Lactobacillus strain ecology and persistence within broiler chickens fed different diets: Identification of persistent strains

Applied and Environmental Microbiology

Volumn 76, Issue 19, 2010, Pages 6494-6503

  Stephenson, David P ^a   Moore, Robert J ^b   Allison, Gwen E ^a,c  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b CSIRO   (Australia)

^c The Australian National University   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BROILER CHICKENS; CONSENSUS SEQUENCE; DELIVERY VEHICLE; ERIC-PCR; EXCLUSION AGENTS; GASTROINTESTINAL TRACT; IN-VIVO; LACTIC ACID BACTERIA; LACTOBACILLUS STRAINS; PROBIOTICS;

ANIMALS; BACTERIOLOGY; BODY FLUIDS; ECOLOGY; LACTIC ACID; NUTRITION; PROTEINS;

STRAIN;

BACTERIAL DNA;

BACTERIUM; COLONIZATION; DIET; DRUG RESISTANCE; GENETIC MARKER; PERSISTENCE; POLYMERASE CHAIN REACTION; POULTRY; PROBIOTICS; PROTEIN;

ANIMAL; ARTICLE; BACTERIUM IDENTIFICATION; BIODIVERSITY; CHICKEN; CLASSIFICATION; DIET; DNA FINGERPRINTING; GASTROINTESTINAL TRACT; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; LACTOBACILLUS; MICROBIOLOGY; RANDOM AMPLIFIED POLYMORPHIC DNA;

ANIMALS; BACTERIAL TYPING TECHNIQUES; BIODIVERSITY; CHICKENS; DIET; DNA FINGERPRINTING; DNA, BACTERIAL; GASTROINTESTINAL TRACT; LACTOBACILLUS; RANDOM AMPLIFIED POLYMORPHIC DNA TECHNIQUE;

BACTERIA (MICROORGANISMS); ENTEROBACTERIACEAE; GALLUS GALLUS; LACTOBACILLUS; LACTOBACILLUS AGILIS; LACTOBACILLUS CRISPATUS; LACTOBACILLUS VAGINALIS;

EID: 78049252737     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01137-10     Document Type: Article

References (57)

