The effect of Campylobacter jejuni and Campylobacter coli colonization on the gut morphology, functional integrity, and microbiota composition of female turkeys
Status PubMed-not-MEDLINE Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
AL-2182/2-1
Deutsche Forschungsgemeinschaft
SR-767/8-1
Deutsche Forschungsgemeinschaft
PubMed
35922874
PubMed Central
PMC9347085
DOI
10.1186/s13099-022-00508-x
PII: 10.1186/s13099-022-00508-x
Knihovny.cz E-zdroje
- Klíčová slova
- Campylobacter, Gut health, Microbiota composition, Morphology, Turkey, Ussing chambers,
- Publikační typ
- časopisecké články MeSH
BACKGROUND: Campylobacter (C.) species are the most common bacterial cause of foodborne diarrhea in humans. Despite colonization, most animals do not show clinical signs, making recognition of affected flocks and disruption of the infection chain before slaughter challenging. Turkeys are often cocolonized with C. jejuni and C. coli. To understand the pathogen-host-interaction in the context of two different Campylobacter species, we compared the colonization patterns and quantities in mono- and co-colonized female commercial turkeys. In three repeated experiments we investigated the impact on gut morphology, functional integrity, and microbiota composition as parameters of gut health at seven, 14, and 28 days post-inoculation. RESULTS: Despite successful Campylobacter colonization, clinical signs or pathological lesions were not observed. C. coli persistently colonized the distal intestinal tract and at a higher load compared to C. jejuni. Both strains were isolated from livers and spleens, occurring more frequently in C. jejuni- and co-inoculated turkeys. Especially in C. jejuni-positive animals, translocation was accompanied by local heterophil infiltration, villus blunting, and shallower crypts. Increased permeability and lower electrogenic ion transport of the cecal mucosa were also observed. A lower relative abundance of Clostridia UCG-014, Lachnospiraceae, and Lactobacillaceae was noted in all inoculated groups compared to controls. CONCLUSIONS: In sum, C. jejuni affects gut health and may interfere with productivity in turkeys. Despite a higher cecal load, the impact of C. coli on investigated parameters was less pronounced. Interestingly, gut morphology and functional integrity were also less affected in co-inoculated animals while the C. jejuni load decreased over time, suggesting C. coli may outcompete C. jejuni. Since a microbiota shift was observed in all inoculated groups, future Campylobacter intervention strategies may involve stabilization of the gut microbiota, making it more resilient to Campylobacter colonization in the first place.
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Igwaran A, Okoh AI. Human campylobacteriosis: a public health concern of global importance. Heliyon. 2019;5(11):1–14. doi: 10.1016/j.heliyon.2019.e02814. PubMed DOI PMC
Zhang Q, Sahin O. Campylobacteriosis. In: Swayne DE, editor. Diseases of Poultry. 14. Hoboken, United States: John Wiley and Sons Ltd; 2020. pp. 754–769.
Wallace JS, Stanley KN, Jones K. The colonization of turkeys by thermophilic Campylobacters. J Appl Microbiol. 1998;85(2):224–230. doi: 10.1046/j.1365-2672.1998.00470.x. PubMed DOI
Awad WA, Hess C, Hess M. Re-thinking the chicken-Campylobacter jejuni interaction: a review. Avian Pathol. 2018;47(4):352–363. doi: 10.1080/03079457.2018.1475724. PubMed DOI
Van Deun K, Pasmans F, Van Immerseel F, Ducatelle R, Haesebrouck F. Butyrate protects Caco-2 cells from Campylobacter jejuni invasion and translocation. Br J Nutr. 2008;100(3):480–484. doi: 10.1017/S0007114508921693. PubMed DOI
Awad WA, Molnar A, Aschenbach JR, Ghareeb K, Khayal B, Hess C, Liebhart D, Dublecz K, Hess M. Campylobacter infection in chickens modulates the intestinal epithelial barrier function. J Innate Immun. 2015;21(2):151–160. doi: 10.1177/1753425914521648. PubMed DOI
