Xylo‐oligosaccharides display a prebiotic activity when used to supplement wheat or corn‐based diets for broilers

Abstract It is now well established that exogenous &bgr;‐1,4‐xylanases improve the nutritive value of wheat‐based diets for poultry. Among other factors, the mechanism of action of exogenous enzymes may involve a microbial route resulting from the generation of prebiotic xylo‐oligosaccharides (XOS) in the birds’ gastro‐intestinal (GI) tract. In a series of three experiments, the effect of XOS on the performance of broilers fed wheat or corn‐based diets was investigated. In experiment 1, birds receiving diets supplemented with XOS displayed an increased weight gain (P = 0.08). The capacity of XOS to improve the performance of animals during a longer trial (42 d) was investigated (Experiment 2). The data revealed that diet supplementation with XOS, tested at two incorporation rates (0.1 and 1 g/kg), or with an exogenous &bgr;‐1,4‐xylanase resulted in an increased nutritive value of the wheat‐based diet. An improvement in animal performance was accompanied by a shift in the microbial populations colonizing the upper portions of the GI tract. XOS were also able to improve the performance of broilers fed a corn‐based diet, although the effects were not apparent at incorporation rates of 10 g/kg. Together these studies suggest that in some cases the capacity of &bgr;‐1,4‐xylanases to improve the nutritive value of wheat‐based diets is more related to their ability to produce prebiotic XOS than to their ability to degrade arabinoxylans. The extremely low quantities of XOS used in this study also challenge the depiction of a prebiotic being a quantitatively fermented substrate. These data also bring into question the validity of the “cell wall” mechanism, as XOS elicited an effect with clearly no action on endosperm cell wall integrity and yet the performance effects noted were equivalent or superior to the added enzymes.

[1]  M. Coimbra,et al.  Revisiting the structural features of arabinoxylans from brewers' spent grain. , 2016, Carbohydrate polymers.

[2]  Board on Agriculture,et al.  Nutrient requirements of poultry , 2016 .

[3]  H. Pereira,et al.  Assessment of the bifidogenic effect of substituted xylo-oligosaccharides obtained from corn straw. , 2016, Carbohydrate polymers.

[4]  J. Dewulf,et al.  Effects of Xylo-Oligosaccharides on Broiler Chicken Performance and Microbiota , 2015, Applied and Environmental Microbiology.

[5]  M. Pinheiro,et al.  Unravelling the Diversity of Grapevine Microbiome , 2014, PloS one.

[6]  M. Coimbra,et al.  Microwave superheated water and dilute alkali extraction of brewers' spent grain arabinoxylans and arabinoxylo-oligosaccharides. , 2014, Carbohydrate polymers.

[7]  Liu Honghong,et al.  Effect of a straw-derived xylooligosaccharide on broiler growth performance, endocrine metabolism, and immune response. , 2013, Canadian journal of veterinary research = Revue canadienne de recherche veterinaire.

[8]  C. Manaia,et al.  Bacterial diversity from the source to the tap: a comparative study based on 16S rRNA gene-DGGE and culture-dependent methods. , 2013, FEMS microbiology ecology.

[9]  J. Prates,et al.  The effects of restricting enzyme supplementation in wheat-based diets to broilers , 2012 .

[10]  M. Coimbra,et al.  Demonstration of the presence of acetylation and arabinose branching as structural features of locust bean gum galactomannans , 2011 .

[11]  Rob Knight,et al.  UCHIME improves sensitivity and speed of chimera detection , 2011, Bioinform..

[12]  Robert C. Edgar,et al.  Search and clustering orders of magnitude faster than BLAST , 2010, Bioinform..

[13]  Martin Hartmann,et al.  Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities , 2009, Applied and Environmental Microbiology.

[14]  J. Delcour,et al.  Heat and pH stability of prebiotic arabinoxylooligosaccharides, xylooligosaccharides and fructooligosaccharides , 2009 .

[15]  W. Verstraete,et al.  Structurally different wheat-derived arabinoxylooligosaccharides have different prebiotic and fermentation properties in rats. , 2008, The Journal of nutrition.

