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

BMC Veterinary Research

Volumn 9, Issue , 2013, Pages

  Videnska, Petra ^a   Sisak, Frantisek ^a   Havlickova, Hana ^a   Faldynova, Marcela ^a   Rychlik, Ivan ^a  

^a VETERINARY RESEARCH INSTITUTE   (Czech Republic)

Author keywords

Chicken; Intestinal tract; Microbiome; Pyrosequencing; Salmonella

Indexed keywords

ENTEROBACTERIACEAE; GALLUS GALLUS; LACHNOSPIRACEAE; LACTOBACILLACEAE; SALMONELLA; SALMONELLA ENTERICA; SALMONELLA ENTERITIDIS;

RNA 16S;

ANIMAL; ANIMAL SALMONELLOSIS; BIRD DISEASE; CECUM; CHICKEN; GENETICS; LACTOBACILLUS; MALE; MICROBIOLOGY; MICROFLORA; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR ENTERITIDIS; VETERINARY; ANIMAL DISEASE; ARTICLE; SALMONELLA ENTERITIDIS;

ANIMALS; CECUM; CHICKENS; LACTOBACILLUS; MALE; MICROBIOTA; POULTRY DISEASES; REAL-TIME POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; SALMONELLA ENTERITIDIS; SALMONELLA INFECTIONS, ANIMAL;

EID: 84880097532     PISSN: None     EISSN: 17466148     Source Type: Journal    
DOI: 10.1186/1746-6148-9-140     Document Type: Article

References (39)

