL, Owens CM. Meat quality of slow- and fast-growing chicken genotypes fed low-nutrient or standard diets and raised indoors or with outdoor access. Poult Sci. 2007;86(10):2245–55. doi: 10.1093/ps/86.10.2245 17878457

16. Xu Y, Yang H, Zhang L, Su Y, Shi D, Xiao H, et al. High-throughput sequencing technology to reveal the composition and function of cecal microbiota in Dagu chicken. Bmc Microbiol. 2016;16(1):259. doi: 10.1186/s12866-016-0877-2 27814685; PubMed Central PMCID: PMC5097418.

17. Magoc T, Salzberg SL. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics. 2011;27(21):2957–63. doi: 10.1093/bioinformatics/btr507 21903629; PubMed Central PMCID: PMC3198573.

18. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114–20. doi: 10.1093/bioinformatics/btu170 24695404; PubMed Central PMCID: PMC4103590.

19. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011;27(16):2194–200. doi: 10.1093/bioinformatics/btr381 21700674; PubMed Central PMCID: PMC3150044.

20. Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature methods. 2013;10(10):996–8. doi: 10.1038/nmeth.2604 23955772.

21. Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, et al. Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nature methods. 2013;10(1):57–9. doi: 10.1038/nmeth.2276 23202435; PubMed Central PMCID: PMC3531572.

22. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic acids research. 2013;41(Database issue):D590–6. doi: 10.1093/nar/gks1219 23193283; PubMed Central PMCID: PMC3531112.

23. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and environmental microbiology. 2009;75(23):7537–41. doi: 10.1128/AEM.01541-09 19801464; PubMed Central PMCID: PMC2786419.

24. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nature methods. 2010;7(5):335–6. doi: 10.1038/nmeth.f.303 20383131; PubMed Central PMCID: PMC3156573.

25. Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R. UniFrac: an effective distance metric for microbial community comparison. Isme J. 2011;5(2):169–72. doi: 10.1038/ismej.2010.133 20827291; PubMed Central PMCID: PMC3105689.

26. Looft T, Johnson TA, Allen HK, Bayles DO, Alt DP, Stedtfeld RD, et al. In-feed antibiotic effects on the swine intestinal microbiome. P Natl Acad Sci USA. 2012;109(5):1691–6. doi: 10.1073/pnas.1120238109 WOS:000299731400069. 22307632

27. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, et al. Metagenomic biomarker discovery and explanation. Genome biology. 2011;12(6):R60. doi: 10.1186/gb-2011-12-6-r60 21702898; PubMed Central PMCID: PMC3218848.

28. Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol. 2013;31(9):814–+. doi: 10.1038/nbt.2676 WOS:000324306300021. 23975157

29. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505(7484):559–63. doi: 10.1038/nature12820 24336217; PubMed Central PMCID: PMC3957428.

30. Zhao L, Wang G, Siegel P, He C, Wang H, Zhao W, et al. Quantitative genetic background of the host influences gut microbiomes in chickens. Sci Rep. 2013;3:1163. doi: 10.1038/srep01163 23362462; PubMed Central PMCID: PMC3557447.

31. Everard A, Lazarevic V, Gaia N, Johansson M, Stahlman M, Backhed F, et al. Microbiome of prebiotic-treated mice reveals novel targets involved in host response during obesity. Isme J. 2014;8(10):2116–30. doi: 10.1038/ismej.2014.45 24694712; PubMed Central PMCID: PMC4163056.

32. Sun J, Wang Y, Li N, Zhong H, Xu H, Zhu Q, et al. Comparative Analysis of the Gut Microbial Composition and Meat Flavor of Two Chicken Breeds in Different Rearing Patterns. BioMed research international. 2018;2018:4343196. doi: 10.1155/2018/4343196 30410932; PubMed Central PMCID: PMC6206517.

33. Pandit RJ, Hinsu AT, Patel NV, Koringa PG, Jakhesara SJ, Thakkar JR, et al. Microbial diversity and community composition of caecal microbiota in commercial and indigenous Indian chickens determined using 16s rDNA amplicon sequencing. Microbiome. 2018;6. Artn 115 doi: 10.1186/S40168-018-0501-9 WOS:000435955700001. 29935540

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;18(12):4727–38. doi: 10.1111/1462-2920.13363 WOS:000392946900033. 27129897

35. Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, et al. Evolution of mammals and their gut microbes. Science. 2008;320(5883):1647–51. doi: 10.1126/science.1155725 18497261; PubMed Central PMCID: PMC2649005.

36. 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. 2016;82(5):1569–76. doi: 10.1128/Aem.03473-15 WOS:000373338800021. 26712550

37. Zhao W, Wang Y, Liu S, Huang J, Zhai Z, He C, et al. The dynamic distribution of porcine microbiota across different ages and gastrointestinal tract segments. Plos One. 2015;10(2):e0117441. doi: 10.1371/journal.pone.0117441 25688558; PubMed Central PMCID: PMC4331431.

38. Wang KH, Shi SR, Dou TC, Sun HJ. Effect of a free-range raising system on growth performance, carcass yield, and meat quality of slow-growing chicken. Poultry Sci. 2009;88(10):2219–23. doi: 10.3382/ps.2008-00423 WOS:000271291700029. 19762879

39. Muriel D, M Carmen C, Kaouther BA, Seppo S, Vos WM, De. The Mucin degrader Akkermansia muciniphila is an abundant resident of the human intestinal tract. Applied and environmental microbiology. 2008;74(5):1646–8. doi: 10.1128/AEM.01226-07 18083887

40. Kostic AD, Chun E, Robertson L, Glickman JN, Gallini CA, Michaud M, et al. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell host & microbe. 2013;14(2):207–15. doi: 10.1016/j.chom.2013.07.007 23954159; PubMed Central PMCID: PMC3772512.

41. Chen X, Jiang W, Tan HZ, Xu GF, Zhang XB, Wei S, et al. Effects of outdoor access on growth performance, carcass composition, and meat characteristics of broiler chickens. Poult Sci. 2013;92(2):435–43. doi: 10.3382/ps.2012-02360 23300311.

42. Zhang T, Xie J, Zhang M, Fu N, Zhang Y. Effect of a potential probiotics Lactococcus garvieae B301 on the growth performance, immune parameters and caecum microflora of broiler chickens. Journal of animal physiology and animal nutrition. 2016;100(3):413–21. doi: 10.1111/jpn.12388 WOS:000379976600002. 26331590

Článek vyšel v časopise


2019 Číslo 12
Nejčtenější tento týden