1. Abbas Hilmi, H. T., A. Surakka, J. Apajalahti, and P. E. Saris. 2007. Identification of the most abundant Lactobacillus species in the crop of 1- and 5-week-old broiler chickens. Appl. Environ. Microbiol. 73:7867-7873.
2. Amit-Romach, E., D. Sklan, and Z. Uni. 2004. Microflora ecology of the chicken intestine using 16S ribosomal DNA primers. Poult. Sci. 83:1093-1098.
3. Apajalahti, J., A. Kettunen, and H. Graham. 2004. Characteristics of the gastrointestinal microbial communities, with special reference to the chicken. Worlds Poult. Sci. J. 60:223-232.
4. Apajalahti, J. H. 2004. Structure and dietary modulation of intestinal microbial communities, p. 69-76. In Proceedings of the Second Mid- Atlantic Nutrition Conference. University of Maryland, College Park, MD.
5. Barnes, E. M., G. C. Mead, and D. A. Barnum. 1972. The intestinal flora of the chicken in the period 2 to 6 weeks of age, with particular reference to the anaerobic bacteria. Br. Poult. Sci. 13:617-622.
6. Berlec, A., and B. Štrukelj. 2009. Novel applications of recombinant lactic acid bacteria in therapy and in metabolic engineering. Recent Pat. Biotechnol. 3:77-87.
7. Bjerrum, L., R. M. Engberg, T. D. Leser, B. B. Jensen, K. Finster, and K. Pedersen. 2006. Microbial community composition of the ileum and cecum of broiler chickens as revealed by molecular and culture-based techniques. Poult. Sci. 85:1151-1164.
8. Bouzaine, T., R. D. Dauphin, P. Thonart, M. C. Urdaci, and M. Hamdi. 2005. Adherence and colonization properties of Lactobacillus rhamnosus TB1, a broiler chicken isolate. Lett. Appl. Microbiol. 40:391-396.
9. Casewell, M., C. Friis, E. Marco, P. McMullin, and I. Phillips. 2003. The European ban on growth-promoting antibiotics and emerging consequences for human and animal health. J. Antimicrob. Chemother. 52:159-161.
10. da Costa, P. M., M. Oliveira, A. Bica, P. Vaz-Pires, and F. Bernardo. 2007. Antimicrobial resistance in Enterococcus spp. and Escherichia coli isolated from poultry feed and feed ingredients. Vet. Microbiol. 120:122-131.
11. Dahiya, J. P., D. Hoehler, D. C. Wilkie, A. G. Van Kessel, and M. D. Drew. 2005. Dietary glycine concentration affects intestinal Clostridium perfringens and lactobacilli populations in broiler chickens. Poult. Sci. 84:1875-1885.
12. Danielsen, M., P. J. Simpson, E. B. O'Connor, R. P. Ross, and C. Stanton. 2007. Susceptibility of Pediococcus spp. to antimicrobial agents. J. Appl. Microbiol. 102:384-389.
13. Danielsen, M., and A. Wind. 2003. Susceptibility of Lactobacillus spp. to antimicrobial agents. Int. J. Food Microbiol. 82:1-11.
14. Decroos, K., T. Vercauteren, G. Werquin, and W. Verstraete. 2004. Repression of Clostridium population in young broiler chickens after administration of a probiotic mixture. Commun. Agric. Appl. Biol. Sci. 69:5-13.
15. Dumonceaux, T. J., J. E. Hill, S. M. Hemmingsen, and A. G. Van Kessel. 2006. Characterization of intestinal microbiota and response to dietary virginiamycin supplementation in the broiler chicken. Appl. Environ. Microbiol. 72:2815-2823.
16. Ehrmann, M. A., P. Kurzak, J. Bauer, and R. F. Vogel. 2002. Characterization of lactobacilli towards their use as probiotic adjuncts in poultry. J. Appl. Microbiol. 92:966-975.
17. Engberg, R. M., M. S. Hedemann, T. D. Leser, and B. B. Jensen. 2000. Effect of zinc bacitracin and salinomycin on intestinal microflora and performance of broilers. Poult. Sci. 79:1311-1319.
18. Foulquié Moreno, M. R., P. Sarantinopoulos, E. Tsakalidou, and L. De Vuyst. 2006. The role and application of enterococci in food and health. Int. J. Food Microbiol. 106:1-24.
19. Frece, J., B. Kos, J. Beganović, S. Vuković, and J. Šušković. 2005. In vivo testing of functional properties of three selected probiotic strains. World J. Microbiol. Biotechnol. 21:1401-1408.
20. Fujiwara, S., Y. Seto, A. Kimura, and H. Hashiba. 2001. Establishment of orally-administered Lactobacillus gasseri SBT2055SR in the gastrointestinal tract of humans and its influence on intestinal microflora and metabolism. J. Appl. Microbiol. 90:343-352.
21. Fuller, R., and A. Turvey. 1971. Bacteria associated with the intestinal wall of the fowl (Gallus domesticus). J. Appl. Bacteriol. 34:617-622.
