1887

Abstract

Campylobacteriosis is still the most commonly reported zoonosis in the European Union causing gastrointestinal disease in humans. One of the most common sources for these food-borne infections is broiler meat. Interactions between (.) and the intestinal microbiota might influence colonization in chickens. The aim of the present study was to gain further knowledge about exclusive interactions of the host microbiota with in -specific phage-free chickens under standardized conditions and special biosafety precautions.

Therefore, 12 artificially infected ( inoculum with a challenge dose of 7.64 log c.f.u.) and 12 control chickens of the breed Ross 308 were kept under special biosafety measures in an animal facility. At day 42 of life, microbiota studies were performed on samples of caecal digesta and mucus. No -specific phages were detected by real-time PCR analysis of caecal digesta of control or artificially infected chickens. Amplification of the 16S rRNA gene was performed within the hypervariable region V4 and subsequently sequenced with Illumina MiSeq platform. R (version 4.0.2) was used to compare the microbiota between -negative and -positive chickens. The factor chickens’ infection status contributed significantly to the differences in microbial composition of mucosal samples, explaining 10.6 % of the microbiota variation (=0.007) and in digesta samples, explaining 9.69 % of the microbiota variation (=0.015). The strongest difference between -non-infected and -infected birds was observed for the family whose presence in -infected birds could not be demonstrated. Further, several genera of the family appeared to be depressed in its abundance due to infection. A negative correlation was found between R-7 group and in -colonised chickens, both genera potentially competing for substrate. This makes R-7 group highly interesting for further studies that aim to find control options for infections and assess the relevance of this finding for chicken health and colonization.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2022-10-03
2024-04-29
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References

  1. European Food Safety Authority (EFSA), European Centre for Disease Prevention (ECDC) The european union one health 2019 zoonoses report. EFSA J 2021; 19:e06406 [View Article]
    [Google Scholar]
  2. Commission Regulation (EU) 2017/1495 of 23 August 2017 amending Regulation (EC) No 2073/2005 as regards Campylobacter in broiler carcases; 2017
  3. Koutsoumanis K, Allende A, Alvarez-Ordóñez A, Bolton D, Bover-Cid S et al. Update and review of control options for Campylobacter in broilers at primary production. EFSA J 2020; 18:e06090 [View Article]
    [Google Scholar]
  4. Newell DG. Animal models of Campylobacter jejuni colonization and disease and the lessons to be learned from similar Helicobacter pylori models. J Appl Microbiol 2001; 90:57S–67S [View Article]
    [Google Scholar]
  5. Hankel J, Jung K, Kuder H, Keller B, Keller C et al. Caecal microbiota of experimentally Campylobacter jejuni-infected chickens at different ages. Front Microbiol 2019; 10:2303 [View Article]
    [Google Scholar]
  6. Han Z, Li L, Willer T, Baumgärtner W, Rautenschlein S. Adhesion and invasion of Campylobacter jejuni in chickens with a modified gut microbiota due to antibiotic treatment. Vet Microbiol 2020; 240:108504 [View Article]
    [Google Scholar]
  7. Han Z, Willer T, Li L, Pielsticker C, Rychlik I et al. Influence of the gut microbiota composition on Campylobacter jejuni colonization in Chickens. Infect Immun 2017; 85:e00380-17 [View Article]
    [Google Scholar]
  8. Kampmann C, Dicksved J, Engstrand L, Rautelin H. Composition of human faecal microbiota in resistance to Campylobacter infection. Clin Microbiol Infect 2016; 22:61 [View Article] [PubMed]
    [Google Scholar]
  9. Alemka A, Corcionivoschi N, Bourke B. Defense and adaptation: the complex inter-relationship between Campylobacter jejuni and mucus. Front Cell Infect Microbiol 2012; 2:15 [View Article]
    [Google Scholar]
  10. Borda-Molina D, Seifert J, Camarinha-Silva A. Current perspectives of the Chicken gastrointestinal tract and its microbiome. Comput Struct Biotechnol J 2018; 16:131–139 [View Article]
    [Google Scholar]
  11. Atterbury RJ, Dillon E, Swift C, Connerton PL, Frost JA et al. Correlation of Campylobacter bacteriophage with reduced presence of hosts in broiler chicken ceca. Appl Environ Microbiol 2005; 71:4885–4887 [View Article] [PubMed]
    [Google Scholar]
  12. Naumann C, Bassler R. Band III Die chemische Untersuchung von Futtermitteln. Methoden der landwirtschaftlichen Forschungs- und Untersuchungsanstalt Darmstadt: VDLUFA-Verlag; 2012
