[en] In broiler chickens, feed additives, including prebiotics, are widely used to improve gut health and to stimulate performance. Xylo-oligosaccharides (XOS) are hydrolytic degradation products of arabinoxylans that can be fermented by the gut microbiota. In the current study it was aimed to analyze the prebiotic properties of XOS when added to the broiler diet. Administration of XOS to chickens, on top of a wheat/rye-based diet, significantly improved the feed conversion ratio. XOS significantly increased villus length in the ileum. It also significantly increased numbers of lactobacilli in the colon and Clostridium cluster XIVa in the caeca. Moreover, the number of gene copies encoding the key bacterial enzyme for butyrate production, butyryl-CoA:acetate CoA-transferase, was significantly increased in the caeca of chickens administered XOS. In this group of chickens, at species level, Lactobacillus crispatus and Anaerostipes butyraticus were significantly increased in abundance in the colon and caecum, respectively. In vitro fermentation of XOS revealed cross-feeding between L. crispatus and A. butyraticus. Lactate, produced by L. crispatus during XOS fermentation, was utilized by the butyrate-producing Anaerostipes species. These data show the beneficial effects of XOS on broiler performance when added to the feed, which potentially can be explained by stimulation of butyrate-producing bacteria through cross-feeding of lactate and subsequent effects of butyrate on gastrointestinal function.
Disciplines :
Microbiology
Author, co-author :
De Maesschalck, C.; Universiteit Gent - Ugent
Eeckhaut, V.; Universiteit Gent - Ugent
Maertens, L.; ILVO
De Lange, L.; Lelystad
Marchal, L.; ForFarmers
Nezer, C.; Quality Partner
De Baere, S.; Universiteit Gent - Ugent
Croubels, S.; Universiteit Gent - Ugent
Daube, Georges ; Université de Liège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires
Dewulf, J.; Universiteit Gent - Ugent
Haesebrouck, F.; Universiteit Gent - Ugent
Ducatelle, R.; Universiteit Gent - Ugent
Taminiau, Bernard ; Université de Liège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires
James SL, Muir JG, Curtis SL, Gibson PR. 2003. Dietary fibre: a roughage guide. Intern Med J 33:291-296. http://dx.doi.org/10.1046/j.1445-5994.2003.00404.x.
Broekaert WF, Courtin CM, Verbeke K, Van de Wiele T, Verstraete W, Delcour JA. 2011. Prebiotic and other health-related effects of cereal-derived arabinoxylans, arabinoxylan-oligosaccharides, and xylooligosaccharides. Crit Rev Food Sci Nutr 51:178-194. http://dx.doi.org/10.1080/10408390903044768.
Aachary AA, Prapulla SG. 2008. Corncob-induced endo-1,4-beta-D-xylanase of Aspergillus oryzae MTCC 5154: production and characterization of xylobiose from glucuronoxylan. J Agric Food Chem 56:3981-3988. http://dx.doi.org/10.1021/jf073430i.
Gibson GR, Probert HM, Loo JV, Rastall RA, Roberfroid MB. 2004. Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutr Res Rev 17:259-275. http://dx.doi.org/10.1079/NRR200479.
Scott KP, Martin JC, Duncan SH, Flint HJ. 2014. Prebiotic stimulation of human colonic butyrate-producing bacteria and bifidobacteria, in vitro. FEMS Microbiol Ecol 87:30-40. http://dx.doi.org/10.1111/1574-6941.12186.
Duncan SH, Louis P, Flint HJ. 2004. Lactate-utilizing bacteria, isolated from human feces, that produce butyrate as a major fermentation product. Appl Environ Microbiol 70:5810-5817. http://dx.doi.org/10.1128/AEM.70.10.5810-5817.2004.
Guilloteau P, Martin L, Eeckhaut V, Ducatelle R, Zabielski R, Van Immerseel F. 2010. From the gut to the peripheral tissues: the multiple effects of butyrate. Nutr Res Rev 23:366-384. http://dx.doi.org/10.1017/S0954422410000247.
Canani RB, Costanzo MD, Leone L, Pedata M, Meli R, Calignano A. 2011. Potential beneficial effects of butyrate in intestinal and extraintestinal diseases. World J Gastroenterol 17:1519-1528. http://dx.doi.org/10.3748/wjg.v17.i12.1519.
