In commercial poultry production, there is a lack of natural flora providers since chickens are hatched in the clean environment of a hatchery. Events occurring soon after hatching are therefore of particular importance, and that is why we were interested in the development of the gut microbial community, the immune response to natural microbial colonization, and the response to Salmonella enterica serovar Enteritidis infection as a function of chicken age. The complexity of chicken gut microbiota gradually increased from day 1 to day 19 of life and consisted of Proteobacteria and Firmicutes. For the first 3 days of life, chicken cecum was protected by increased expression of chicken β-defensins (i.e., gallinacins 1, 2, 4, and 6), expression of which dropped from day 4 of life. On the other hand, a transient increase in interleukin-8 (IL-8) and IL-17 expression could be observed in chicken cecum on day 4 of life, indicating physiological inflammation and maturation of the gut immune system. In agreement, the response of chickens infected with S. Enteritidis on days 1, 4, and 16 of life shifted from Th1 (characterized mainly by induction of gamma interferon [IFN-γ] and inducible nitric oxide synthase [iNOS]), observed in younger chickens, to Th17, observed in 16-day-old chickens (characterized mainly by IL-17 induction). Active modification of chicken gut microbiota in the future may accelerate or potentiate the maturation of the gut immune system and increase its resistance to infection with different pathogens.

Veterinary Research Institute Hudcova 70 621 00 Brno Czech Republic

Zobrazit více v PubMed

Amit-Romach E., Sklan D., Uni Z. 2004. Microflora ecology of the chicken intestine using 16S ribosomal DNA primers. Poult. Sci. 83:1093–1098 PubMed

Bar-Shira E., Friedman A. 2006. Development and adaptations of innate immunity in the gastrointestinal tract of the newly hatched chick. Dev. Comp. Immunol. 30:930–941 PubMed

Bar-Shira E., Sklan D., Friedman A. 2003. Establishment of immune competence in the avian GALT during the immediate post-hatch period. Dev. Comp. Immunol. 27:147–157 PubMed

Berndt A., et al. 2007. Chicken cecum immune response to Salmonella enterica serovars of different levels of invasiveness. Infect. Immun. 75:5993–6007 PubMed PMC

Curtis M. M., Way S. S. 2009. Interleukin-17 in host defence against bacterial, mycobacterial and fungal pathogens. Immunology 126:177–185 PubMed PMC

De Boever S., Vangestel C., De Backer P., Croubels S., Sys S. U. 2008. Identification and validation of housekeeping genes as internal control for gene expression in an intravenous LPS inflammation model in chickens. Vet. Immunol. Immunopathol. 122:312–317 PubMed

Eyerich S., Eyerich K., Cavani A., Schmidt-Weber C. 2010. IL-17 and IL-22: siblings, not twins. Trends Immunol. 31:354–361 PubMed

Eyerich S., et al. 2009. Th22 cells represent a distinct human T cell subset involved in epidermal immunity and remodeling. J. Clin. Invest. 119:3573–3585 PubMed PMC

Gaboriau-Routhiau V., et al. 2009. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity 31:677–689 PubMed

Godinez I., et al. 2008. T cells help to amplify inflammatory responses induced by Salmonella enterica serotype Typhimurium in the intestinal mucosa. Infect. Immun. 76:2008–2017 PubMed PMC

Holt P. S., Gast R. K., Porter R. E., Jr., Stone H. D. 1999. Hyporesponsiveness of the systemic and mucosal humoral immune systems in chickens infected with Salmonella enterica serovar enteritidis at one day of age. Poult. Sci. 78:1510–1517 PubMed

Ivanov I. I., et al. 2008. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 4:337–349 PubMed PMC

Li Y. P., Bang D. D., Handberg K. J., Jorgensen P. H., Zhang M. F. 2005. Evaluation of the suitability of six host genes as internal control in real-time RT-PCR assays in chicken embryo cell cultures infected with infectious bursal disease virus. Vet. Microbiol. 110:155–165 PubMed

Liang S. C., et al. 2006. Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J. Exp. Med. 203:2271–2279 PubMed PMC

Lillehoj H. S., Chung K. S. 1992. Postnatal development of T-lymphocyte subpopulations in the intestinal intraepithelium and lamina propria in chickens. Vet. Immunol. Immunopathol. 31:347–360 PubMed

Lowenthal J. W., Connick T. E., McWaters P. G., York J. J. 1994. Development of T cell immune responsiveness in the chicken. Immunol. Cell Biol. 72:115–122 PubMed

Lu J., et al. 2003. Diversity and succession of the intestinal bacterial community of the maturing broiler chicken. Appl. Environ. Microbiol. 69:6816–6824 PubMed PMC

Methner U., Barrow P. A., Berndt A., Steinbach G. 1999. Combination of vaccination and competitive exclusion to prevent Salmonella colonization in chickens: experimental studies. Int. J. Food Microbiol. 49:35–42 PubMed