Pielsticker C, Glunder G, Aung YH, Rautenschlein S. Colonization pattern of C. jejuni isolates of human and avian origin and differences in the induction of immune responses in chicken. Vet Immunol Immunopathol. 2016;169:1–9. doi: 10.1016/j.vetimm.2015.11.005. PubMed DOI
Awad WA, Aschenbach JR, Ghareeb K, Khayal B, Hess C, Hess M. Campylobacter jejuni influences the expression of nutrient transporter genes in the intestine of chickens. Vet Microbiol. 2014;172(1–2):195–201. doi: 10.1016/j.vetmic.2014.04.001. PubMed DOI
Awad WA, Mann E, Dzieciol M, Hess C, Schmitz-Esser S, Wagner M, Hess M. Age-related differences in the luminal and mucosa-associated gut microbiome of broiler chickens and shifts associated with Campylobacter jejuni infection. Front Cell Infect Microbiol. 2016;6:1–17. doi: 10.3389/fcimb.2016.00154. PubMed DOI PMC
Awad WA, Dublecz F, Hess C, Dublecz K, Khayal B, Aschenbach JR, Hess M. Campylobacter jejuni colonization promotes the translocation of Escherichia coli to extra-intestinal organs and disturbs the short-chain fatty acids profiles in the chicken gut. Poult Sci. 2016;95(10):2259–2265. doi: 10.3382/ps/pew151. PubMed DOI
Backert S, Boehm M, Wessler S, Tegtmeyer N. Transmigration route of Campylobacter jejuni across polarized intestinal epithelial cells: paracellular, transcellular or both? Cell Commun Signal. 2013;11:1–15. doi: 10.1186/1478-811x-11-72. PubMed DOI PMC
Humphrey S, Chaloner G, Kemmett K, Davidson N, Williams N, Kipar A, Humphrey T, Wigley P. Campylobacter jejuni is not merely a commensal in commercial broiler chickens and affects bird welfare. mBio. 2014;5(4):1–7. doi: 10.1128/mBio.01364-14. PubMed DOI PMC
Sylte MJ, Sivasankaran SK, Trachsel J, Sato Y, Wu Z, Johnson TA, Chandra LC, Zhang Q, Looft T. The acute host-response of turkeys colonized with Campylobacter coli. Front Vet Sci. 2021;8:1–11. doi: 10.3389/fvets.2021.613203. PubMed DOI PMC
de Zoete MR, Keestra AM, Roszczenko P, van Putten JPM. Activation of human and chicken toll-like receptors by Campylobacter spp. Infect Immun. 2010;78(3):1229–1238. doi: 10.1128/Iai.00897-09. PubMed DOI PMC
Sylte MJ, Johnson TA, Meyer EL, Inbody MH, Trachsel J, Looft T, Susta L, Wu Z, Zhang Q. Intestinal colonization and acute immune response in commercial turkeys following inoculation with Campylobacter jejuni constructs encoding antibiotic-resistance markers. Vet Immunol Immunopathol. 2019;210:6–14. doi: 10.1016/j.vetimm.2019.02.003. PubMed DOI
Scupham AJ. Succession in the intestinal microbiota of preadolescent turkeys. FEMS Microbiol Ecol. 2007;60(1):136–147. doi: 10.1111/j.1574-6941.2006.00245.x. PubMed DOI
Wilkinson TJ, Cowan AA, Vallin HE, Onime LA, Oyama LB, Cameron SJ, Gonot C, Moorby JM, Waddams K, Theobald VJ, Leemans D, Bowra S, Nixey C, Huws SA. Characterization of the microbiome along the gastrointestinal tract of growing turkeys. Front Microbiol. 2017;8:1–11. doi: 10.3389/fmicb.2017.01089. PubMed DOI PMC
Kubasova T, Kollarcikova M, Crhanova M, Karasova D, Cejkova D, Sebkova A, Matiasovicova J, Faldynova M, Pokorna A, Cizek A, Rychlik I. Contact with adult hen affects development of caecal microbiota in newly hatched chicks. PLoS One. 2019;14(3):1–13. doi: 10.1371/journal.pone.0212446. PubMed DOI PMC
Connerton PL, Richards PJ, Lafontaine GM, O’Kane PM, Ghaffar N, Cummings NJ, Smith DL, Fish NM, Connerton IF. The effect of the timing of exposure to Campylobacter jejuni on the gut microbiome and inflammatory responses of broiler chickens. Microbiome. 2018;6(88):1–17. doi: 10.1186/s40168-018-0477-5. PubMed DOI PMC
Dhillon AS, Shivaprasad HL, Schaberg D, Wier F, Weber S, Bandli D. Campylobacter jejuni infection in broiler chickens. Avian Dis. 2006;50(1):55–58. doi: 10.1637/7411-071405r.1. PubMed DOI
Alter T, Weber RM, Hamedy A, Glunder G. Carry-over of thermophilic Campylobacter spp. between sequential and adjacent poultry flocks. Vet Microbiol. 2011;147(1–2):90–95. doi: 10.1016/j.vetmic.2010.06.005. PubMed DOI
Aviagen Turkeys. B.U.T. 6 Performance Objectives. vol POBRB6/EN. 5. Tattenhall, United Kingdom: Aviagen Turkeys Limited; 2020.