22. Gardiner, G. E., P. G. Casey, G. Casey, P. B. Lynch, P. G. Lawlor, C. Hill, G. F. Fitzgerald, C. Stanton, and R. P. Ross. 2004. Relative ability of orally administered Lactobacillus murinus to predominate and persist in the porcine gastrointestinal tract. Appl. Environ. Microbiol. 70:1895-1906.
23. Garriga, M., M. Pascual, J. M. Monfort, and M. Hugas. 1998. Selection of lactobacilli for chicken probiotic adjuncts. J. Appl. Microbiol. 84:125-132.
24. Geier, M. S., V. A. Torok, G. E. Allison, K. Ophel-Keller, and R. J. Hughes. 2009. Indigestible carbohydrates alter the intestinal microbiota but do not influence the performance of broiler chickens. J. Appl. Microbiol. 106:1540-1548.
25. Gérard, P., C. Brézillon, F. Quéré, A. Salmon, and S. Rabot. 2008. Characterization of cecal microbiota and response to an orally administered Lactobacillus probiotic strain in the broiler chicken. J. Mol. Microbiol. Biotechnol. 14:115-122.
26. Gong, J., W. Si, R. J. Forster, R. Huang, H. Yu, Y. Yin, C. Yang, and Y. Han. 2007. 16S rRNA gene-based analysis of mucosa-associated bacterial community and phylogeny in the chicken gastrointestinal tracts: from crops to ceca. FEMS Microbiol. Ecol. 59:147-157.
27. Gong, J., H. Yu, T. Liu, J. J. Gill, J. R. Chambers, R. Wheatcroft, and P. M. Sabour. 2008. Effects of zinc bacitracin, bird age and access to range on bacterial microbiota in the ileum and caeca of broiler chickens. J. Appl. Microbiol. 104:1372-1382.
28. Guan, L. L., K. E. Hagen, G. W. Tannock, D. R. Korver, G. M. Fasenko, and G. E. Allison. 2003. Detection and identification of Lactobacillus species in crops of broilers of different ages by using PCR-denaturing gradient gel electrophoresis and amplified ribosomal DNA restriction analysis. Appl. Environ. Microbiol. 69:6750-6757.
29. Hautefort, I., B. Flechon, J. Degrouard, and M. Fons. 2000. Adhesion to the digestive mucosa is not sufficient for durable persistence of different Lactobacillus fermentum strains in the digestive tract of mice. Microb. Ecol. Health Dis. 12:48-56.
30. Jin, L. Z., Y. W. Ho, M. A. Ali, N. Abdullah, K. B. Ong, and S. Jalaludin. 1996. Adhesion of Lactobacillus isolates to intestinal epithelial cells of chicken. Lett. Appl. Microbiol. 22:229-232. (Pubitemid 26083318)
31. Kizerwetter-Świda, M., and M. Binek. 2009. Protective effect of potentially probiotic Lactobacillus strain on infection with pathogenic bacteria in chickens. Pol. J. Vet. Sci. 12:15-20.
32. Kizerwetter-Świda, M., and M. Binek. 2005. Selection of potentially probiotic Lactobacillus strains towards their inhibitory activity against poultry enteropathogenic bacteria. Pol. J. Microbiol. 54:287-294.
33. Knarreborg, A., M. A. Simon, R. M. Engberg, B. B. Jensen, and G. W. Tannock. 2002. Effects of dietary fat source and subtherapeutic levels of antibiotic on the bacterial community in the ileum of broiler chickens at various ages. Appl. Environ. Microbiol. 68:5918-5924.
34. Koenen, M. E., R. Van Der Hulst, M. Leering, S. H. M. Jeurissen, and W. J. A. Boersma. 2004. Development and validation of a new in vitro assay for selection of probiotic bacteria that express immune-stimulating properties in chickens in vivo. FEMS Immunol. Med. Microbiol. 40:119-127.
35. Kulkarni, R. R., V. R. Parreira, Y. F. Jiang, and J. F. Prescott. 2010. A live oral recombinant Salmonella enterica serovar Typhimurium vaccine expressing Clostridium perfringens antigens confers protection against necrotic enteritis in broiler chickens. Clin. Vaccine Immunol. 17:205-214.
36. Lan, P. T., T. Binh Le, and Y. Benno. 2003. Impact of two probiotic Lactobacillus strains feeding on fecal lactobacilli and weight gains in chicken. J. Gen. Appl. Microbiol. 49:29-36.
37. La Ragione, R. M., A. Narbad, M. J. Gasson, and M. J. Woodward. 2004. In vivo characterization of Lactobacillus johnsonii FI9785 for use as a defined competitive exclusion agent against bacterial pathogens in poultry. Lett. Appl. Microbiol. 38:197-205.
38. Lu, J., U. Idris, B. Harmon, C. Hofacre, J. J. Maurer, and M. D. Lee. 2003.Diversity and succession of the intestinal bacterial community of the maturing broiler chicken. Appl. Environ. Microbiol. 69:6816-6824.
