Effect of carbohydrate composition in barley and oat cultivars on microbial ecophysiology and proliferation of Salmonella enterica in an in vitro model of the porcine gastrointestinal tract

Applied and Environmental Microbiology

Volumn 75, Issue 22, 2009, Pages 7006-7016

  Pieper, Robert ^a,b,e   Bindelle, Jérôme ^a,b,c,d   Rossnagel, Brian ^a   Van Kessel, Andrew ^a   Leterme, Pascal ^b  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b PRAIRIE SWINE CENTRE INC   (Canada)

^c UNIVERSITY OF LIÈGE   (Belgium)

^d FNRS   (Belgium)

^e FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOPECTINS; CARBOHYDRATES; CLOSTRIDIUM; CLUSTER ANALYSIS; CYCLODEXTRINS; ECOLOGY; FERMENTATION; GAS CHROMATOGRAPHY; MAMMALS; PHYSIOLOGY; POLYMERASE CHAIN REACTION; SALMONELLA; VOLATILE FATTY ACIDS;

CARBOHYDRATE COMPOSITIONS; CLOSTRIDIUM BUTYRICUM; FERMENTATION KINETICS; GASTROINTESTINAL TRACT; MICROBIAL COMMUNITY COMPOSITION; NON-STARCH POLYSACCHARIDES; SHORT-CHAIN FATTY ACIDS; TERMINAL RESTRICTION FRAGMENT LENGTH POLYMORPHISMS;

PLANTS (BOTANY);

AMYLOPECTIN; AMYLOSE; BETA GLUCAN; GENOMIC DNA; RNA 16S; SHORT CHAIN FATTY ACID; STARCH;

BACTERIUM; BARLEY; CARBOHYDRATE; CHEMICAL COMPOSITION; CLUSTER ANALYSIS; CULTIVAR; DIGESTIVE SYSTEM; ECOPHYSIOLOGY; GAS CHROMATOGRAPHY; HOST-PATHOGEN INTERACTION; HYDROLYSIS; MICROBIAL COMMUNITY; PIG; PROTEIN; REACTION KINETICS;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL STRAIN; BACTEROIDES; BARLEY; CARBOHYDRATE ANALYSIS; CLOSTRIDIUM; CONTROLLED STUDY; CULTIVAR; ECOPHYSIOLOGY; FERMENTATION; GAS CHROMATOGRAPHY; GASTROINTESTINAL TRACT; GENE SEQUENCE; IN VITRO STUDY; INTESTINE FLORA; MICROBIAL COMMUNITY; MICROFLORA; NONHUMAN; NUCLEOTIDE SEQUENCE; OAT; POLYMERASE CHAIN REACTION; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; RUMINOCOCCUS FLAVEFACIENS; SALMONELLA ENTERICA; SWINE;

AVENA; BACTERIA (MICROORGANISMS); BACTEROIDES; CLOSTRIDIUM; CLOSTRIDIUM BUTYRICUM; CLOSTRIDIUM RAMOSUM; CLOSTRIDIUM XYLANOLYTICUM; HORDEUM; RUMINOCOCCUS FLAVEFACIENS; SALMONELLA; SALMONELLA ENTERICA; SUIDAE; SUS;

EID: 70449364997     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01343-09     Document Type: Article

References (42)

