Chicken Caecal Microbiome modifications induced by campylobacter Jejuni colonization and by a non-antibiotic feed additive

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Thibodeau, Alexandre ^a   Fravalo, Philippe ^a   Yergeau, Etienne ^b   Arsenault, Julie ^a   Lahaye, Ludovic ^c   Letellier, Ann ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^c Groupe de Recherche et D'enseignement en Salubrité Alimentaire ^*  (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL COUNT; BACTERIAL GENE; BIFIDOBACTERIUM; CAMPYLOBACTER JEJUNI; CECUM; CHICKEN; CLOSTRIDIA; CONTROLLED STUDY; DIET SUPPLEMENTATION; GENE SEQUENCE; INTESTINE FLORA; MICROBIAL DIVERSITY; MICROBIOME; MOLLICUTES; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; RNA 16S GENE; STREPTOCOCCUS; ANIMAL; ANIMAL FOOD; BIODIVERSITY; DRUG EFFECTS; GENETICS; MICROBIOLOGY; MICROFLORA; MOLECULAR TYPING; PHYSIOLOGY;

FOOD ADDITIVE; RNA 16S; SORBIC ACID; THYMOL;

ANIMAL FEED; ANIMALS; BIFIDOBACTERIUM; BIODIVERSITY; CAMPYLOBACTER JEJUNI; CECUM; CHICKENS; FOOD ADDITIVES; MICROBIOTA; MOLECULAR TYPING; RNA, RIBOSOMAL, 16S; SORBIC ACID; THYMOL;

EID: 84941308459     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0131978     Document Type: Article

References (60)

1. Cean A, Stef L, Simiz E, Julean C, Dumitrescu G, Vasile A, et al. Effect of human isolated probiotic bacteria on preventing Campylobacter jejuni colonization of poultry. Foodborne Pathog Dis. 2015; 12(2): 122-30. doi: 10.1089/fpd.2014.1849
2. Gras LM, Smid JH, Wagenaar JA, de Boer AG, Havelaar AH, Friesema IHM, et al. Risk Factors for Campylobacteriosis of Chicken, Ruminant, and Environmental Origin: A Combined Case-Control and Source Attribution Analysis. Plos One. 2012; 7(8). ARTN e42599 doi: 10.1371/journal.pone.0042599
3. Hermans D, Pasmans F, Messens W, Martel A, Van Immerseel F, Rasschaert G, et al. Poultry as a Host for the Zoonotic Pathogen Campylobacter jejuni. Vector-Borne Zoonot. 2012; 12(2):89-98. doi: 10.1089/vbz.2011.0676.
4. Luber P, Brynestad S, Topsch D, Scherer K, Bartelt E. Quantification of Campylobacter species crosscontamination during handling of contaminated fresh chicken parts in kitchens. Appl Environ Microb. 2006; 72(1):66-70. doi: 10.1128/Aem.72.1.66-70.2006.
5. Rosenquist H, Nielsen NL, Sommer HM, Norrung B, Christensen BB. Quantitative risk assessment of human campylobacteriosis associated with thermophilic Campylobacter species in chickens. Int J Food Microbiol. 2003; 83(1):87-103. doi: 10.1016/S0168-1605(02)00317-3
6. Hermans D, Pasmans F, Heyndrickx M, Van Immerseel F, Martel A, Deun K, et al. A tolerogenic mucosal immune response leads to persistent Campylobacter jejuni colonization in the chicken gut. Crit Rev Microbiol. 2012; 38(1):17-29. doi: 10.3109/1040841x.2011.615298.
7. Hermans D, Van Deun K, Martel A, Van Immerseel F, Messens W, Heyndrickx M, et al. Colonization factors of Campylobacter jejuni in the chicken gut. Vet Res. 2011; 42. Artn 82 doi: 10.1186/1297-9716-42-82.