39. Matijašić, B. B., S. Stojković, and I. Rogelj. 2006. Survival and in vivo adhesion of human isolates Lactobacillus gasseri LF221 and K7 in weaned piglets and their effects on coliforms, clostridia and lactobacilli viable counts in faeces and mucosa. J. Dairy Res. 73:417-422.
40. Mead, G. C. 1997. Bacteria in the gastrointestinal tract of birds, p. 216-240. In R. I. Mackie, B. A. White, and R. E. Isaacson (ed.), Gastrointestinal microbiology, vol. 2. Gastrointestinal microbes and host interactions. Chapman and Hall, New York, NY.
41. Murphy, L., C. Dunne, B. Kiely, F. Shanahan, G. C. O'Sullivan, and J. K. Collins. 1999. In vivo assessment of potential probiotic Lactobacillus salivarius strains: evaluation of their establishment, persistence, and localisation in the murine gastrointestinal tract. Microb. Ecol. Health Dis. 11:149-157.
42. Pascual, M., M. Hugas, J. I. Badiola, J. M. Monfort, and M. Garriga. 1999. Lactobacillus salivarius CTC2197 prevents Salmonella enteritidis colonization in chickens. Appl. Environ. Microbiol. 65:4981-4986.
43. Rada, V., and M. Marounek. 1997. Effect of maduramicin and monensin on survival of Lactobacillus salivarius 51R administered in the crop and caeca of young chickens. Arch. Tierernahr. 50:25-29.
44. Shin, J. W., J. K. Kang, K. I. Jang, and K. Y. Kim. 2002. Intestinal colonization characteristics of Lactobacillus spp. isolated from chicken cecum and competitive inhibition against Salmonella typhimurium. J. Microbiol. Biotechnol. 12:576-582.
45. Shinoda, T., D. Kusuda, Y. Ishida, N. Ikeda, K. Kaneko, O. Masuda, and N. Yamamoto. 2001. Survival of Lactobacillus helveticus strain CP53 in the human gastrointestinal tract. Lett. Appl. Microbiol. 32:108-113.
46. Sieo, C. C., N. Abdullah, W. S. Tan, and Y. W. Ho. 2006. In vivo study on the persistence of transformed'-glucanase-producing Lactobacillus strains in the gastrointestinal tract of chickens. J. Anim. Feed Sci. 15:261-274.
47. Smulikowska, S., K. Ś lizewska, J. Biernasiak, A. Mieczkowska, and P. Michałowski. 2005. The effect of a probiotic composed of Lactobacillus and yeasts, and of flavomycin on the performance and faecal microflora of broiler chickens. J. Anim. Feed Sci. 14:483-485.
48. Stephenson, D. P., R. J. Moore, and G. E. Allison. 2009. Comparison and utilization of repetitive-element PCR techniques for typing Lactobacillus isolates from the chicken gastrointestinal tract. Appl. Environ. Microbiol. 75:6764-6776.
49. Taheri, H. R., H. Moravej, F. Tabandeh, M. Zaghari, and M. Shivazad. 2009. Screening of lactic acid bacteria toward their selection as a source of chicken probiotic. Poult. Sci. 88:1586-1593.
50. Timmerman, H. M., C. J. M. Koning, L. Mulder, F. M. Rombouts, and A. C. Beynen. 2004. Monostrain, multistrain and multispecies probiotics-a comparison of functionality and efficacy. Int. J. Food Microbiol. 96:219-233.
51. Van Immerseel, F., J. I. Rood, R. J. Moore, and R. W. Titball. 2009. Rethinking our understanding of the pathogenesis of necrotic enteritis in chickens. Trends Microbiol. 17:32-36.
52. Walter, J. 2008. Ecological role of lactobacilli in the gastrointestinal tract: implications for fundamental and biomedical research. Appl. Environ. Microbiol. 74:4985-4996.
53. Wells, J. M., and A. Mercenier. 2008. Mucosal delivery of therapeutic and prophylactic molecules using lactic acid bacteria. Nat. Rev. Microbiol. 6:349-362.
54. Wise, M. G., and G. R. Siragusa. 2007. Quantitative analysis of the intestinal bacterial community in one- to three-week-old commercially reared broiler chickens fed conventional or antibiotic-free vegetable-based diets. J. Appl. Microbiol. 102:1138-1149.
55. Yu, B., J. R. Liu, F. S. Hsiao, T. T. Lee, and P. W. S. Chiou. 2008. The probiotic and adherence properties of Lactobacillus reuteri Pg4 expressing the rumen microbial β-glucanase. Asian-australas. J. Anim. Sci. 21:1324-1329.
56. Yu, Q. H., S. M. Dong, W. Y. Zhu, and Q. Yang. 2007. Use of green fluorescent protein to monitor Lactobacillus in the gastro-intestinal tract of chicken. FEMS Microbiol. Lett. 275:207-213.
57. Zekarias, B., H. Mo, and R. Curtiss III. 2008. Recombinant attenuated Salmonella enterica serovar typhimurium expressing the carboxy-terminal domain of alpha toxin from Clostridium perfringens induces protective responses against necrotic enteritis in chickens. Clin. Vaccine Immunol. 15: 805-816.