{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,9]],"date-time":"2026-01-09T21:04:12Z","timestamp":1767992652079,"version":"3.49.0"},"reference-count":43,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2023,12,5]],"date-time":"2023-12-05T00:00:00Z","timestamp":1701734400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Rural Development Administration, Republic of Korea, and the 2023 the RDA Fellowship Program of Rural Development Administration, Republic of Korea","award":["PJ01569302"],"award-info":[{"award-number":["PJ01569302"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Life"],"abstract":"<jats:p>The gastrointestinal tract microbiome is essential for regulating nutrient absorption, gut immune function, and host growth and development. In the present study, we characterized the development of ileum and cecum microbiota in pullets throughout the rearing period, encompassing a period from the day of hatching to 18 weeks of age. The growth performance and intestinal microbiome (ileum and cecum) of pullets were analyzed at 1, 5, 11, and 18 weeks of age. The richness of the ileum and cecum bacterial communities (alpha diversity) was higher in pullets at 18 weeks of age than in those at 1 and 5 weeks of age. Microbiota from weeks 1, 5, 11, and 18 were distinctly grouped in a NMDS plot, representing beta diversity within the ileum. However, the results for cecum microbiota did not reveal evident separation among the different age groups in the weighted UniFrac. In conclusion, our findings demonstrate variations and diversification in ileum and cecum microbiota across different rearing stages in pullets. These insights have the potential to inform the development of nutritional strategies that promote gut health and contribute to the improved development of pullets.<\/jats:p>","DOI":"10.3390\/life13122302","type":"journal-article","created":{"date-parts":[[2023,12,5]],"date-time":"2023-12-05T08:09:17Z","timestamp":1701763757000},"page":"2302","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Microbiome Changes in Layer Pullets Reared in Floor Pens along the Growth Period"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-6959-9790","authenticated-orcid":false,"given":"Hee-Jin","family":"Kim","sequence":"first","affiliation":[{"name":"Poultry Research Institute, National Institute of Animal Science, Rural Development Administration, Pyeongchang 25342, Republic of Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hyun-Soo","family":"Kim","sequence":"additional","affiliation":[{"name":"Poultry Research Institute, National Institute of Animal Science, Rural Development Administration, Pyeongchang 25342, Republic of Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yeon-Seo","family":"Yun","sequence":"additional","affiliation":[{"name":"Poultry Research Institute, National Institute of Animal Science, Rural Development Administration, Pyeongchang 25342, Republic of Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hyekyoung","family":"Shin","sequence":"additional","affiliation":[{"name":"Poultry Research Institute, National Institute of Animal Science, Rural Development Administration, Pyeongchang 25342, Republic of Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Woo-Do","family":"Lee","sequence":"additional","affiliation":[{"name":"Poultry Research Institute, National Institute of Animal Science, Rural Development Administration, Pyeongchang 25342, Republic of Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jiseon","family":"Son","sequence":"additional","affiliation":[{"name":"Poultry Research Institute, National Institute of Animal Science, Rural Development Administration, Pyeongchang 25342, Republic of Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1982-2023","authenticated-orcid":false,"given":"Eui-Chul","family":"Hong","sequence":"additional","affiliation":[{"name":"Poultry Research Institute, National Institute of Animal Science, Rural Development Administration, Pyeongchang 25342, Republic of Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ik-Soo","family":"Jeon","sequence":"additional","affiliation":[{"name":"Poultry Research Institute, National Institute of Animal Science, Rural Development Administration, Pyeongchang 25342, Republic of Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hwan-Ku","family":"Kang","sequence":"additional","affiliation":[{"name":"Poultry Research Institute, National Institute of Animal Science, Rural Development Administration, Pyeongchang 25342, Republic of Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2023,12,5]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"893","DOI":"10.1071\/AN20396","article-title":"Nutrition, feeding and laying hen welfare","volume":"61","author":"Bryden","year":"2021","journal-title":"Anim. Prod. Sci."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"841","DOI":"10.1016\/j.aninu.2020.11.019","article-title":"Age-associated changes in caecal microbiome and their apparent correlations with growth performances of layer pullets","volume":"7","author":"Liu","year":"2021","journal-title":"Anim. Nutr."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"631","DOI":"10.1007\/s00018-012-1070-x","article-title":"Regulation of intestinal epithelial permeability by tight junctions","volume":"70","author":"Suzuki","year":"2013","journal-title":"Cell. Mol. Life Sci."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"254","DOI":"10.3389\/fvets.2018.00254","article-title":"Chicken gut microbiota: Importance and detection technology","volume":"5","author":"Shang","year":"2018","journal-title":"Front. Vet. Sci."