1. Aabo, S., O. F. Rasmussen, I. Rossen, P. D. Sørensen, and J. E. Olsen. 1993. Salmonella identification by the polymerase chain reaction. Mol. Cell. Probes 7:171-178.
2. Awati, A., B. A. Williams, M. W. Bosch, Y. C. Li, and M. W. A. Verstegen. 2006. Use of the in vitro cumulative gas production technique for pigs: an examination of alterations in fermentation products and substrate losses at various time points. J. Anim. Sci. 84:1110-1118.
3. Barcenilla, A., S. E. Pryde, J. C. Martin, S. H. Duncan, C. S. Stewart, C. Henderson, and H. J. Flint. 2000. Phylogenetic relationships of butyrate-producing bacteria from the human gut. Appl. Environ. Microbiol. 66:1654-1661.
4. Bauer, E., B. A. Williams, C. Voigt, R. Mosenthin, and W. M. A. Verstegen. 2001. Microbial activities of faeces from unweaned and adult pigs, in relation to selected fermentable carbohydrates. Anim. Sci. 73:313-322.
5. Bindelle, J., A. Buldgen, C. Boudry, and P. Leterme. 2007. Effect of inoculum and pepsin-pancreatin hydrolysis on fibre fermentation measured by the gas production technique in pigs. Anim. Feed Sci. Technol. 132:111-122.
6. Brennan, C. S., and L. J. Cleary. 2005. The potential use of cereal (1→3,1→4)-β glucans as functional food ingredients. J. Cereal Sci. 42:1-13.
7. Callaway, T. R., J. A. Carroll, J. D. Arthington, C. Pratt, T. S. Edrington, R. C. Anderson, M. L. Galyean, S. C. Ricke, P. Crandall, and D. J. Nisbet. 2008. Citrus products decrease growth of E. coli O157:H7 and Salmonella typhimurium in pure culture and in fermentation with mixed ruminal microorganisms in vitro. Food Pathol. Dis. 5:621-627.
8. Castillo, M., S. M. Martin-Oruem, E. G. Manzanilla, I. Badiola, M. Martin, and J. Gasa. 2006. Quantification of total bacteria, enterobacteria and lactobacilli populations in pig digesta by real-time PCR. Vet. Microbiol. 114:165-170.
9. Crosby, L. D., and C. S. Criddle. 2003. Understanding bias in microbial community analysis techniques due to rrn operon copy number heterogeneity. Biotechniques 34:790-798.
10. DeSantis, T. D., P. Hugenholtz, K. Keller, E. L. Brodie, N. Larsen, Y. M. Piceno, R. Phan, and G. L. Andersen. 2006. NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes. Nucleic Acids Res. 34:W394-W399.
11. Egert, M., and M. W. Friedrich. 2003. Formation of pseudo-terminal restriction fragments, a PCR-related bias affecting terminal restriction length polymorphism analysis of microbial community structure. Appl. Environ. Microbiol. 69:2555-2562.
12. Englyst, H. N., and G. J. Hudson. 1987. Method for routine measurement of dietary fibre as non-starch polysaccharides. A comparison with gas liquid chromatography. Food Chem. 24:63-76.
13. Flint, H. J., E. A. Bayer, E. T. Rincon, R. Lahmed, and B. A. White. 2008. Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat. Rev. Microbiol. 6:121-131.
14. France, J., M. S. Dhanoa, M. K. Theodorou, S. J. Lister, D. R. Davies, and D. Isac. 1993. A model to interpret gas accumulation profiles associated with in vitro degradation of ruminant feeds. J. Theor. Biol. 163:99-111.
15. Hill, J. E., S. M. Hemmingsen, B. G. Goldade, T. J. Dumonceaux, J. Klassen, R. T. Zijlstra, S. H. Goh, and A. G. Van Kessel. 2005. Comparison of ileum microflora of pigs fed corn-, wheat-, or barley-based diets by chaperonin-60 sequencing and quantitative PCR. Appl. Environ. Microbiol. 71:867-875.
16. Hiltner, P., and B. A. Dehority. 1983. Effect of soluble carbohydrates on digestion of cellulose by pure cultures of rumen bacteria. Appl. Environ. Microbiol. 46:642-648.
17. Høltekjolen, A. K., A. K. Uhlen, E. Bråthen, S. Sahlstrøm, and S. H. Knutsen. 2006. Contents of starch and non-starch polysaccharides in barley varieties of different origin. Food Chem. 94:348-358. (Pubitemid 41058949)
18. Hughes, S. A., P. R. Shewry, G. R. Gibson, B. V. McCleary, and R. A. Rastall. 2008. In vitro fermentation of oat and barley derived β-glucans by human faecal microbiota. FEMS Microbiol. Ecol. 64:482-493.
19. Izydorczyk, M. S., J. Storsley, D. Labossiere, A. W. MacGregor, and B. G. Rossnagel. 2000. Variation in total and soluble β-glucan content in hulless barley: effects of thermal, physical, and enzymic treatments. J. Agric. Food Chem. 48:982-989.
20. Julliand, V., A. De Vaux, L. Millet, and G. Fonty. 1999. Identification of Ruminococcus flavefaciens as the predominant cellulolytic bacterial species in the equine cecum. Appl. Environ. Microbiol. 65:3738-3741.
21. Lee, D.-H., Y.-G. Zo, and S.-J. Kim. 1996. Nonradioactive method to study genetic profiles of natural bacterial communities by PCR-single-strand- conformation polymorphism. Appl. Environ. Microbiol. 62:3112-3120.
22. Leser, T. D., J. Z. Amenuvor, T. K. Jensen, R. H. Lindecrona, M. Boye, and K. Moller. 2002. Culture-independent analysis of gut bacteria: the pig gastrointestinal tract microbiota revisited. Appl. Environ. Microbiol. 68:673-690.