Beery JT, Hugdahl MB, Doyle MP. Colonization of gastrointestinal tracts of chicks by Campylobacter jejuni. Appl Environ Microbiol. 1988;54(10):2365–2370. doi: 10.1128/aem.54.10.2365-2370.1988. PubMed DOI PMC
Wassenaar TM, Vanderzeijst BAM, Ayling R, Newell DG. Colonization of chicks by motility mutants of Campylobacter jejuni demonstrates the importance of flagellin-a expression. J Gen Microbiol. 1993;139:1171–1175. doi: 10.1099/00221287-139-6-1171. PubMed DOI
Chaloner G, Wigley P, Humphrey S, Kemmett K, Lacharme-Lora L, Humphrey T, Williams N. Dynamics of dual infection with Campylobacter jejuni strains in chickens reveals distinct strain-to-strain variation in infection ecology. Appl Environ Microbiol. 2014;80(20):6366–6372. doi: 10.1128/Aem.01901-14. PubMed DOI PMC
Cox NA, Hofacre CL, Bailey JS, Buhr RJ, Wilson JL, Hiett KL, Richardson LJ, Musgrove MT, Cosby DE, Tankson JD, Vizzier YL, Cray PF, Vaughn LE, Holt PS, Bourassa DV. Presence of Campylobacter jejuni in various organs one hour, one day, and one week following oral or intracloacal inoculations of broiler chicks. Avian Dis. 2005;49(1):155–158. doi: 10.1637/7234-070704r. PubMed DOI
Backert S, Hofreuter D. Molecular methods to investigate adhesion, transmigration, invasion and intracellular survival of the foodborne pathogen Campylobacter jejuni. J Microbiol Methods. 2013;95(1):8–23. doi: 10.1016/j.mimet.2013.06.031. PubMed DOI
Kwon O, Han TS, Son MY. Intestinal morphogenesis in development, regeneration, and disease: the potential utility of intestinal organoids for studying compartmentalization of the crypt-villus structure. Front Cell Dev Biol. 2020;8:1–14. doi: 10.3389/fcell.2020.593969. PubMed DOI PMC
Powell FL, Rothwell L, Clarkson MJ, Kaiser P. The turkey, compared to the chicken, fails to mount an effective early immune response to Histomonas meleagridis in the gut. Parasite Immunol. 2009;31(6):312–327. doi: 10.1111/j.1365-3024.2009.01113.x. PubMed DOI
Garriga C, Rovira N, Moreto M, Planas JM. Expression of Na+-D-glucose cotransporter in brush-border membrane of the chicken intestine. Am J Physiol Regul Integr Comp Physiol. 1999;276(2):627–631. doi: 10.1152/ajpregu.1999.276.2.R627. PubMed DOI
Awad WA, Hess C, Khayal B, Aschenbach JR, Hess M. In vitro exposure to Escherichia coli decreases ion conductance in the jejunal epithelium of broiler chickens. PLoS One. 2014;9(3):1–8. doi: 10.1371/journal.pone.0092156. PubMed DOI PMC
Riesenfeld G, Sklan D, Bar A, Eisner U, Hurwitz S. Glucose-absorption and starch digestion in the intestine of the chicken. J Nutr. 1980;110(1):117–121. doi: 10.1093/jn/110.1.117. PubMed DOI
Pinca A, Bautista N, Adiova C, Sangel P. Comparative expression analysis of small intestine nutrient transporters sodium/glucose cotransporter 1 (SGLT1) and peptide transporter 1 (PepT1) between Itik Pinas (Anas platyrhynchos L.) and commercial layer chicken (Gallus gallus domesticus) Philipp J Sci. 2019;148:433–439.
