Influence of the Gut Microbiota Composition on Campylobacter jejuni Colonization in Chickens
Jazyk angličtina Země Spojené státy americké Médium electronic-print
Typ dokumentu časopisecké články
PubMed
28808158
PubMed Central
PMC5649013
DOI
10.1128/iai.00380-17
PII: IAI.00380-17
Knihovny.cz E-zdroje
- Klíčová slova
- Campylobacter jejuni, gut microbiota, immune response,
- MeSH
- antibakteriální látky farmakologie MeSH
- B-lymfocyty imunologie mikrobiologie MeSH
- bursa Fabricii účinky léků imunologie mikrobiologie MeSH
- Campylobacter jejuni účinky léků imunologie patogenita MeSH
- cékum účinky léků imunologie mikrobiologie MeSH
- gnotobiologické modely imunologie MeSH
- ileum účinky léků imunologie mikrobiologie MeSH
- interakce hostitele a patogenu imunologie MeSH
- játra účinky léků imunologie mikrobiologie MeSH
- kampylobakterové infekce imunologie mikrobiologie veterinární MeSH
- kur domácí MeSH
- mikrobiální interakce imunologie MeSH
- nemoci drůbeže imunologie mikrobiologie MeSH
- počet mikrobiálních kolonií MeSH
- slezina účinky léků imunologie mikrobiologie MeSH
- střevní mikroflóra imunologie MeSH
- T-lymfocyty imunologie mikrobiologie MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- antibakteriální látky MeSH
The Campylobacter jejuni-host interaction may be affected by the host's gut microbiota through competitive exclusion, metabolites, or modification of the immune response. To understand this interaction, C. jejuni colonization and local immune responses were compared in chickens with different gut microbiota compositions. Birds were treated with an antibiotic cocktail (AT) (experiments 1 and 2) or raised under germfree (GF) conditions (experiment 3). At 18 days posthatch (dph), they were orally inoculated either with 104 CFU of C. jejuni or with diluent. Cecal as well as systemic C. jejuni colonization, T- and B-cell numbers in the gut, and gut-associated tissue were compared between the different groups. Significantly higher numbers of CFU of C. jejuni were detected in the cecal contents of AT and GF birds, with higher colonization rates in spleen, liver, and ileum, than in birds with a conventional gut microbiota (P < 0.05). Significant upregulation of T and B lymphocyte numbers was detected in cecum, cecal tonsils, and bursa of Fabricius of AT or GF birds after C. jejuni inoculation compared to the respective controls (P < 0.05). This difference was less clear in birds with a conventional gut microbiota. Histopathological gut lesions were observed only in C. jejuni-inoculated AT and GF birds but not in microbiota-colonized C. jejuni-inoculated hatchmates. These results demonstrate that the gut microbiota may contribute to the control of C. jejuni colonization and prevent lesion development. Further studies are needed to identify key players of the gut microbiota and the mechanisms behind their protective role.