8. Laisney MJ, Gillard MO, Salvat G. Influence of bird strain on competitive exclusion of Campylobacter jejuni in young chicks. Brit Poultry Sci. 2004; 45(1):49-54. doi: 10.1080/00071660410001668851.
9. Sylvester FA, Philpott D, Gold B, Lastovica A, Forstner JF. Adherence to lipids and intestinal mucin by a recently recognized human pathogen, Campylobacter upsaliensis. Infect Immun. 1996; 64(10): 4060-6.
10. Van Deun K, Pasmans F, Ducatelle R, Flahou B, Vissenberg K, Martel A, et al. Colonization strategy of Campylobacter jejuni results in persistent infection of the chicken gut. Vet Microbiol. 2008; 130(3-4): 285-97. doi: 10.1016/j.vetmic.2007.11.027.
11. Smith CK, AbuOun M, Cawthraw SA, Humphrey TJ, Rothwell L, Kaiser P, et al. Campylobacter colonization of the chicken induces a proinflammatory response in mucosal tissues. Fems Immunol Med Mic. 2008; 54(1):114-21. doi: 10.1111/j.1574-695X.2008.00458.x.
12. Humphrey S, Chaloner G, Kemmett K, Davidson N, Williams N, Kipar A, et al. Campylobacter jejuni Is Not Merely a Commensal in Commercial Broiler Chickens and Affects Bird Welfare. Mbio. 2014; 5(4). UNSP e01364-14 doi: 10.1128/mBio.01364-14
13. Rothberg JM, Hinz W, Rearick TM, Schultz J, Mileski W, Davey M, et al. An integrated semiconductor device enabling non-optical genome sequencing. Nature. 2011; 475(7356):348-52. doi: 10.1038/Nature10242.
14. Yergeau E, Lawrence JR, Sanschagrin S, Waiser MJ, Korber DR, Greer CW. Next-Generation Sequencing of Microbial Communities in the Athabasca River and Its Tributaries in Relation to Oil Sands Mining Activities. Appl Environ Microb. 2012; 78(21):7626-37. doi: 10.1128/Aem.02036-12.
15. Qu A, Brulc JM, Wilson MK, Law BF, Theoret JR, Joens LA, et al. Comparative Metagenomics Reveals Host Specific Metavirulomes and Horizontal Gene Transfer Elements in the Chicken Cecum Microbiome. Plos One. 2008; 3(8). Artn E2945 doi: 10.1371/Journal.Pone.0002945.
16. Wei S, Morrison M, Yu Z. Bacterial census of poultry intestinal microbiome. Poultry Sci. 2013; 92(3): 671-83. doi: 10.3382/ps.2012-02822.
17. Oakley BB, Lillehoj HS, Kogut MH, Kim WK, Maurer JJ, Pedroso A, et al. The chicken gastrointestinal microbiome. Fems Microbiol Lett. 2014; 360(2):100-12. doi: 10.1111/1574-6968.12608
18. Sergeant MJ, Constantinidou C, Cogan TA, Bedford MR, Penn CW, Pallen MJ. Extensive Microbial and Functional Diversity within the Chicken Cecal Microbiome. Plos One. 2014; 9(3). ARTN e91941 doi: 10.1371/journal.pone.0091941.
19. Oakley BB, Buhr RJ, Ritz CW, Kiepper BH, Berrang ME, Seal BS, et al. Successional changes in the chicken cecal microbiome during 42 days of growth are independent of organic acid feed additives. Bmc Vet Res. 2014; 10. Artn 282 doi: 10.1186/S12917-014-0282-8.
20. Giannenas I, Papadopoulos E, Tsalie E, Triantafillou E, Henikl S, Teichmann K, et al. Assessment of dietary supplementation with probiotics on performance, intestinal morphology and microflora of chickens infected with Eimeria tenella. Vet Parasitol. 2012; 188(1-2):31-40. doi: 10.1016/j.vetpar.2012.02.017.