    [Google Scholar]
  13. Visscher C, Klingenberg L, Hankel J, Brehm R, Langeheine M et al. Influence of a specific amino acid pattern in the diet on the course of an experimental Campylobacter jejuni infection in broilers. Poult Sci 2018; 97:4020–4030 [View Article] [PubMed]
    [Google Scholar]
  14. Jäckel C, Hammerl JA, Rau J, Hertwig S. A multiplex real-time PCR for the detection and differentiation of Campylobacter phages. PLOS ONE 2017; 12:e0190240 [View Article] [PubMed]
    [Google Scholar]
  15. Gong J, Forster RJ, Yu H, Chambers JR, Sabour PM et al. Diversity and phylogenetic analysis of bacteria in the mucosa of chicken ceca and comparison with bacteria in the cecal lumen. FEMS Microbiol Lett 2002; 208:1–7 [View Article] [PubMed]
    [Google Scholar]
  16. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A 2011; 108 Suppl 1:4516–4522 [View Article]
    [Google Scholar]
  17. Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 2013; 10:996–998 [View Article] [PubMed]
    [Google Scholar]
  18. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 2013; 41:D590–6 [View Article]
    [Google Scholar]
  19. Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 2007; 73:5261–5267 [View Article] [PubMed]
    [Google Scholar]
  20. McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLOS ONE 2013; 8:e61217 [View Article]
    [Google Scholar]
  21. Oksanen J, Blanchet F, Friendly M, Kindt R, Legendre P et al. Vegan: community ecology package. R package version 2.5-7; 2020
  22. Kassambara A. Pipe-Friendly Framework for Basic Statistical Tests [R Package Rstatix Version 0.7.0]; 2021 https://cloud.r-project.org/web/packages/rstatix/index.html
  23. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 2014; 15:12 [View Article] [PubMed]
    [Google Scholar]
  24. Wickham H. ggplot2: Elegant Graphics for Data Analysis New York: Springer-Verlag; 2016
    [Google Scholar]
  25. Wei T, Simko V. R package “corrplot”: Visualization of a Correlation Matrix (Version 0.84); 2017 https://github.com/taiyun/corrplot
  26. Anonymus ROSS 308/ROSS 308 FF BROILER: Performance Objectives [internet]. Aviagen Group; 2019 https://eu.aviagen.com/tech-center/
  27. Awad WA, Mann E, Dzieciol M, Hess C, Schmitz-Esser S et al. 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; 6:154 [View Article]
    [Google Scholar]
  28. Thibodeau A, Fravalo P, Yergeau É, Arsenault J, Lahaye L et al. Chicken caecal microbiome modifications induced by Campylobacter jejuni colonization and by a non-antibiotic feed additive. PLoS One 2015; 10:e0131978 [View Article]
    [Google Scholar]
  29. McKenna A, Ijaz UZ, Kelly C, Linton M, Sloan WT et al. Impact of industrial production system parameters on chicken microbiomes: mechanisms to improve performance and reduce Campylobacter. Microbiome 2020; 8:128 [View Article]
    [Google Scholar]
  30. Pandit RJ, Hinsu AT, Patel NV, Koringa PG, Jakhesara SJ et al. Microbial diversity and community composition of caecal microbiota in commercial and indigenous Indian chickens determined using 16s rDNA amplicon sequencing. Microbiome 2018; 6:115 [View Article]
    [Google Scholar]
  31. Kaakoush NO, Sodhi N, Chenu JW, Cox JM, Riordan SM et al. The interplay between Campylobacter and Helicobacter species and other gastrointestinal microbiota of commercial broiler chickens. Gut Pathog 2014; 6:18 [View Article]
    [Google Scholar]
  32. Connerton PL, Richards PJ, Lafontaine GM, O’Kane PM, Ghaffar N et al. The effect of the timing of exposure to Campylobacter jejuni on the gut microbiome and inflammatory responses of broiler chickens. Microbiome 2018; 6: [View Article] [PubMed]
    [Google Scholar]
  33. Vos P, Garrity G, Jones D, Krieg NR, Ludwig W et al. Bergey’s manual of systematic bacteriology The Firmicutes: Springer Science & Business Media; 2011
    [Google Scholar]
  34. Patterson JA, Burkholder KM. Application of prebiotics and probiotics in poultry production. Poult Sci 2003; 82:627–631 [View Article] [PubMed]
    [Google Scholar]
  35. Dolka B, Chrobak-Chmiel D, Czopowicz M, Szeleszczuk P. Characterization of pathogenic Enterococcus cecorum from different poultry groups: Broiler chickens, layers, turkeys, and waterfowl. PLoS One 2017; 12:e0185199 [View Article]
    [Google Scholar]
  36. Pd H, Defoort P, Steelant J, Swam H, Tanghe L et al. Enterococcus cecorum osteomyelitis and arthritis in broiler chickens. Vlaams Diergeneeskundig Tijdschrift 2009; 78:44–48
    [Google Scholar]
  37. Jung A, Chen LR, Suyemoto MM, Barnes HJ, Borst LB. A review of Enterococcus cecorum Infection in Poultry. Avian Dis 2018; 62:261–271 [View Article]
    [Google Scholar]