INRA UMR1282 Infectiologie et Santé Publique Nouzilly France
University of Veterinary Medicine Hannover Clinic for Poultry Hannover Germany
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Frost JA. 2001. Current epidemiological issues in human campylobacteriosis. Symp Ser Soc Appl Microbiol 2001(30):85S–95S. PubMed
Bronzwaer S, Hugas M, Collins JD, Newell DG, Robinson T, Makela P, Havelaar A. 2009. EFSA's 12th Scientific Colloquium—assessing health benefits of controlling Campylobacter in the food chain. Int J Food Microbiol 131:284–285. doi:10.1016/j.ijfoodmicro.2009.01.033. PubMed DOI
Hermans D, Pasmans F, Heyndrickx M, Van Immerseel F, Martel A, Van Deun K, Haesebrouck F. 2012. A tolerogenic mucosal immune response leads to persistent Campylobacter jejuni colonization in the chicken gut. Crit Rev Microbiol 38:17–29. doi:10.3109/1040841X.2011.615298. PubMed DOI
Blaut M, Clavel T. 2007. Metabolic diversity of the intestinal microbiota: implications for health and disease. J Nutr 137:751S–755S. PubMed
Holmes E, Li JV, Athanasiou T, Ashrafian H, Nicholson JK. 2011. Understanding the role of gut microbiome–host metabolic signal disruption in health and disease. Trends Microbiol 19:349–359. doi:10.1016/j.tim.2011.05.006. PubMed DOI
Lawley TD, Walker AW. 2013. Intestinal colonization resistance. Immunology 138:1–11. doi:10.1111/j.1365-2567.2012.03616.x. PubMed DOI PMC
Bereswill S, Fischer A, Plickert R, Haag LM, Otto B, Kuhl AA, Dasti JI, Zautner AE, Munoz M, Loddenkemper C, Gross U, Gobel UB, Heimesaat MM. 2011. Novel murine infection models provide deep insights into the “menage a trois” of Campylobacter jejuni, microbiota and host innate immunity. PLoS One 6:e20953. doi:10.1371/journal.pone.0020953. PubMed DOI PMC
Smith HW, Tucker JF. 1978. The effect of antimicrobial feed additives on the colonization of the alimentary tract of chickens by Salmonella typhimurium. J Hyg (Lond) 80:217–231. doi:10.1017/S0022172400053560. PubMed DOI PMC
O'Loughlin JL, Samuelson DR, Braundmeier-Fleming AG, White BA, Haldorson GJ, Stone JB, Lessmann JJ, Eucker TP, Konkel ME. 2015. The intestinal microbiota influences Campylobacter jejuni colonization and extraintestinal dissemination in mice. Appl Environ Microbiol 81:4642–4650. doi:10.1128/AEM.00281-15. PubMed DOI PMC
Smith CK, Kaiser P, Rothwell L, Humphrey T, Barrow PA, Jones MA. 2005. Campylobacter jejuni-induced cytokine responses in avian cells. Infect Immun 73:2094–2100. doi:10.1128/IAI.73.4.2094-2100.2005. PubMed DOI PMC
Jennings JL, Sait LC, Perrett CA, Foster C, Williams LK, Humphrey TJ, Cogan TA. 2011. Campylobacter jejuni is associated with, but not sufficient to cause vibrionic hepatitis in chickens. Vet Microbiol 149:193–199. doi:10.1016/j.vetmic.2010.11.005. PubMed DOI
Pielsticker C, Glünder G, Rautenschlein S. 2016. Colonization pattern of C. jejuni isolates of human and avian origin and differences in the induction of immune responses in chicken. Vet Immunol Immunopathol 169:1–9. doi:10.1016/j.vetimm.2015.11.005. PubMed DOI
Shaughnessy RG, Meade KG, Cahalane S, Allan B, Reiman C, Callanan JJ, O'Farrelly C. 2009. Innate immune gene expression differentiates the early avian intestinal response between Salmonella and Campylobacter. Vet Immunol Immunopathol 132:191–198. doi:10.1016/j.vetimm.2009.06.007. PubMed DOI
Han Z, Willer T, Pielsticker C, Gerzova L, Rychlik I, Rautenschlein S. 2016. Differences in host breed and diet influence colonization by Campylobacter jejuni and induction of local immune responses in chicken. Gut Pathog 8:56. doi:10.1186/s13099-016-0133-1. PubMed DOI PMC