Hsu CK, Liao JW, Chung YC, Hsieh CP, Chan YC. 2004. Xylooligosaccharides and fructooligosaccharides affect the intestinal microbiota and precancerous colonic lesion development in rats. J Nutr 134:1523-1528.
Gobinath D, Madhu AN, Prashant G, Srinivasan K, Prapulla SG. 2010. Beneficial effect of xylo-oligosaccharides and fructo-oligosaccharides in streptozotocin-induced diabetic rats. Br J Nutr 104:40-47. http://dx.doi.org/10.1017/S0007114510000243.
Smiricky-Tjardes MR, Flickinger EA, Grieshop CM, Bauer LL, Murphy MR, Fahey GC, Jr. 2003. In vitro fermentation characteristics of selected oligosaccharides by swine fecal microflora. J Anim Sci 81:2505-2514.
Zhenping S, Wenting L, Ruikui Y, Jia L, Honghong L, Wei S, Zhongmie W, Jingpan L, Zhe S, Yuling Q. 2013. Effect of a straw-derived xylooligosaccharide on broiler growth performance, endocrine metabolism, and immune response. Can J Vet Res 77:105-109.
Sekelja M, Rud I, Knutsen SH, Denstadli V, Westereng B, Naes T, Rudi K. 2012. Abrupt temporal fluctuations in the chicken fecal microbiota are explained by its gastrointestinal origin. Appl Environ Microbiol 78:2941-2948. http://dx.doi.org/10.1128/AEM.05391-11.
Meimandipour A, Shuhaimi M, Hair-Bejo M, Azhar K, Kabeir BM, Rasti B, Yazid AM. 2009. In vitro fermentation of broiler cecal content: the role of lactobacilli and pH value on the composition of microbiota and end products fermentation. Lett Appl Microbiol 49:415-420. http://dx.doi.org/10.1111/j.1472-765X.2009.02674.x.
Dumonceaux TJ, Hill JE, Hemmingsen SM, Van Kessel AG. 2006. Characterization of intestinal microbiota and response to dietary virginiamycin supplementation in the broiler chicken. Appl Environ Microbiol 72:2815-2823. http://dx.doi.org/10.1128/AEM.72.4.2815-2823.2006.
Gong J, Forster RJ, Yu H, Chambers JR, Sabour PM, Wheatcroft R, Chen S. 2002. Diversity and phylogenetic analysis of bacteria in the mucosa of chicken ceca and comparison with bacteria in the cecal lumen. FEMS Microbiology Lett 208:1-7. http://dx.doi.org/10.1111/j.1574-6968.2002.tb11051.x.
Lepage P, Leclerc MC, Joossens M, Mondot S, Blottiere HM, Raes J, Ehrlich D, Dore J. 2013. A metagenomic insight into our gut's microbiome. Gut 62:146-158. http://dx.doi.org/10.1136/gutjnl-2011-301805.
Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, Mende DR, Li J, Xu J, Li S, Li D, Cao J, Wang B, Liang H, Zheng H, Xie Y, Tap J, Lepage P, Bertalan M, Batto JM, Hansen T, Le Paslier D, Linneberg A, Nielsen HB, Pelletier E, Renault P, Sicheritz-Ponten T, Turner K, Zhu H, Yu C, Li S, Jian M, Zhou Y, Li Y, Zhang X, Li S, Qin N, Yang H, Wang J, Brunak S, Dore J, Guarner F, Kristiansen K, Pedersen O, Parkhill J, Weissenbach J, Meta HITC, Bork P, Ehrlich SD, Wang J. 2010. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59-65. http://dx.doi.org/10.1038/nature08821.
Torok VA, Ophel-Keller K, Loo M, Hughes RJ. 2008. Application of methods for identifying broiler chicken gut bacterial species linked with increased energy metabolism. Appl Environ Microbiol 74:783-791. http://dx.doi.org/10.1128/AEM.01384-07.
Lu J, Idris U, Harmon B, Hofacre C, Maurer JJ, Lee MD. 2003. Diversity and succession of the intestinal bacterial community of the maturing broiler chicken. Appl Environ Microbiol 69:6816-6824. http://dx.doi.org/10.1128/AEM.69.11.6816-6824.2003.
Knarreborg A, Simon MA, Engberg RM, Jensen BB, Tannock GW. 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. http://dx.doi.org/10.1128/AEM.68.12.5918-5924.2002.