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"873","DOI":"10.3923\/javaa.2012.873.877","article-title":"Impact and manipulation of gut microflora in poultry: A review","volume":"11","author":"Adil","year":"2012","journal-title":"J. Anim. Vet. Adv."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"220","DOI":"10.1038\/nature11550","article-title":"Diversity, stability and resilience of the human gut microbiota","volume":"489","author":"Lozupone","year":"2012","journal-title":"Nature"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"308","DOI":"10.1080\/03079457.2016.1152625","article-title":"Microbial shifts associated with necrotic enteritis","volume":"45","author":"Antonissen","year":"2016","journal-title":"Avian Pathol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1017\/S1466252312000138","article-title":"The microbiome of the chicken gastrointestinal tract","volume":"13","author":"Yeoman","year":"2012","journal-title":"Anim. Health Res. Rev."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Videnska, P., Sedlar, K., Lukac, M., Faldynova, M., Gerzova, L., Cejkova, D., Sisak, F., and Rychlik, I. (2014). Succession and replacement of bacterial populations in the caecum of egg laying hens over their whole life. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0115142"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"122","DOI":"10.1016\/j.virol.2020.10.011","article-title":"Gut microbiota is associated with protection against Marek\u2019s disease virus infection in chickens","volume":"553","author":"Bavananthasivam","year":"2021","journal-title":"Virology"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Waite, D.W., and Taylor, M.W. (2014). Characterizing the avian gut microbiota: Membership, driving influences, and potential function. Front. Microbiol., 5.","DOI":"10.3389\/fmicb.2014.00223"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Diaz Carrasco, J.M., Casanova, N.A., and Fern\u00e1ndez Miyakawa, M.E. (2019). Microbiota, gut health and chicken productivity: What is the connection?. Microorganisms, 7.","DOI":"10.3390\/microorganisms7100374"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"108","DOI":"10.4161\/gmic.26945","article-title":"Intestinal microbiome of poultry and its interaction with host and diet","volume":"5","author":"Pan","year":"2014","journal-title":"Gut Microbes"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1016\/j.csbj.2018.03.002","article-title":"Current perspectives of the chicken gastrointestinal tract and its microbiome","volume":"16","author":"Seifert","year":"2018","journal-title":"Comput. Struct. Biotechnol. J."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"811","DOI":"10.1038\/nature06245","article-title":"An ecological and evolutionary perspective on human\u2013microbe mutualism and disease","volume":"449","author":"Dethlefsen","year":"2017","journal-title":"Nature"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1099","DOI":"10.1007\/s00484-015-1103-x","article-title":"Dietary supplementation of a mixture of Lactobacillus strains enhances performance of broiler chickens raised under heat stress conditions","volume":"60","author":"Shokryazdan","year":"2016","journal-title":"Int. J. Biometeorol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1016\/J.ENG.2017.01.008","article-title":"The human microbiota in health and disease","volume":"3","author":"Wang","year":"2017","journal-title":"Engineering"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"45308","DOI":"10.1038\/srep45308","article-title":"Gut metagenomic analysis reveals prominent roles of Lactobacillus and cecal microbiota in chicken feed efficiency","volume":"7","author":"Yan","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/gb-2011-12-6-r60","article-title":"Metagenomic biomarker discovery and explanation","volume":"12","author":"Segata","year":"2011","journal-title":"Genome. Biol."},{"key":"ref_20","first-page":"79","article-title":"Development of the normal gastrointestinal microflora of specific pathogen-free chickens","volume":"92","author":"Coloe","year":"1984","journal-title":"Epidemiol. Infect."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"6816","DOI":"10.1128\/AEM.69.11.6816-6824.2003","article-title":"Diversity and succession of the intestinal bacterial community of the maturing broiler chicken","volume":"69","author":"Lu","year":"2003","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1100","DOI":"10.1093\/ps\/82.7.1100","article-title":"Poultry digestive microflora biodiversity as indicated by denaturing gradient gel electrophoresis","volume":"82","author":"Hume","year":"2003","journal-title":"Poult. Sci."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"e03137-18","DOI":"10.1128\/AEM.03137-18","article-title":"Farm stage, bird age, and body site dominantly affect the quantity, taxonomic composition, and dynamics of respiratory and gut microbiota of com-mercial layer chickens","volume":"85","author":"Ngunjiri","year":"2019","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1007\/s00248-002-2015-y","article-title":"Spatial and temporal variation of the intestinal bacterial community in commercially raised broiler chickens during growth","volume":"44","author":"Keuzenkamp","year":"2002","journal-title":"Microb. Ecol."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Li, X., Wu, S., Li, X., Yan, T., Duan, Y., Yang, X., Duan, Y., Sun, Q., and Yang, X. (2018). Simultaneous supplementation of Bacillus subtilis and antibiotic growth promoters by stages improved intestinal function of pullets by altering gut microbiota. Front. Microbiol., 9.","DOI":"10.3389\/fmicb.2018.02328"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"2","DOI":"10.3389\/fvets.2016.00002","article-title":"Development of the chick microbiome: How early exposure influences future microbial diversity","volume":"3","author":"Ballou","year":"2016","journal-title":"Front. Vet. Sci."