21. Stanley D, Wu SB, Rodgers N, Swick RA, Moore RJ. Differential Responses of Cecal Microbiota to Fishmeal, Eimeria and Clostridium perfringens in a Necrotic Enteritis Challenge Model in Chickens. Plos One. 2014; 9(8). ARTN e104739 doi: 10.1371/journal.pone.0104739.
22. Singh P, Karimi A, Devendra K, Waldroup PW, Cho KK, Kwon YM. Influence of penicillin on microbial diversity of the cecal microbiota in broiler chickens. Poultry Sci. 2013; 92(1):272-6. doi: 10.3382/ps. 2012-02603.
23. Videnska P, Faldynova M, Juricova H, Babak V, Sisak F, Havlickova H, et al. Chicken faecal microbiota and disturbances induced by single or repeated therapy with tetracycline and streptomycin. Bmc Vet Res. 2013; 9. Artn 30 doi: 10.1186/1746-6148-9-30
24. Newell DG, Elvers KT, Dopfer D, Hansson I, Jones P, James S, et al. Biosecurity-Based Interventions and Strategies To Reduce Campylobacter spp. on Poultry Farms. Appl Environ Microb. 2011; 77(24): 8605-14. doi: 10.1128/Aem.01090-10.
25. Hermans D, Van Deun K, Messens W, Martel A, Van Immerseel F, Haesebrouck F, et al. Campylobacter control in poultry by current intervention measures ineffective: Urgent need for intensified fundamental research. Vet Microbiol. 2011; 152(3-4):219-28. doi: 10.1016/j.vetmic.2011.03.010.
26. Thibodeau A, Fravalo P, Taboada EN, Laurent-Lewandowski S, Guevremont E, Quessy S, et al. Extensive characterization of Campylobacter jejuni chicken isolates to uncover genes involved in the ability to compete for gut colonization. Bmc Microbiol. 2015; 15. Artn 97 doi: 10.1186/S12866-015-0433-5.
27. Thibodeau A, Fravalo P, Garneau P, Masson L, Laurent-Lewandowski S, Quessy S, et al. Distribution of Colonization and Antimicrobial Resistance Genes in Campylobacter jejuni Isolated from Chicken. Foodborne Pathog Dis. 2013; 10(4):382-91. doi: 10.1089/fpd.2012.1271.
28. Hutchinson DN, Bolton FJ. Improved Blood Free Selective Medium for the Isolation of Campylobacter Jejuni from Fecal Specimens. J Clin Pathol. 1984; 37(8):956-7. doi: 10.1136/Jcp.37.8.956-B.
29. Thibodeau A, Fravalo P, Laurent-Lewandowski S, Guevremont E, Quessy S, Letellier A. Presence and characterization of Campylobacter jejuni in organically raised chickens in Quebec. Can J Vet Res. 2011; 75(4):298-307.
30. Juteau P, Tremblay D, Villemur R, Bisaillon JG, Beaudet R. Analysis of the bacterial community inhabiting an aerobic thermophilic sequencing batch reactor (AT-SBR) treating swine waste. Appl Microbiol Biot. 2004; 66(1):115-22. doi: 10.1007/s00253-004-1692-5
31. Clifford RJ, Milillo M, Prestwood J, Quintero R, Zurawski DV, Kwak YI, et al. Detection of Bacterial 16S rRNA and Identification of Four Clinically Important Bacteria by Real-Time PCR. Plos One. 2012; 7(11). ARTN e48558 doi: 10.1371/journal.pone.0048558
32. Oh MH, Paek SH, Shin GW, Kim HY, Jung GY, Oh S. Simultaneous Identification of Seven Foodborne Pathogens and Escherichia coli (Pathogenic and Nonpathogenic) Using Capillary Electrophoresis-Based Single-Strand Conformation Polymorphism Coupled with Multiplex PCR. J Food Protect. 2009; 72(6):1262-6.