Apajalahti J, Kettunen A, Graham H. 2004. Characteristics of the gastrointestinal microbial communities, with special reference to the chicken. World Poultry Sci J 60:223-232. http://dx.doi.org/10.1079/WPS20040017.
Bjerrum L, Engberg RM, Leser TD, Jensen BB, Finster K, Pedersen K. 2006. Microbial community composition of the ileum and cecum of broiler chickens as revealed by molecular and culture-based techniques. Poult Sc 85:1151-1164. http://dx.doi.org/10.1093/ps/85.7.1151.
Collins MD, Lawson PA, Willems A, Cordoba JJ, Fernandez-Garayzabal J, Garcia P, Cai J, Hippe H, Farrow JA. 1994. The phylogeny of the genus Clostridium: proposal of five new genera and eleven new species combinations. Int J Syst Bacteriol 44:812-826. http://dx.doi.org/10.1099/00207713-44-4-812.
Duncan SH, Louis P, Flint HJ. 2007. Cultivable bacterial diversity from the human colon. Lett Appl Microbiol 44:343-350. http://dx.doi.org/10.1111/j.1472-765X.2007.02129.x.
Pryde SE, Duncan SH, Hold GL, Stewart CS, Flint HJ. 2002. The microbiology of butyrate formation in the human colon. FEMS Microbiol Lett 217:133-139. http://dx.doi.org/10.1111/j.1574-6968.2002.tb11467.x.
Griffiths RI, Whiteley AS, O'Donnell AG, Bailey MJ. 2000. Rapid method for coextraction ofDNAandRNAfrom natural environments for analysis of ribosomal DNA- and rRNA-based microbial community composition. Appl Environ Microbiol 66:5488-5491. http://dx.doi.org/10.1128/AEM.66.12.5488-5491.2000.
Kowalchuk GA, Stienstra AW, Heilig GH, Stephen JR, Woldendorp JW. 2000. Molecular analysis of ammonia-oxidising bacteria in soil of successional grasslands of the Drentsche A (The Netherlands). FEMS Microbiol Ecol 31:207-215. http://dx.doi.org/10.1111/j.1574-6941.2000.tb00685.x.
Hopkins MJ, Macfarlane GT, Furrie E, Fite A, Macfarlane S. 2005. Characterisation of intestinal bacteria in infant stools using real-time PCR and Northern hybridisation analyses. FEMS Microbiol Ecol 54:77-85. http://dx.doi.org/10.1016/j.femsec.2005.03.001.
Louis P, Flint HJ. 2007. Development of a semiquantitative degenerate real-time pcr-based assay for estimation of numbers of butyryl-coenzyme A (CoA) CoA transferase genes in complex bacterial samples. Appl Environ Microbiol 73:2009-2012. http://dx.doi.org/10.1128/AEM.02561-06.
Brosius J, Dull TJ, Sleeter DD, Noller HF. 1981. Gene organization and primary structure of a ribosomal RNA operon from Escherichia coli. J Mol Biol 148:107-127. http://dx.doi.org/10.1016/0022-2836(81)90508-8.
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537-7541. http://dx.doi.org/10.1128/AEM.01541-09.
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194-2200. http://dx.doi.org/10.1093/bioinformatics/btr381.
Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glockner FO. 2007. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188-7196. http://dx.doi.org/10.1093/nar/gkm864.
Barcenilla A, Pryde SE, Martin JC, Duncan SH, Stewart CS, Henderson C, Flint HJ. 2000. Phylogenetic relationships of butyrate-producing bacteria from the human gut. Appl Environ Microbiol 66:1654-1661. http://dx.doi.org/10.1128/AEM.66.4.1654-1661.2000.
Moura P, Barata R, Carvalheiro F, Girio F, Loureiro-Dias MC, Esteves MP. 2007. In vitro fermentation of xylo-oligosaccharides from corn cobs autohydrolysis by Bifidobacterium and Lactobacillus strains. Food Sci Technol 40:963-972.
De Baere S, Eeckhaut V, Steppe M, De Maesschalck C, De Backer P, Van Immerseel F, Croubels S. 2013. Development of a HPLC-UV method for the quantitative determination of four short-chain fatty acids and lactic acid produced by intestinal bacteria during in vitro fermentation. J Pharm Biomed Anal 80:107-115. http://dx.doi.org/10.1016/j.jpba.2013.02.032.