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Dai, D., Wu, S.G., Zhang, H.J., Qi, G.H., and Wang, J. (2020). Dynamic alterations in early intestinal development, microbiota and metabolome induced by in ovo feeding of L-arginine in a layer chick model. J. Anim. Sci. Biotechnol., 11.","DOI":"10.1186\/s40104-020-0427-5"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1163","DOI":"10.1038\/srep01163","article-title":"Quantitative genetic background of the host influences gut microbiomes in chickens","volume":"3","author":"Zhao","year":"2013","journal-title":"Sci. Rep."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Nordentoft, S., M\u00f8lbak, L., Bjerrum, L., De Vylder, J., Van Immerseel, F., and Pedersen, K. (2011). The influence of the cage system and colonisation of Salmonella Enteritidis on the microbial gut flora of laying hens studied by T-RFLP and 454 py-rosequencing. BMC Microb., 11.","DOI":"10.1186\/1471-2180-11-187"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"e00402-19","DOI":"10.1128\/AEM.00402-19","article-title":"Bacillus subtilis strain DSM 29784 modulates the cecal microbiome, concentration of short-chain fatty acids, and apparent retention of dietary components in shaver white chickens during grower, developer, and laying phases","volume":"85","author":"Neijat","year":"2019","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1619","DOI":"10.3945\/jn.109.104638","article-title":"Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers","volume":"139","author":"Peng","year":"2009","journal-title":"J. Nutr."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"3018","DOI":"10.1172\/JCI128521","article-title":"The gut-bone axis: How bacterial metabolites bridge the distance","volume":"129","author":"Zaiss","year":"2019","journal-title":"J. Clin. Investig."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"10595","DOI":"10.1007\/s11033-012-1947-7","article-title":"High through put 16S rRNA gene-based pyrosequencing analysis of the fecal microbiota of high FCR and low FCR broiler growers","volume":"39","author":"Singh","year":"2012","journal-title":"Mol. Biol. Rep."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1120","DOI":"10.3945\/jn.111.140988","article-title":"Bacteroides uniformis is a putative bacterial species associated with the degradation of the isoflavone genistein in human feces","volume":"141","author":"Renouf","year":"2011","journal-title":"J. Nutr."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Gauffin Cano, P., Santacruz, A., Moya, \u00c1., and Sanz, Y. (2012). Bacteroides uniformis CECT 7771 ameliorates metabolic and immunological dysfunction in mice with high-fat-diet induced obesity. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0041079"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1569","DOI":"10.1128\/AEM.03473-15","article-title":"Important metabolic pathways and biological processes expressed by chicken cecal microbiota","volume":"82","author":"Polansky","year":"2016","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"16714","DOI":"10.1038\/s41598-022-20736-0","article-title":"Gut microbiota shift in layer pullets fed on black soldier fly larvae-based feeds towards enhancing healthy gut microbial community","volume":"12","author":"Ndotono","year":"2022","journal-title":"Sci. Rep."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"639","DOI":"10.1007\/s00203-009-0492-9","article-title":"Inhibition of uropathogens by lactic acid bacteria isolated from dairy foods and cow\u2019s intestine in western Nigeria","volume":"191","author":"Ayeni","year":"2009","journal-title":"Arch. Microbiol."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Vieco-Saiz, N., Belguesmia, Y., Raspoet, R., Auclair, E., Gancel, F., Kempf, I., and Drider, D. (2019). Benefits and inputs from lactic acid bacteria and their bacteriocins as alternatives to antibiotic growth promoters during food-animal production. Front. Microbiol., 10.","DOI":"10.3389\/fmicb.2019.00057"},{"key":"ref_40","unstructured":"Chege, S.M. (2016). The Rasputin Effect: When Commensals and Symbionts Become Parasitic, Springer."},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Xiao, S., Mi, J., Chen, Y., Feng, K., Mei, L., Liao, X., Liao, X., Wu, Y., and Wang, Y. (2023). The abundance and diversity of antibiotic resistance genes in layer chicken ceca is associated with farm enviroment. Front. Microbiol., 14.","DOI":"10.3389\/fmicb.2023.1177404"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1016\/j.aninu.2023.07.006","article-title":"The temporal fluctuations and development of faecal microbiota in commercial layer flocks","volume":"15","author":"Joat","year":"2023","journal-title":"Anim. Nutr."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"101330","DOI":"10.1016\/j.psj.2021.101330","article-title":"Centennial Review: Recent developments in host-pathogen interactions during necrotic enteritis in poultry","volume":"100","author":"Emami","year":"2021","journal-title":"Poult. Sci."}],"container-title":["Life"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2075-1729\/13\/12\/2302\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T21:33:33Z","timestamp":1760132013000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2075-1729\/13\/12\/2302"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,12,5]]},"references-count":43,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2023,12]]}},"alternative-id":["life13122302"],"URL":"https:\/\/doi.org\/10.3390\/life13122302","relation":{},"ISSN":["2075-1729"],"issn-type":[{"value":"2075-1729","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,12,5]]}}}