[16]  T. Wiele,et al.  Dietary Inclusion of Wheat Bran Arabinoxylooligosaccharides Induces Beneficial Nutritional Effects in Chickens , 2008 .

[17]  F. Paul,et al.  Oligosaccharide feed additives , 2007 .

[18]  Y. Chan,et al.  Dietary intake of xylooligosaccharides improves the intestinal microbiota, fecal moisture, and pH value in the elderly , 2007 .

[19]  X. Zhao,et al.  Cecal populations of lactobacilli and bifidobacteria and Escherichia coli populations after in vivo Escherichia coli challenge in birds fed diets with purified lignin or mannanoligosaccharides. , 2007, Poultry science.

[20]  Florbela Carvalheiro,et al.  In vitro fermentation of xylo-oligosaccharides from corn cobs autohydrolysis by Bifidobacterium and Lactobacillus strains , 2007 .

[21]  L. Phillip,et al.  Effects of purified lignin and mannan oligosaccharides on intestinal integrity and microbial populations in the ceca and litter of broiler chickens. , 2007, Poultry science.

[22]  W. Kim,et al.  Effects of Xylooligosaccharide Intake on Fecal Bifidobacteria, Lactic acid and Lipid Metabolism in Korean Young Women , 2007 .

[23]  M. A. Kassim Dietary modulation of the human colonic microbiota through plant-derived prebiotic compounds , 2007 .

[24]  G. Macfarlane,et al.  Review article: prebiotics in the gastrointestinal tract , 2006, Alimentary pharmacology & therapeutics.

[25]  Susan M. Huse,et al.  Microbial diversity in the deep sea and the underexplored “rare biosphere” , 2006, Proceedings of the National Academy of Sciences.

[26]  Antonio Santos,et al.  Prebiotics and their long-term influence on the microbial populations of the mouse bowel. , 2006, Food microbiology.

[27]  J. Prates,et al.  Use of β-Glucanases and β-1,4-Xylanases to Supplement Diets Containing Alfalfa and Rye for Laying Hens: Effects on Bird Performance and Egg Quality , 2006 .

[28]  M. Choct,et al.  Enzymes for the feed industry: past, present and future , 2006 .

[29]  R. D. de Souza,et al.  Colonic Health: Fermentation and Short Chain Fatty Acids , 2006, Journal of clinical gastroenterology.

[30]  M. Roberfroid,et al.  Dietary modulation of the human colonic microbiota: updating the concept of prebiotics , 2004, Nutrition Research Reviews.

[31]  C. Fontes,et al.  Xylanase Inhibitors Affect the Action of Exogenous Enzymes Used to Supplement Triticum durum-Based Diets for Broiler Chicks , 2004 .

[32]  L. Ferreira,et al.  A family 6 carbohydrate-binding module potentiates the efficiency of a recombinant xylanase used to supplement cereal-based diets for poultry , 2004, British poultry science.

[33]  Y. Chan,et al.  Xylooligosaccharides and fructooligosaccharides affect the intestinal microbiota and precancerous colonic lesion development in rats. , 2004, The Journal of nutrition.

[34]  G. Gibson,et al.  Carbohydrate preferences of Bifidobacterium species isolated from the human gut. , 2003, Current issues in intestinal microbiology.

[35]  A. Voragen,et al.  In vitro fermentability of differently substituted xylo-oligosaccharides. , 2002, Journal of agricultural and food chemistry.

[36]  W. Walker,et al.  Nutritional impact of pre- and probiotics as protective gastrointestinal organisms. , 2002, Annual review of nutrition.

[37]  T. Mattila-Sandholm,et al.  In vitro fermentation of cereal dietary fibre carbohydrates by probiotic and intestinal bacteria , 2002 .

[38]  W. Walker,et al.  Nutritional Impact of Probiotics as Protective Gastrointestinal Organisms , 2002 .

[39]  B. Kos,et al.  Role of Lactic Acid Bacteria and Bifidobacteria in Synbiotic Effect , 2001 .

[40]  M. Bedford Exogenous enzymes in monogastric nutrition - their current value and future benefits. , 2000 .