Shakouri MD, Kermanshahi H, Mohsenzadeh M. 2006. Effect of different non starch polysaccharides in semi purified diets on performance and intestinal microflora of young broiler chickens. Int J Poult Sci 5 6:557-561.
Torok VA, Hughes RJ, Mikkelsen LL, Perez-Maldonado R, Balding K, MacAlpine R, Percy NJ, Ophel-Keller K. 2011. Identification and characterization of potential performance-related gut microbiotas in broiler chickens across various feeding trials. Appl Environ Microbiol 77:5868-5878. http://dx.doi.org/10.1128/AEM.00165-11.
Wei S, Morrison M, Yu Z. 2013. Bacterial census of poultry intestinal microbiome. Poult Sci 92:671-683. http://dx.doi.org/10.3382/ps.2012-02822.
Kravtsov EG, Yermolayev AV, Anokhina IV, Yashina NV, Chesnokova VL, Dalin MV. 2008. Adhesion characteristics of Lactobacillus is a criterion of the probiotic choice. Bull Exp Biol Med 145:232-234. http://dx.doi.org/10.1007/s10517-008-0058-x.
Sengupta R, Altermann E, Anderson RC, McNabb WC, Moughan PJ, Roy NC. 2013. The role of cell surface architecture of lactobacilli in host-microbe interactions in the gastrointestinal tract. Mediat Inflamm 2013:237921.
Servin AL. 2004. Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiol Rev 28:405-440. http://dx.doi.org/10.1016/j.femsre.2004.01.003.
Rinttila T, Apajalathi J. 2013. Intestinal microbiota and metabolites-implications for broiler chicken health and performance. J Appl Poult Res 22:647-658. http://dx.doi.org/10.3382/japr.2013-00742.
Jin LZ, Ho YW, Abdullah N, Jalaludin S. 1998. Growth performance, intestinal microbial populations, and serum cholesterol of broilers fed diets containing Lactobacillus cultures. Poult Sci 77:1259-1265. http://dx.doi.org/10.1093/ps/77.9.1259.
Jin LZ, Ho YW, Abdullah N, Jalaludin S. 2000. Digestive and bacterial enzyme activities in broilers fed diets supplemented with Lactobacillus cultures. Poult Sci 79:886-891. http://dx.doi.org/10.1093/ps/79.6.886.
Belenguer A, Duncan SH, Holtrop G, Anderson SE, Lobley GE, Flint HJ. 2007. Impact of pH on lactate formation and utilization by human fecal microbial communities. Appl Environ Microbiol 73:6526-6533. http://dx.doi.org/10.1128/AEM.00508-07.
Harmsen HJM, Raangs GC, He T, Degener JE, Welling GW. 2002. Extensive set of 16S rRNA-based probes for detection of bacteria in human feces. Appl Environ Microbiol 68:2982-2990. http://dx.doi.org/10.1128/AEM.68.6.2982-2990.2002.
Hippe B, Zwielehner J, Liszt K, Lassl C, Unger F, Haslberger AG. 2011. Quantification of butyryl CoA:acetate CoA-transferase genes reveals different butyrate production capacity in individuals according to diet and age. FEMS Microbiol Lett 316:130-135. http://dx.doi.org/10.1111/j.1574-6968.2010.02197.x.
Louis P, Flint HJ. 2009. Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiol Lett 294:1-8. http://dx.doi.org/10.1111/j.1574-6968.2009.01514.x.
Sato T, Matsumoto K, Okumura T, Yokoi W, Naito E, Yoshida Y, Nomoto K, Ito M, Sawada H. 2008. Isolation of lactate-utilizing butyrate-producing bacteria from human feces and in vivo administration of Anaerostipes caccae strain L2 and galacto-oligosaccharides in a rat model. FEMS Microbiol Ecol 66:528-536. http://dx.doi.org/10.1111/j.1574-6941.2008.00528.x.
Belenguer A, Duncan SH, Calder AG, Holtrop G, Louis P, Lobley GE, Flint HJ. 2006. Two routes of metabolic cross-feeding between Bifidobacterium adolescentis and butyrate-producing anaerobes from the human gut. Appl Environ Microbiol 72:3593-3599. http://dx.doi.org/10.1128/AEM.72.5.3593-3599.2006.
Hodgkiss JP. 1984. Peristalsis and antiperistalsis in the chicken caecum are myogenic. Q J Exp Physiol 69:161-170. http://dx.doi.org/10.1113/expphysiol.1984.sp002777.