Humphrey S, Chaloner G, Kemmett K, Davidson N, Williams N, Kipar A, Humphrey T, Wigley P. 2014. Campylobacter jejuni is not merely a commensal in commercial broiler chickens and affects bird welfare. mBio 5:e01364-14. doi:10.1128/mBio.01364-14. PubMed DOI PMC
Heimesaat MM, Haag LM, Fischer A, Otto B, Kuhl AA, Gobel UB, Bereswill S. 2013. Survey of extra-intestinal immune responses in asymptomatic long-term Campylobacter jejuni-infected mice. Eur J Microbiol Immunol (Bp) 3:174–182. doi:10.1556/EuJMI.3.2013.3.4. PubMed DOI PMC
Bereswill S, Plickert R, Fischer A, Kuhl AA, Loddenkemper C, Batra A, Siegmund B, Gobel UB, Heimesaat MM. 2011. What you eat is what you get: novel Campylobacter models in the quadrangle relationship between nutrition, obesity, microbiota and susceptibility to infection. Eur J Microbiol Immunol (Bp) 1:237–248. doi:10.1556/EuJMI.1.2011.3.8. PubMed DOI PMC
Diehl GE, Longman RS, Zhang J-X, Breart B, Galan C, Cuesta A, Schwab SR, Littman DR. 2013. Microbiota restricts trafficking of bacteria to mesenteric lymph nodes by CX3CR1hi cells. Nature 494:116–120. doi:10.1038/nature11809. PubMed DOI PMC
Kalliomäki MA, Walker WA. 2005. Physiologic and pathologic interactions of bacteria with gastrointestinal epithelium. Gastroenterol Clin North Am 34:383–399. doi:10.1016/j.gtc.2005.05.007. PubMed DOI
Gantois I, Ducatelle R, Pasmans F, Haesebrouck F, Hautefort I, Thompson A, Hinton J, Van Immerseel F. 2006. Butyrate specifically down-regulates Salmonella pathogenicity island 1 gene expression. Appl Environ Microbiol 72:946–949. doi:10.1128/AEM.72.1.946-949.2006. PubMed DOI PMC
Marteyn B, Scorza FB, Sansonetti PJ, Tang C. 2011. Breathing life into pathogens: the influence of oxygen on bacterial virulence and host responses in the gastrointestinal tract. Cell Microbiol 13:171–176. doi:10.1111/j.1462-5822.2010.01549.x. PubMed DOI
Beery JT, Hugdahl MB, Doyle MP. 1988. Colonization of gastrointestinal tracts of chicks by Campylobacter jejuni. Appl Environ Microbiol 54:2365–2370. PubMed PMC
Dhillon AS, Shivaprasad HL, Schaberg D, Wier F, Weber S, Bandli D. 2006. Campylobacter jejuni infection in broiler chickens. Avian Dis 50:55–58. doi:10.1637/7411-071405R.1. PubMed DOI
Rinttilä T, Apajalahti J. 2013. Intestinal microbiota and metabolites—implications for broiler chicken health and performance. J Appl Poult Res 22:647–658. doi:10.3382/japr.2013-00742. DOI
Kogut MH. 2013. The gut microbiota and host innate immunity: regulators of host metabolism and metabolic diseases in poultry? J Appl Poult Res 22:637–646. doi:10.3382/japr.2013-00741. DOI
Awad WA, Molnar A, Aschenbach JR, Ghareeb K, Khayal B, Hess C, Liebhart D, Dublecz K, Hess M. 2015. Campylobacter infection in chickens modulates the intestinal epithelial barrier function. Innate Immun 21:151–160. doi:10.1177/1753425914521648. PubMed DOI
O'Loughlin JL, Samuelson DR, Braundmeier-Fleming AG, White BA, Haldorson GJ, Stone JB, Lessmann JJ, Eucker TP, Konkel ME. 2015. The intestinal microbiota influences Campylobacter jejuni colonization and extra-intestinal dissemination in mice. Appl Environ Microbiol doi:10.1128/AEM.00281-15. PubMed DOI PMC
Alutis M, Grundmann U, Fischer A, Kühl A, Bereswill S, Heimesaat M. 2014. Selective gelatinase inhibition reduces apoptosis and pro-inflammatory immune cell responses in Campylobacter jejuni-infected gnotobiotic IL-10 deficient mice. Eur J Microbiol Immunol 4:213–222. doi:10.1556/EuJMI-D-14-00031. PubMed DOI PMC
Sahin O, Luo N, Huang S, Zhang Q. 2003. Effect of Campylobacter-specific maternal antibodies on Campylobacter jejuni colonization in young chickens. Appl Environ Microbiol 69:5372–5379. doi:10.1128/AEM.69.9.5372-5379.2003. PubMed DOI PMC