[41]  S. Dänicke,et al.  Interactions between dietary fat type and enzyme supplementation in broiler diets with high pentosan contents: effects on precaecal and total tract digestibility of fatty acids, metabolizability of gross energy, digesta viscosity and weights of small intestine , 2000 .

[42]  A. Voragen,et al.  Fermentation of plant cell wall derived polysaccharides and their corresponding oligosaccharides by intestinal bacteria. , 2000, Journal of agricultural and food chemistry.

[43]  S. DaÈnickea,et al.  Interactions between dietary fat type and enzyme supplementation in broiler diets with high pentosan contents: effects on precaecal and total tract digestibility of fatty acids, metabolizability of gross energy, digesta viscosity and weights of small intestine , 2000 .

[44]  H. Ishii,et al.  Xylooligosaccharide decreases blood ammonia levels in patients with liver cirrhosis , 2000, American Journal of Gastroenterology.

[45]  G R Gibson,et al.  Probiotics, prebiotics, and synbiotics: approaches for modulating the microbial ecology of the gut. , 1999, The American journal of clinical nutrition.

[46]  C. Barthomeuf,et al.  Non-digestible oligosaccharides used as prebiotic agents: mode of production and beneficial effects on animal and human health. , 1999, Reproduction, nutrition, development.

[47]  A. Piva Non-conventional feed additives , 1998 .

[48]  A. Siitonen,et al.  Oat β-glucan and xylan hydrolysates as selective substrates for Bifidobacterium and Lactobacillus strains , 1998, Applied Microbiology and Biotechnology.

[49]  M. Villamide,et al.  Effect of storage time and dietary enzyme on the metabolizable energy and digesta viscosity of barley-based diets for poultry. , 1998, Poultry science.

[50]  M. Tenkanen,et al.  Endo-β-1,4-xylanase families: differences in catalytic properties , 1997 .

[51]  G. N. Richards,et al.  Effect of sucrose thermal oligosaccharide caramel, dietary vitamin-mineral level, and brooding temperature on growth and intestinal bacterial populations of broiler chickens. , 1997, Poultry science.

[52]  G. N. Richards,et al.  Selective enrichment of bifidobacteria in the intestinal tract of broilers by thermally produced kestoses and effect on broiler performance. , 1997, Poultry science.

[53]  G. Fahey,et al.  Selected indigestible oligosaccharides affect large bowel mass, cecal and fecal short-chain fatty acids, pH and microflora in rats. , 1997, The Journal of nutrition.

[54]  A. Morgan,et al.  The use of enzymes in poultry diets , 1996 .

[55]  G. Pesti Nutrient requirements of poultry , 1995 .

[56]  G R Gibson,et al.  Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. , 1995, The Journal of nutrition.

[57]  J. D. V. D. Klis,et al.  Effect of a soluble polysaccharide (carboxy methyl cellulose) on the physico‐chemical conditions in the gastrointestinal tract of broilers , 1993 .

[58]  R. R. Marquardt,et al.  Effect of enzyme supplementation on the performance and digestive tract size of broiler chickens fed wheat- and barley-based diets. , 1993, Poultry science.

[59]  H. Yamada,et al.  Structure and properties of oligosaccharides from wheat bran , 1993 .

[60]  H. Classen,et al.  Reduction of intestinal viscosity through manipulation of dietary rye and pentosanase concentration is effected through changes in the carbohydrate composition of the intestinal aqueous phase and results in improved growth rate and food conversion efficiency of broiler chicks. , 1992, The Journal of nutrition.

[61]  H. Classen,et al.  The effect of pelleting, salt, and pentosanase on the viscosity of intestinal contents and the performance of broilers fed rye. , 1991, Poultry science.

[62]  N. Matsumoto,et al.  In vitro digestibility and in vivo utilization of xylobiose. , 1991 .

[63]  M. Sugano,et al.  Effects of Xylooligosaccharides on Blood Glucose, Serum and Liver Lipids and Cecum Short-chain Fatty Acids in Diabetic Rats , 1991 .

[64]  N. Matsumoto,et al.  Effect of Xylooligosaccharide on the Growth of Bifidobacteria , 1990 .