1. Gaboriau-Routhiau V, Rakotobe S, Lecuyer E, Mulder I, Lan A, Bridonneau C, Rochet V, Pisi A, De Paepe M, Brandi G, et al. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity 2009, 31:677-689. 10.1016/j.immuni.2009.08.020, 19833089.
2. Hill DA, Hoffmann C, Abt MC, Du Y, Kobuley D, Kirn TJ, Bushman FD, Artis D. Metagenomic analyses reveal antibiotic-induced temporal and spatial changes in intestinal microbiota with associated alterations in immune cell homeostasis. Mucosal Immunol 2010, 3:148-158. 10.1038/mi.2009.132, 2824244, 19940845.
3. Ismail AS, Behrendt CL, Hooper LV. Reciprocal interactions between commensal bacteria and gamma delta intraepithelial lymphocytes during mucosal injury. J Immunol 2009, 182:3047-3054. 10.4049/jimmunol.0802705, 2763635, 19234201.
4. Lillehoj HS. Avian gut-associated immune system: implication in coccidial vaccine development. Poult Sci 1993, 72:1306-1311. 10.3382/ps.0721306, 8346157.
5. Lu J, Idris U, Harmon B, Hofacre C, Maurer JJ, Lee MD. Diversity and succession of the intestinal bacterial community of the maturing broiler chicken. Appl Environ Microbiol 2003, 69:6816-6824. 10.1128/AEM.69.11.6816-6824.2003, 262306, 14602645.
6. Zhu XY, Zhong T, Pandya Y, Joerger RD. 16S rRNA-based analysis of microbiota from the cecum of broiler chickens. Appl Environ Microbiol 2002, 68:124-137. 10.1128/AEM.68.1.124-137.2002, 126585, 11772618.
7. O'Toole PW, Claesson MJ. Gut microbiota: Changes throughout the lifespan from infancy to elderly. Int Dairy J 2010, 20:281-291.
8. Dethlefsen L, Huse S, Sogin ML, Relman DA. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol 2008, 6:e280. 10.1371/journal.pbio.0060280, 2586385, 19018661.
9. Lofmark S, Jernberg C, Jansson JK, Edlund C. Clindamycin-induced enrichment and long-term persistence of resistant Bacteroides spp. and resistance genes. J Antimicrob Chemother 2006, 58:1160-1167. 10.1093/jac/dkl420, 17046967.
10. Robinson CJ, Young VB. Antibiotic administration alters the community structure of the gastrointestinal micobiota. Gut Microbes 2010, 1:279-284. 10.4161/gmic.1.4.12614, 2954510,2954510, 20953272.
11. Videnska P, Faldynova M, Juricova H, Babak V, Sisak F, Havlickova H, Rychlik I. Chicken faecal microbiota and disturbances induced by single or repeated therapy with tetracycline and streptomycin. BMC Vet Res 2013, 9:30. 10.1186/1746-6148-9-30, 3598895, 23406343.
12. Hoffmann C, Hill DA, Minkah N, Kirn T, Troy A, Artis D, Bushman F. Community-wide response of the gut microbiota to enteropathogenic Citrobacter rodentium infection revealed by deep sequencing. Infect Immun 2009, 77:4668-4678. 10.1128/IAI.00493-09, 2747949, 19635824.
13. Lupp C, Robertson ML, Wickham ME, Sekirov I, Champion OL, Gaynor EC, Finlay BB. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe 2007, 2:119-129. 10.1016/j.chom.2007.06.010, 18005726.
14. Manichanh C, Rigottier-Gois L, Bonnaud E, Gloux K, Pelletier E, Frangeul L, Nalin R, Jarrin C, Chardon P, Marteau P, et al. Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach. Gut 2006, 55:205-211. 10.1136/gut.2005.073817, 1856500, 16188921.
15. Barman M, Unold D, Shifley K, Amir E, Hung K, Bos N, Salzman N. Enteric salmonellosis disrupts the microbial ecology of the murine gastrointestinal tract. Infect Immun 2008, 76:907-915. 10.1128/IAI.01432-07, 2258829, 18160481.
16. Juricova H, Videnska P, Lukac M, Faldynova M, Babak V, Havlickova H, Sisak F, Rychlik I. Influence of Salmonella enterica serovar Enteritidis infection on the development of cecum microbiota in newly hatched chicks. Appl Environ Microbiol 2013, 79:745-7. 10.1128/AEM.02628-12, 3553771, 23144133.
17. Stecher B, Robbiani R, Walker AW, Westendorf AM, Barthel M, Kremer M, Chaffron S, Macpherson AJ, Buer J, Parkhill J, et al. Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol 2007, 5:2177-2189. 1951780, 17760501.
18. Thiennimitr P, Winter SE, Baumler AJ. Salmonella, the host and its microbiota. Curr Opin Microbiol 2012, 15:108-114. 10.1016/j.mib.2011.10.002, 3265626, 22030447.
19. Santos RL, Raffatellu M, Bevins CL, Adams LG, Tukel C, Tsolis RM, Baumler AJ. Life in the inflamed intestine, Salmonella style. Trends Microbiol 2009, 17:498-506. 10.1016/j.tim.2009.08.008, 3235402, 19819699.
20. Raffatellu M, George MD, Akiyama Y, Hornsby MJ, Nuccio SP, Paixao TA, Butler BP, Chu H, Santos RL, Berger T, et al. Lipocalin-2 resistance confers an advantage to Salmonella enterica serotype Typhimurium for growth and survival in the inflamed intestine. Cell Host Microbe 2009, 5:476-486. 10.1016/j.chom.2009.03.011, 2768556, 19454351.
21. Winter SE, Thiennimitr P, Winter MG, Butler BP, Huseby DL, Crawford RW, Russell JM, Bevins CL, Adams LG, Tsolis RM, et al. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 2010, 467:426-429. 10.1038/nature09415, 2946174, 20864996.