Methner U., Barrow P. A., Gregorova D., Rychlik I. 2004. Intestinal colonisation-inhibition and virulence of Salmonella phoP, rpoS and ompC deletion mutants in chickens. Vet. Microbiol. 98:37–43 PubMed

Methner U., Barrow P. A., Martin G., Meyer H. 1997. Comparative study of the protective effect against Salmonella colonisation in newly hatched SPF chickens using live, attenuated Salmonella vaccine strains, wild-type Salmonella strains or a competitive exclusion product. Int. J. Food Microbiol. 35:223–230 PubMed

Mwangi W. N., et al. 2010. Regional and global changes in TCRalphabeta T cell repertoires in the gut are dependent upon the complexity of the enteric microflora. Dev. Comp. Immunol. 34:406–417 PubMed

Neish A. S., Denning T. L. 2010. Advances in understanding the interaction between the gut microbiota and adaptive mucosal immune responses. F1000 Biol. Rep. 2:27 doi: 10.3410/B2-27 PubMed DOI PMC

Nograles K. E., et al. 2008. Th17 cytokines interleukin (IL)-17 and IL-22 modulate distinct inflammatory and keratinocyte-response pathways. Br. J. Dermatol. 159:1092–1102 PubMed PMC

Qu A., et al. 2008. Comparative metagenomics reveals host specific metavirulomes and horizontal gene transfer elements in the chicken cecum microbiome. PLoS One 3:e2945. PubMed PMC

Raffatellu M., et al. 2009. Lipocalin-2 resistance confers an advantage to Salmonella enterica serotype Typhimurium for growth and survival in the inflamed intestine. Cell Host Microbe 5:476–486 PubMed PMC

Rychlik I., et al. 2009. Virulence potential of five major pathogenicity islands (SPI-1 to SPI-5) of Salmonella enterica serovar Enteritidis for chickens. BMC Microbiol. 9:268. PubMed PMC

Schulz S. M., et al. 2008. Protective immunity to systemic infection with attenuated Salmonella enterica serovar enteritidis in the absence of IL-12 is associated with IL-23-dependent IL-22, but not IL-17. J. Immunol. 181:7891–7901 PubMed

Sokol H., et al. 2008. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc. Natl. Acad. Sci. U. S. A. 105:16731–16736 PubMed PMC

Thompson C. L., Wang B., Holmes A. J. 2008. The immediate environment during postnatal development has long-term impact on gut community structure in pigs. ISME J. 2:739–748 PubMed

Van Immerseel F., et al. 2002. Dynamics of immune cell infiltration in the caecal lamina propria of chickens after neonatal infection with a Salmonella enteritidis strain. Dev. Comp. Immunol. 26:355–364 PubMed

Withanage G. S., et al. 2004. Rapid expression of chemokines and proinflammatory cytokines in newly hatched chickens infected with Salmonella enterica serovar Typhimurium. Infect. Immun. 72:2152–2159 PubMed PMC

Wolk K., et al. 2004. IL-22 increases the innate immunity of tissues. Immunity 21:241–254 PubMed

Zhu X. Y., Zhong T., Pandya Y., Joerger R. D. 2002. 16S rRNA-based analysis of microbiota from the cecum of broiler chickens. Appl. Environ. Microbiol. 68:124–137 PubMed PMC

Colonization of chickens with competitive exclusion products results in extensive differences in metabolite composition in cecal digesta

Research Note: A mixture of Bacteroides spp. and other probiotic intestinal anaerobes reduces colonization by pathogenic E. coli strain O78:H4-ST117 in newly hatched chickens

Interleukin 4 inducible 1 gene (IL4I1) is induced in chicken phagocytes by Salmonella Enteritidis infection

Gene expression in the chicken caecum is dependent on microbiota composition

Transient and Prolonged Response of Chicken Cecum Mucosa to Colonization with Different Gut Microbiota

Composition of Gut Microbiota Influences Resistance of Newly Hatched Chickens to Salmonella Enteritidis Infection

Gene Expression Profiles of Chicken Embryo Fibroblasts in Response to Salmonella Enteritidis Infection

Gene expression in the chicken caecum in response to infections with non-typhoid Salmonella

Influence of Salmonella enterica serovar Enteritidis infection on the composition of chicken cecal microbiota

Chicken innate immune response to oral infection with Salmonella enterica serovar Enteritidis

Chicken faecal microbiota and disturbances induced by single or repeated therapy with tetracycline and streptomycin

Influence of Salmonella enterica serovar enteritidis infection on the development of the cecum microbiota in newly hatched chicks

Characterization of chicken spleen transcriptome after infection with Salmonella enterica serovar Enteritidis

Cytokine signaling in splenic leukocytes from vaccinated and non-vaccinated chickens after intravenous infection with Salmonella enteritidis