Janssen PW, Lentle RG, Hulls C, Ravindran V, Amerah AM. 2009. Spatiotemporal mapping of the motility of the isolated chicken caecum. J Comp Physiol B Biochem Syst Environ Physiol 179:593-604. http://dx.doi.org/10.1007/s00360-009-0342-8.
Gantois I, Ducatelle R, Pasmans F, Haesebrouck F, Hautefort I, Thompson A, Hinton JC, Van Immerseel F. 2006. Butyrate specifically down-regulates Salmonella pathogenicity island 1 gene expression. Appl Environ Microbiol 72:946-949. http://dx.doi.org/10.1128/AEM.72.1.946-949.2006.
Timbermont L, Lanckriet A, Dewulf J, Nollet N, Schwarzer K, Haesebrouck F, Ducatelle R, Van Immerseel F. 2010. Control of Clostridium perfringens-induced necrotic enteritis in broilers by target-released butyric acid, fatty acids and essential oils. Avian Pathol 39:117-121. http://dx.doi.org/10.1080/03079451003610586.
Willemsen LEM, Koetsier MA, van Deventer SJH, van Tol EAF. 2003. Short chain fatty acids stimulate epithelial mucin 2 expression through differential effects on prostaglandin E-1 and E-2 production by intestinal myofibroblasts. Gut 52:1442-1447. http://dx.doi.org/10.1136/gut.52.10.1442.
Hamer HM, Jonkers D, Venema K, Vanhoutvin S, Troost FJ, Brummer RJ. 2008. The role of butyrate on colonic function. Aliment Pharmacol Ther 27:104-119.
Inan MS, Rasoulpour RJ, Yin L, Hubbard AK, Rosenberg DW, Giardina C. 2000. The luminal short-chain fatty acid butyrate modulates NF-kappa B activity in a human colonic epithelial cell line. Gastroenterology 118:724-734. http://dx.doi.org/10.1016/S0016-5085(00)70142-9.
Klampfer L, Huang J, Sasazuki T, Shirasawa S, Augenlicht L. 2003. Inhibition of interferon gamma signaling by the short chain fatty acid butyrate. Mol Cancer Res 1:855-862.
Wächtershäuser A, Loitsch SM, Stein J. 2000. PPAR-γ is selectively upregulated in Caco-2 cells by butyrate. Biochem Bioph Res Commun 272:380-385. http://dx.doi.org/10.1006/bbrc.2000.2793.
Schwab M, Reynders V, Loitsch S, Steinhilber D, Stein J, Schroder O. 2007. Involvement of different nuclear hormone receptors in butyrate-mediated inhibition of inducible NF kappa B signalling. Mol Immunol 44:3625-3632. http://dx.doi.org/10.1016/j.molimm.2007.04.010.
Martin H. 2010. Role of PPAR-gamma in inflammation. Prospects for therapeutic intervention by food components. Mutat Res 690:57-63.
Dube PE, Brubaker PL. 2007. Frontiers in glucagon-like peptide-2: multiple actions, multiple mediators. Am J Physiol Endocrinol Metab 293: E460-E465. http://dx.doi.org/10.1152/ajpendo.00149.2007.
Drucker DJ. 2001. The glucagon-like peptides. Endocrinology 142:521-527. http://dx.doi.org/10.1210/endo.142.2.7983.
de Heuvel E, Wallace L, Sharkey KA, Sigalet DL. 2012. Glucagon-like peptide 2 induces vasoactive intestinal polypeptide expression in enteric neurons via phophatidylinositol 3-kinase-gamma signaling. Am J Physiol Endocrinol Metab 303:E994-E1005. http://dx.doi.org/10.1152/ajpendo.00291.2012.
Hu XF, Guo YM, Huang BY, Bun S, Zhang LB, Li JH, Liu D, Long FY, Yang X, Jiao P. 2010. The effect of glucagon-like peptide 2 injection on performance, small intestinal morphology, and nutrient transporter expression of stressed broiler chickens. Poult Sci 89:1967-1974. http://dx.doi.org/10.3382/ps.2009-00547.
Rey FE, Faith JJ, Bain J, Muehlbauer MJ, Stevens RD, Newgard CB, Gordon JI. 2010. Dissecting the in vivo metabolic potential of two human gut acetogens. J Biol Chem 285:22082-22090. http://dx.doi.org/10.1074/jbc.M110.117713.