33. CastilloM, Martin-Orue SM, Manzanilla EG, Badiola I,Martin M, Gasa J. Quantification of total bacteria, enterobacteria and lactobacilli populations in pig digesta by real-Time PCR. VetMicrobiol. 2006; 114(1-2): 165-70. doi: 10.1016/j.vetmic.2005.11.055
34. Matsuki T, Watanabe K, Fujimoto J, Kado Y, Takada T, Matsumoto K, et al. Quantitative PCR with 16S rRNA-Gene-Targeted species-specific primers for analysis of human intestinal bifidobacteria. Appl Environ Microb. 2004; 70(1):167-73. doi: 10.1128/Aem.70.1.167-173.2004
35. Sanschagrin S, Yergeau E. Next-generation Sequencing of 16S Ribosomal RNA Gene Amplicons. Jove-J Vis Exp. 2014;(90: ). ARTN e51709 doi: 10.3791/51709
36. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities. Appl Environ Microb. 2009; 75(23):7537-41. doi: 10.1128/Aem.01541-09
37. Huse SM, Welch DM, Morrison HG, Sogin ML. Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ Microbiol. 2010; 12(7):1889-98. doi: 10.1111/j.1462-2920.2010.02193.x
38. Molatova Z, Skrivanova E, Bare J, Houf K, Bruggeman G, Marounek M. Effect of coated and noncoated fatty acid supplementation on broiler chickens experimentally infected with Campylobacter jejuni. J Anim Physiol an N. 2011; 95(6):701-6. doi: 10.1111/j.1439-0396.2010.01100.x
39. Grilli E, Vitari F, Domeneghini C, Palmonari A, Tosi G, Fantinati P, et al. Development of a feed additive to reduce caecal Campylobacter jejuni in broilers at slaughter age: from in vitro to in vivo, a proof of concept. J Appl Microbiol. 2013; 114(2):308-17. doi: 10.1111/Jam.12053
40. Hermans D, Martel A, Van Deun K, Van Immerseel F, Heyndrickx M, Haesebrouck F, et al. The Cinnamon-Oil Ingredient trans-Cinnamaldehyde Fails To Target Campylobacter jejuni Strain KC 40 in the Broiler Chicken Cecum Despite Marked In Vitro Activity. J Food Protect. 2011; 74(10):1729-34. doi: 10. 4315/0362-028x.Jfp-10-487
41. Videnska P, Sisak F, Havlickova H, Faldynova M, Rychlik I. Influence of Salmonella enterica serovar Enteritidis infection on the composition of chicken cecal microbiota. Bmc Vet Res. 2013; 9. Artn 140 doi: 10.1186/1746-6148-9-140
42. Stanley D, Keyburn AL, Denman SE, Moore RJ. Changes in the caecal microflora of chickens following Clostridium perfringens challenge to induce necrotic enteritis. Vet Microbiol. 2012; 159(1-2):155-62. doi: 10.1016/j.vetmic.2012.03.032
43. Johansen CH, Bjerrum L, Finster K, Pedersen K. Effects of a Campylobacter jejuni infection on the development of the intestinal microflora of broiler chickens. Poultry Sci. 2006; 85(4):579-87.
44. Sofka D, Pfeifer A, Gleiss B, Paulsen P, Hilbert F. Changes within the intestinal flora of broilers by colonisation with Campylobacter jejuni. Berl Munch Tierarztl. 2015; 128(3-4):104-10. doi: 10.2376/0005-9366-128-104
45. Kaakoush NO, Sodhi N, Chenu JW, Cox JM, Riordan SM, Mitchell HM. The interplay between Campylobacter and Helicobacter species and other gastrointestinal microbiota of commercial broiler chickens. Gut Pathog. 2014; 6. Artn 18 doi: 10.1186/1757-4749-6-18.