22. Berndt A, Wilhelm A, Jugert C, Pieper J, Sachse K, Methner U. Chicken cecum immune response to Salmonella enterica serovars of different levels of invasiveness. Infect Immun 2007, 75:5993-6007. 10.1128/IAI.00695-07, 2168364, 17709416.
23. Crhanova M, Hradecka H, Faldynova M, Matulova M, Havlickova H, Sisak F, Rychlik I. Immune response of chicken gut to natural colonization by gut microflora and to Salmonella enterica serovar Enteritidis infection. Infect Immun 2011, 79:2755-2763. 10.1128/IAI.01375-10, 3191970, 21555397.
24. Matulova M, Rajova J, Vlasatikova L, Volf J, Stepanova H, Havlickova H, Sisak F, Rychlik I. Characterization of chicken spleen transcriptome after infection with Salmonella enterica serovar Enteritidis. PLoS One 2012, 7:e48101. 10.1371/journal.pone.0048101, 3477135, 23094107.
25. Danzeisen JL, Kim HB, Isaacson RE, Tu ZJ, Johnson TJ. Modulations of the chicken cecal microbiome and metagenome in response to anticoccidial and growth promoter treatment. PLoS One 2011, 6:e27949. 10.1371/journal.pone.0027949, 3218064, 22114729.
26. Beal RK, Powers C, Wigley P, Barrow PA, Smith AL. Temporal dynamics of the cellular, humoral and cytokine responses in chickens during primary and secondary infection with Salmonella enterica serovar Typhimurium. Avian Pathol 2004, 33:25-33. 10.1080/03079450310001636282, 14681065.
27. Withanage GS, Wigley P, Kaiser P, Mastroeni P, Brooks H, Powers C, Beal R, Barrow P, Maskell D, McConnell I. Cytokine and chemokine responses associated with clearance of a primary Salmonella enterica serovar Typhimurium infection in the chicken and in protective immunity to rechallenge. Infect Immun 2005, 73:5173-5182. 10.1128/IAI.73.8.5173-5182.2005, 1201213, 16041035.
28. Endt K, Stecher B, Chaffron S, Slack E, Tchitchek N, Benecke A, Van Maele L, Sirard JC, Mueller AJ, Heikenwalder M, et al. The microbiota mediates pathogen clearance from the gut lumen after non-typhoidal Salmonella diarrhea. PLoS Pathog 2010, 6:e1001097. 10.1371/journal.ppat.1001097, 2936549, 20844578.
29. Hoszowski A, Truszczynski M. Prevention of Salmonella typhimurium caecal colonisation by different preparations for competitive exclusion. Comp Immunol Microbiol Infect Dis 1997, 20:111-117. 10.1016/S0147-9571(96)00042-2, 9208196.
30. Methner U, Barrow PA, Martin G, Meyer H. 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 1997, 35:223-230. 10.1016/S0168-1605(96)01236-6, 9105931.
31. Methner U, Barrow PA, Berndt A, Steinbach G. Combination of vaccination and competitive exclusion to prevent Salmonella colonization in chickens: experimental studies. Int J Food Microbiol 1999, 49:35-42. 10.1016/S0168-1605(99)00051-3, 10477068.
32. Barrow PA. Further observations on the effect of feeding diets containing avoparcin on the excretion of salmonellas by experimentally infected chickens. Epidemiol Infect 1989, 102:239-252. 10.1017/S0950268800029915, 2249444, 2522883.
33. Croswell A, Amir E, Teggatz P, Barman M, Salzman NH. Prolonged impact of antibiotics on intestinal microbial ecology and susceptibility to enteric Salmonella infection. Infect Immun 2009, 77:2741-2753. 10.1128/IAI.00006-09, 2708550, 19380465.
34. Sekirov I, Tam NM, Jogova M, Robertson ML, Li Y, Lupp C, Finlay BB. Antibiotic-induced perturbations of the intestinal microbiota alter host susceptibility to enteric infection. Infect Immun 2008, 76:4726-4736. 10.1128/IAI.00319-08, 2546810, 18678663.
35. Nordentoft S, Molbak L, Bjerrum L, De Vylder J, Van Immerseel F, Pedersen K. The influence of the cage system and colonisation of Salmonella Enteritidis on the microbial gut flora of laying hens studied by T-RFLP and 454 pyrosequencing. BMC Microbiol 2011, 11:187. 10.1186/1471-2180-11-187, 3188488, 21859465.
36. Rychlik I, Karasova D, Sebkova A, Volf J, Sisak F, Havlickova H, Kummer V, Imre A, Szmolka A, Nagy B. Virulence potential of five major pathogenicity islands (SPI-1 to SPI-5) of Salmonella enterica serovar Enteritidis for chickens. BMC Microbiol 2009, 9:268. 10.1186/1471-2180-9-268, 2803193, 20021686.
37. Nossa CW, Oberdorf WE, Yang L, Aas JA, Paster BJ, Desantis TZ, Brodie EL, Malamud D, Poles MA, Pei Z. Design of 16S rRNA gene primers for 454 pyrosequencing of the human foregut microbiome. World J Gastroenterol 2010, 16:4135-4144. 10.3748/wjg.v16.i33.4135, 2932916, 20806429.
38. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010, 7:335-336. 10.1038/nmeth.f.303, 3156573, 20383131.
39. Lozupone C, Knight R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 2005, 71:8228-8235. 10.1128/AEM.71.12.8228-8235.2005, 1317376, 16332807.