Awad WA, Smorodchenko A, Hess C, Aschenbach JR, Molnar A, Dublecz K, Khayal B, Pohl EE, Hess M. 2015. Increased intracellular calcium level and impaired nutrient absorption are important pathogenicity traits in the chicken intestinal epithelium during Campylobacter jejuni colonization. Appl Microbiol Biotechnol 99:6431–6441. doi:10.1007/s00253-015-6543-z. PubMed DOI
Pelaseyed T, Bergström JH, Gustafsson JK, Ermund A, Birchenough GM, Schütte A, Post S, Svensson F, Rodríguez-Piñeiro AM, Nyström EE. 2014. The mucus and mucins of the goblet cells and enterocytes provide the first defense line of the gastrointestinal tract and interact with the immune system. Immunol Rev 260:8–20. doi:10.1111/imr.12182. PubMed DOI PMC
Cheled-Shoval S, Gamage NW, Amit-Romach E, Forder R, Marshal J, Van Kessel A, Uni Z. 2014. Differences in intestinal mucin dynamics between germ-free and conventionally reared chickens after mannan-oligosaccharide supplementation. Poult Sci 93:636–644. doi:10.3382/ps.2013-03362. PubMed DOI
Alemka A, Whelan S, Gough R, Clyne M, Gallagher ME, Carrington SD, Bourke B. 2010. Purified chicken intestinal mucin attenuates Campylobacter jejuni pathogenicity in vitro. J Med Microbiol 59:898–903. doi:10.1099/jmm.0.019315-0. PubMed DOI
Shortt C, Scanlan E, Hilliard A, Cotroneo CE, Bourke B, Cróinín TÓ. 2016. DNA supercoiling regulates the motility of Campylobacter jejuni and is altered by growth in the presence of chicken mucus. mBio 7:e01227-16. doi:10.1128/mBio.01227-16. PubMed DOI PMC
Smith CK, Abuoun M, Cawthraw SA, Humphrey TJ, Rothwell L, Kaiser P, Barrow PA, Jones MA. 2008. Campylobacter colonization of the chicken induces a proinflammatory response in mucosal tissues. FEMS Immunol Med Microbiol 54:114–121. doi:10.1111/j.1574-695X.2008.00458.x. PubMed DOI
Murphy H, Cogan T, Humphrey T. 2011. Direction of neutrophil movements by Campylobacter-infected intestinal epithelium. Microbes Infect 13:42–48. doi:10.1016/j.micinf.2010.09.007. PubMed DOI
Berndt A, Wilhelm A, Jugert C, Pieper J, Sachse K, Methner U. 2007. Chicken cecum immune response to Salmonella enterica serovars of different levels of invasiveness. Infect Immun 75:5993–6007. doi:10.1128/IAI.00695-07. PubMed DOI PMC
Schwarz A, Gauly M, Abel H, Das G, Humburg J, Rohn K, Breves G, Rautenschlein S. 2011. Immunopathogenesis of Ascaridia galli infection in layer chicken. Dev Comp Immunol 35:774–784. doi:10.1016/j.dci.2011.02.012. PubMed DOI
Higgs R, Cormican P, Cahalane S, Allan B, Lloyd AT, Meade K, James T, Lynn DJ, Babiuk LA, O'Farrelly C. 2006. Induction of a novel chicken Toll-like receptor following Salmonella enterica serovar Typhimurium infection. Infect Immun 74:1692–1698. doi:10.1128/IAI.74.3.1692-1698.2006. PubMed DOI PMC
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. doi:10.1038/nmeth.f.303. PubMed DOI PMC
Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R. 2011. UniFrac: an effective distance metric for microbial community comparison. ISME J 5:169–172. doi:10.1038/ismej.2010.133. PubMed DOI PMC
Schellenberg P, Maillard J. 1973. Techniques d'élevage de volailles axéniques. Journées de Recherches Avicoles et Cunicoles INRA-ITAVI-WPSA, p 283–285. ITAVI, Paris, France.
Barman M, Unold D, Shifley K, Amir E, Hung K, Bos N, Salzman N. 2008. Enteric salmonellosis disrupts the microbial ecology of the murine gastrointestinal tract. Infect Immun 76:907–915. doi:10.1128/IAI.01432-07. PubMed DOI PMC
Gene expression in the chicken caecum is dependent on microbiota composition