23. Liu, W. T., T. L. Marsh, H. Cheng, and L. J. Forney. 1997. Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl. Environ. Microbiol. 63:4516-4522.
24. Ludwig, W., O. Strunk, R. Westram, L. Richter, H. Meier, Yadhukumar, A. Buchner, T. Lai, S. Steppi, G. Jobb, W. Forster, I. Brettske, S. Gerber, A. W. Ginhart, O. Gross, S. Grumann, S. Hermann, R. Jost, A. Konig, T. Liss, R. Lussmann, M. May, B. Nonhoff, B. Reichel, R. Stehlow, A. Stamatakis, N. Stuckmann, A. Vilbig, M. Lenke, T. Ludwig, A. Bode, and K. H. Schleifer. 2004. ARB: a software environment for sequence data. Nucleic Acids Res. 32:1363-1371. (Pubitemid 38854737)
25. Martín-Peláez, S., G. R. Gibson, S. M. Martín- Orúe, A. Klinder, R. A. Rastall, R. M. La Ragione, M. J. Woodward, and A. Costabile. 2008. In vitro fermentation of carbohydrates by porcine faecal inocula and their influence on Salmonella typhimurium growth in batch culture systems. FEMS Microbiol. Ecol. 66:608-619.
26. Martín-Peláez, S., A. G. Manzanilla, M. Anguita, M. Fondevila, M. Martín, E. Mateu, and S. M. Martín-Orúe. 2009. Different fibrous ingredients and coarsely ground maize affect hindgut fermentation in the pig in vitro but not Salmonella Typhimurium survival. Anim. Feed Sci. Technol. 153:141-152.
27. Matsuki, T., K. Watanabe, J. Fujimoto, T. Takada, and R. Tanaka. 2004. Use of 16S rRNA gene-targeted group-specific primers for real-time PCR analysis of predominant bacteria in human feces. Appl. Environ. Microbiol. 70:7220-7228.
28. Matsuki, T., K. Watanabe, J. Fujimoto, Y. Miyamoto, T. Takada, K. Matsumoto, H. Oyaizu, and R. Tanaka. 2002. Development of 16S rRNA-gene-targeted group-specific primers for the detection and identification of predominant bacteria in human feces. Appl. Environ. Microbiol. 68:5445-5451.
29. Menke, K. H., and H. Steingass. 1988. Estimation of the energetic feed value obtained from chemical analysis and in vitro gas production using rumen fluid. Anim. Res. Dev. 28:7-55.
30. O'Connor, A. M., T. Denagamage, J. M. Sargeant, A. Rajic, and J. McKean. 2008. Feeding management practices and feed characteristics associated with Salmonella prevalence in live and slaughtered market-weight finisher swine: a systematic review and summation of evidence from 1950 to 2005. Prev. Vet. Med. 87:213-228.
31. Pettigrew, J. E. 2006. Reduced use of antibiotic growth promoters in diets fed to weanling pigs: dietary tools, part 1. Anim. Biotechnol. 17:207-215.
32. Pieper, R., R. Jha, B. Rossnagel, A. G. Van Kessel, W. B. Souffrant, and P. Leterme. 2008. Effect of barley and oat cultivars with different carbohydrate compositions on the intestinal bacterial communities in weaned piglets. FEMS Microbiol. Ecol. 66:556-566.
33. Pryde, S. E., S. H. Duncan, G. L. Hold, C. S. Stewart, and H. J. Flint. 2002. The microbiology of butyrate formation in the human colon. FEMS Microbiol. Lett. 217:133-139.
34. Ricke, P., S. Kolb, and G. Braker. 2005. Application of a newly developed ARB software-integrated tool for in silico terminal restriction fragment length polymorphism analysis reveals the dominance of a novel pmoA cluster in a forest soil. Appl. Environ. Microbiol. 71:1671-1673. (Pubitemid 40396714)
35. Song, Y., C. Liu, and S. M. Finegold. 2004. Real-time PCR quantitation of clostridia in feces of autistic children. Appl. Environ. Microbiol. 70:6459-6465.
36. Stein, H. H., and D. Y. Kil. 2006. Reduced use of antibiotic growth promoters in diets fed to weanling pigs: dietary tools, part 2. Anim. Biotechnol. 17:217-231.
37. Ter Braak, C. J. F., and P. Šmilauer. 2002. CANOCO reference manual and CanoDraw for Windows user's guide: software for canonical community ordination (version 4.5). Microcomputer Power. Ithaca, NY.
38. Thompson, C. L., B. Wang, and A. J. Holmes. 2008. The immediate environment during postnatal development has long-term impact on gut community structure in pigs. ISME J. 2:739-748.
39. Varel, V. H., and J. T. Yen. 1997. Microbial perspective on fiber utilization by swine. J. Anim. Sci. 75:2715-2722.
40. Walker, A. W., S. H. Duncan, E. C. McWilliam Leitch, M. W. Child, and H. J. Flint. 2005. pH and peptide supply can radically alter bacterial populations and short-chain fatty acid ratios within microbial communities from the human colon. Appl. Environ. Microbiol. 71:3692-3700.
41. Walter, J., C. Hertel, G. W. Tannock, C. M. Lis, K. Munro, and W. P. Hammes. 2001. Detection of Lactobacillus, Leuconostoc, and Weissella species in human feces by using group-specific PCR primers and denaturing gradient gel electrophoresis. Appl. Environ. Microbiol. 67:2578-2585.
42. Xu, J., M. K. Bjursell, J. Himrod, S. Deng, L. K. Carmichael, H. C. Chiang, L. V. Hooper, and J. I. Gordon. 2003. A genomic view of the human-Bacteroides thetaiotaomicron symbiosis. Science 299:2074-2076.