  38. Pultz NJ, Hoskins LC, Donskey CJ. Vancomycin-resistant Enterococci may obtain nutritional support by scavenging carbohydrate fragments generated during mucin degradation by the anaerobic microbiota of the colon. Microb Drug Resist 2006; 12:63–67 [View Article]
    [Google Scholar]
  39. Sicard J-F, Le Bihan G, Vogeleer P, Jacques M, Harel J. Interactions of intestinal bacteria with components of the intestinal mucus. Front Cell Infect Microbiol 2017; 7:387 [View Article]
    [Google Scholar]
  40. Tu QV, McGuckin MA, Mendz GL. Campylobacter jejuni response to human mucin MUC2: modulation of colonization and pathogenicity determinants. J Med Microbiol 2008; 57:795–802 [View Article]
    [Google Scholar]
  41. Richards P, Fothergill J, Bernardeau M, Wigley P. Development of the caecal microbiota in three broiler breeds. Front Vet Sci 2019; 6:201 [View Article]
    [Google Scholar]
  42. Rychlik I. Composition and function of chicken gut microbiota. Animals 2020; 10:103 [View Article]
    [Google Scholar]
  43. 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; 100:480–484 [View Article]
    [Google Scholar]
  44. Duncan SH, Hold GL, Harmsen HJM, Stewart CS, Flint HJ. Growth requirements and fermentation products of Fusobacterium prausnitzii, and a proposal to reclassify it as Faecalibacterium prausnitzii gen. nov., comb. nov. Int J Syst Evol Microbiol 2002; 52:2141–2146 [View Article]
    [Google Scholar]
  45. Patuzzi I, Orsini M, Cibin V, Petrin S, Mastrorilli E et al. The Interplay between Campylobacter and the caecal microbial community of commercial broiler chickens over ime. Microorganisms 2021; 9:221 [View Article]
    [Google Scholar]
  46. Allaoua M, Bonnafé E, Etienne P, Noirot V, Gabarrou J-F et al. A carvacrol-based product reduces Campylobacter jejuni load and alters microbiota composition in the caeca of chickens. J Appl Microbiol 2022; 132:4501–4516 [View Article]
    [Google Scholar]
  47. Fisinin VI, Laptev GY, Nikonov IN, Il’Ina LA, Yildirim EA et al. Microbiome and production performance. Sel’skokhozyaistvennaya Biologiya 2016; 51:883–890 [View Article]
    [Google Scholar]
  48. Borda-Molina D, Vital M, Sommerfeld V, Rodehutscord M, Camarinha-Silva A. Insights into broilers’ gut microbiota fed with phosphorus, calcium, and phytase supplemented diets. Front Microbiol 2016; 7:2033 [View Article]
    [Google Scholar]
  49. Trujillo ME, Dedysh S, DeVos P, Hedlund B, Kämpfer P et al. Bergey’s Manual of Systematics of Archaea and Bacteria 2016 pp 1–5 [View Article]
    [Google Scholar]
  50. Asakura H, Nakayama T, Yamamoto S, Izawa K, Kawase J et al. Long-term grow-out affects Campylobacter jejuni colonization fitness in coincidence with altered microbiota and lipid composition in the cecum of laying hens. Front Vet Sci 2021; 8:675570 [View Article]
    [Google Scholar]
  51. Morotomi M, Nagai F, Watanabe Y. Description of Christensenella minuta gen. nov., sp. nov., isolated from human faeces, which forms a distinct branch in the order Clostridiales, and proposal of Christensenellaceae fam. nov. Int J Syst Evol Microbiol 2012; 62:144–149 [View Article]
    [Google Scholar]
  52. Waters JL, Ley RE. The human gut bacteria Christensenellaceae are widespread, heritable, and associated with health. BMC Biol 2019; 17:83 [View Article]
    [Google Scholar]
  53. Zou A, Sharif S, Parkinson J. Lactobacillus elicits a “Marmite effect” on the chicken cecal microbiome. NPJ Biofilms Microbiomes 2018; 4:27 [View Article]
    [Google Scholar]
  54. Zhou X, Jiang X, Yang C, Ma B, Lei C et al. Cecal microbiota of tibetan chickens from five geographic regions were determined by 16S rRNA sequencing. Microbiologyopen 2016; 5:753–762 [View Article]
    [Google Scholar]
  55. Cazals A, Estellé J, Bruneau N, Coville J-L, Menanteau P et al. Differences in caecal microbiota composition and Salmonella carriage between experimentally infected inbred lines of chickens. Genet Sel Evol 2022; 54:7 [View Article]
    [Google Scholar]
  56. Hofreuter D. Defining the metabolic requirements for the growth and colonization capacity of Campylobacter jejuni. Front Cell Infect Microbiol 2014; 4:137 [View Article]
    [Google Scholar]
  57. Gao B, Vorwerk H, Huber C, Lara-Tejero M, Mohr J et al. Metabolic and fitness determinants for in vitro growth and intestinal colonization of the bacterial pathogen Campylobacter jejuni. PLoS Biol 2017; 15:e2001390 [View Article]
    [Google Scholar]
  58. Beaumont M, Portune KJ, Steuer N, Lan A, Cerrudo V et al. Quantity and source of dietary protein influence metabolite production by gut microbiota and rectal mucosa gene expression: a randomized, parallel, double-blind trial in overweight humans. Am J Clin Nutr 2017; 106:1005–1019 [View Article]
    [Google Scholar]
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