46. Skanseng B, Kaldhusdal M, Rudi K. Comparison of chicken gut colonisation by the pathogens Campylobacter jejuni and Clostridium perfringens by real-Time quantitative PCR. Mol Cell Probe. 2006; 20(5):269-79. doi: 10.1016/j.mcp.2006.02.001
47. Line JE, Hiett KL, Guard-Bouldin J, Seal BS. Differential carbon source utilization by Campylobacter jejuni 11168 in response to growth temperature variation. J Microbiol Meth. 2010; 80(2):198-202. doi: 10.1016/j.mimet.2009.12.011
48. 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 Micr. 2012; 62:144-9. doi: 10.1099/Ijs.0.026989-0
49. 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 Micr. 2002; 52:2141-6.
50. Hansen AK, Hansen CHF, Krych L, Nielsen DS. Impact of the gut microbiota on rodent models of human disease. World J Gastroentero. 2014; 20(47):17727-36.
51. Duncan SH, Holtrop G, Lobley GE, Calder AG, Stewart CS, Flint HJ. Contribution of acetate to butyrate formation by human faecal bacteria. Brit J Nutr. 2004; 91(6):915-23.
52. Van Deun K, Pasmans F, Van Immerseel F, Ducatelle R, Haesebrouck F. Butyrate protects Caco-2 cells from Campylobacter jejuni invasion and translocation. Brit J Nutr. 2008; 100(3):480-4. doi: 10.1017/S0007114508921693
53. Wrzosek L, Miquel S, Noordine ML, Bouet S, Chevalier-Curt MJ, Robert V, et al. Bacteroides thetaiotaomicron and Faecalibacterium prausnitzii influence the production of mucus glycans and the development of goblet cells in the colonic epithelium of a gnotobiotic model rodent. Bmc Biol. 2013; 11. Artn 61 doi: 10.1186/1741-7007-11-61.
54. Mookiah S, Sieo CC, Ramasamy K, Abdullah N, Ho YW. Effects of dietary prebiotics, probiotic and synbiotics on performance, caecal bacterial populations and caecal fermentation concentrations of broiler chickens. J Sci Food Agr. 2014; 94(2):341-8. doi: 10.1002/Jsfa.6365
55. Ding W, Wang HF, Griffiths MW. Problotics down-regulate flaA sigma(28) promoter in Campylobacter jejuni. J Food Protect. 2005; 68(11):2295-300.
56. Santini C, Baffoni L, Gaggia F, Granata M, Gasbarri R, Di Gioia D, et al. Characterization of probiotic strains: An application as feed additives in poultry against Campylobacter jejuni. Int J Food Microbiol. 2010; 141:S98-S108. doi: 10.1016/j.ijfoodmicro.2010.03.039
57. Messier S, Quessy S, Robinson Y, Devriese LA, Hommez J, Fairbrother JM. Focal Dermatitis and Cellulitis in Broiler-Chickens-Bacteriological and Pathological Findings. Avian Dis. 1993; 37(3):839-44. doi: 10.2307/1592039
58. Tiihonen K, Kettunen H, Bento MHL, Saarinen M, Lahtinen S, Ouwehand AC, et al. The effect of feeding essential oils on broiler performance and gut microbiota. Brit Poultry Sci. 2010; 51(3):381-92. Pii 925013654 doi: 10.1080/00071668.2010.496446
59. Cross DE, McDevitt RM, Hillman K, Acamovic T. The effect of herbs and their associated essential oils on performance, dietary digestibility and gut microflora in chickens from 7 to 28 days of age. Brit Poultry Sci. 2007; 48(4):496-506. doi: 10.1080/00071660701463221.
60. Boroojeni FG, Vahjen W, Mader A, Knorr F, Ruhnke I, Rohe I, et al. The effects of different thermal treatments and organic acid levels in feed on microbial composition and activity in gastrointestinal tract of broilers. Poultry Sci. 2014; 93(6):1440-52. doi: 10.3382/ps.2013-03763