Li H, Cheng J, Yuan Y, Luo R, Zhu Z. Age-related intestinal monosaccharides transporters expression and villus surface area increase in broiler and layer chickens. J Anim Physiol Anim Nutr (Berl) 2020;104(1):144–155. doi: 10.1111/jpn.13211. PubMed DOI
Thorens B. GLUT2, glucose sensing and glucose homeostasis. Diabetologia. 2015;58(2):221–232. doi: 10.1007/s00125-014-3451-1. PubMed DOI
Dharmsathaphorn K, Pandol SJ. Mechanism of chloride secretion induced by carbachol in a colonic epithelial-cell line. J Clin Invest. 1986;77(2):348–354. doi: 10.1172/Jci112311. PubMed DOI PMC
Schwarz A, Gauly M, Abel H, Das G, Humburg J, Weiss AT, Breves G, Rautenschlein S. Pathobiology of Heterakis gallinarum mono-infection and co-infection with Histomonas meleagridis in layer chickens. Avian Pathol. 2011;40(3):277–287. doi: 10.1080/03079457.2011.561280. PubMed DOI
Moran O, Zegarra-Moran O. On the measurement of the functional properties of the CFTR. J Cyst Fibros. 2008;7(6):483–494. doi: 10.1016/j.jcf.2008.05.003. PubMed DOI
Nighot PK, Blikslager AT. ClC-2 regulates mucosal barrier function associated with structural changes to the villus and epithelial tight junction. Am J Physiol Gastrointest Liver Physiol. 2010;299(2):449–456. doi: 10.1152/ajpgi.00520.2009. PubMed DOI
Negoro S, Shimohata T, Hatayama S, Sato Y, Matsumoto M, Iba H, Aihara M, Uebanso T, Hamada Y, Nishikawa Y, Yamasaki S, Mawatari K, Takahashi A. Campylobacter jejuni infection suppressed Cl- secretion induced by CFTR activation in T-84 cells. J Infect Chemother. 2014;20(11):682–688. doi: 10.1016/j.jiac.2014.07.007. PubMed DOI
Shannon CE. A mathematical theory of communication. Bell Syst Tech J. 1948;27(3):379–423. doi: 10.1002/j.1538-7305.1948.tb01338.x. DOI
Hankel J, Jung K, Kuder H, Keller B, Keller C, Galvez E, Strowig T, Visscher C. Caecal microbiota of experimentally Campylobacter jejuni-infected chickens at different ages. Front Microbiol. 2019;10:1–11. doi: 10.3389/fmicb.2019.02303. PubMed DOI PMC
Biddle A, Stewart L, Blanchard J, Leschine S. Untangling the genetic basis of fibrolytic specialization by Lachnospiraceae and Ruminococcaceae in diverse gut communities. Diversity. 2013;5(3):627–640. doi: 10.3390/d5030627. DOI
Li Z, Wang WW, Liu D, Guo YM. Effects of Lactobacillus acidophilus on the growth performance and intestinal health of broilers challenged with Clostridium perfringens. J Anim Sci Biotechnol. 2018;9:1–10. doi: 10.1186/s40104-018-0243-3. PubMed DOI PMC
Kitamoto S, Alteri CJ, Rodrigues M, Nagao-Kitamoto H, Sugihara K, Himpsl SD, Bazzi M, Miyoshi M, Nishioka T, Hayashi A, Morhardt TL, Kuffa P, Grasberger H, El-Zaatari M, Bishu S, Ishii C, Hirayama A, Eaton KA, Dogan B, Simpson KW, Inohara N, Mobley HLT, Kao JY, Fukuda S, Barnich N, Kamada N. Dietary L-serine confers a competitive fitness advantage to Enterobacteriaceae in the inflamed gut. Nat Microbiol. 2020;5(1):116–125. doi: 10.1038/s41564-019-0591-6. PubMed DOI PMC
Wang G, He YF, Jin X, Zhou YH, Chen XH, Zhao JX, Zhang H, Chen W. The effect of co-infection of food-borne pathogenic bacteria on the progression of Campylobacter jejuni infection in mice. Front Microbiol. 2018;9:1–13. doi: 10.3389/fmicb.2018.01977. PubMed DOI PMC
Lam YY, Ha CWY, Campbell CR, Mitchell AJ, Dinudom A, Oscarsson J, Cook DI, Hunt NH, Caterson ID, Holmes AJ, Storlien LH. Increased gut permeability and microbiota change associate with mesenteric fat inflammation and metabolic dysfunction in diet-induced obese mice. PLoS One. 2012;7(3):1–10. doi: 10.1371/journal.pone.0034233. PubMed DOI PMC
Ishikawa T, Mizunoe Y, Kawabata S, Takade A, Harada M, Wai SN, Yoshida S. The iron-binding protein Dps confers hydrogen peroxide stress resistance to Campylobacter jejuni. J Bacteriol. 2003;185(3):1010–1017. doi: 10.1128/Jb.185.3.1010-1017.2003. PubMed DOI PMC
Kers JG, Velkers FC, Fischer EAJ, Hermes GDA, Stegeman JA, Smidt H. Host and environmental factors affecting the intestinal microbiota in chickens. Front Microbiol. 2018;9:1–14. doi: 10.3389/fmicb.2018.00235. PubMed DOI PMC
Grimes JL Nutritional determinants for gut health and litter characteristics in turkeys. In: 20th European Symposium on Poultry Nutrition, Prague, Czech Republic, 2015. World’s Poultry Science Association (WPSA), pp 115–120
Xiao SS, Mi JD, Mei L, Liang JB, Feng KX, Wu YB, Liao XD, Wang Y. Microbial diversity and community variation in the intestines of layer chickens. Animals-Basel. 2021;11(3):1–17. doi: 10.3390/ani11030840. PubMed DOI PMC
Bindari YR, Gerber PF. Centennial review: factors affecting the chicken gastrointestinal microbial composition and their association with gut health and productive performance. Poult Sci. 2022;101(1):1–19. doi: 10.1016/j.psj.2021.101612. PubMed DOI PMC
Jolley KA, Bray JE, Maiden MCJ. Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Res. 2018;3:1–20. doi: 10.12688/wellcomeopenres.14826.1. PubMed DOI PMC
Rath A, Rautenschlein S, Rzeznitzeck J, Breves G, Hewicker-Trautwein M, Waldmann KH, von Altrock A. Impact of Campylobacter spp. on the integrity of the porcine gut. Animals-Basel. 2021;11(9):1–14. doi: 10.3390/ani11092742. PubMed DOI PMC
European Parliament and Council (2010) Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010 on the protection of animals used for scientific purposes.
Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9(7):671–675. doi: 10.1038/nmeth.2089. PubMed DOI PMC
Clarke LL. A guide to Ussing chamber studies of mouse intestine. Am J Physiol Gastrointest Liver Physiol. 2009;296(6):1151–1166. doi: 10.1152/ajpgi.90649.2008. PubMed DOI PMC
Elfers K, Marr I, Wilkens MR, Breves G, Langeheine M, Brehm R, Muscher-Banse AS. Expression of tight junction proteins and cadherin 17 in the small intestine of young goats offered a reduced N and/or Ca diet. PLoS One. 2016;11(4):1–19. doi: 10.1371/journal.pone.0154311. PubMed DOI PMC
Polansky O, Sekelova Z, Faldynova M, Sebkova A, Sisak F, Rychlik I. Important metabolic pathways and biological processes expressed by chicken cecal microbiota. Appl Environ Microbiol. 2016;82(5):1569–1576. doi: 10.1128/Aem.03473-15. 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, Tumbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7(5):335–336. doi: 10.1038/nmeth.f.303. PubMed DOI PMC
Bolyen E, Rideout JR, Dillon MR, Bokulich N, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bai Y, Bisanz JE, Bittinger K, Brejnrod A, Brislawn CJ, Brown CT, Callahan BJ, Caraballo-Rodriguez AM, Chase J, Cope EK, Da Silva R, Diener C, Dorrestein PC, Douglas GM, Durall DM, Duvallet C, Edwardson CF, Ernst M, Estaki M, Fouquier J, Gauglitz JM, Gibbons SM, Gibson DL, Gonzalez A, Gorlick K, Guo JR, Hillmann B, Holmes S, Holste H, Huttenhower C, Huttley GA, Janssen S, Jarmusch AK, Jiang LJ, Kaehler BD, Bin Kang K, Keefe CR, Keim P, Kelley ST, Knights D, Koester I, Kosciolek T, Kreps J, Langille MGI, Lee J, Ley R, Liu YX, Loftfield E, Lozupone C, Maher M, Marotz C, Martin BD, McDonald D, McIver LJ, Melnik AV, Metcalf JL, Morgan SC, Morton JT, Naimey AT, Navas-Molina JA, Nothias LF, Orchanian SB, Pearson T, Peoples SL, Petras D, Preuss ML, Pruesse E, Rasmussen LB, Rivers A, Robeson MS, Rosenthal P, Segata N, Shaffer M, Shiffer A, Sinha R, Song SJ, Spear JR, Swafford AD, Thompson LR, Torres PJ, Trinh P, Tripathi A, Turnbaugh PJ, Ul-Hasan S, vander Hooft JJJ, Vargas F, Vazquez-Baeza Y, Vogtmann E, von Hippel M, Walters W, Wan YH, Wang MX, Warren J, Weber KC, Williamson CHD, Willis AD, Xu ZZ, Zaneveld JR, Zhang YL, Zhu QY, Knight R, Caporaso JG. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37(8):852–857. doi: 10.1038/s41587-019-0209-9. PubMed DOI PMC