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Fermentable non-starch polysaccharides increases the abundance of Bacteroides–Prevotella–Porphyromonas in ileal microbial community of growing pigs

Published online by Cambridge University Press:  21 July 2014

E. Ivarsson ,
S. Roos ,
H. Y. Liu  and
J. E. Lindberg
E. Ivarsson*
Affiliation:
Department of Animal Nutrition and Management, Swedish University of Agricultural Sciences, PO Box 7024, SE-750 07 Uppsala, Sweden
S. Roos
Affiliation:
Department of Microbiology, Uppsala BioCenter, Swedish University of Agricultural Sciences, PO Box 7025, SE-750 07 Uppsala, Sweden
H. Y. Liu
Affiliation:
Department of Animal Nutrition and Management, Swedish University of Agricultural Sciences, PO Box 7024, SE-750 07 Uppsala, Sweden
J. E. Lindberg
Affiliation:
Department of Animal Nutrition and Management, Swedish University of Agricultural Sciences, PO Box 7024, SE-750 07 Uppsala, Sweden
*
†E-mail: Emma.Ivarsson@slu.se
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Abstract

Most plant-origin fiber sources used in pig production contains a mixture of soluble and insoluble non-starch polysaccharides (NSP). The knowledge about effects of these sources of NSP on the gut microbiota and its fermentation products is still scarce. The aim of this study was to investigate effects of feeding diets with native sources of NSP on the ileal and fecal microbial composition and the dietary impact on the concentration of short-chain fatty acids (SCFA) and lactic acid. The experiment comprised four diets and four periods in a change-over design with seven post valve t-cecum cannulated growing pigs. The four diets were balanced to be similar in NSP content and included one of four fiber sources, two diets were rich in pectins, through inclusion of chicory forage (CFO) and sugar beet pulp, and two were rich in arabinoxylan, through inclusion of wheat bran (WB) and grass meal. The gut microbial composition was assessed with terminal restriction fragment (TRF) length polymorphism and the abundance of Lactobacillus spp., Enterobacteriaceae, Bacteroides–Prevotella–Porphyromonas and the β-xylosidase gene, xynB, were assessed with quantitative PCR. The gut microbiota did not cluster based on NSP structure (arabinoxylan or pectin) rather, the effect was to a high degree ingredient specific. In pigs fed diet CFO, three TRFs related to Prevotellaceae together consisted of more than 25% of the fecal microbiota, which is about 3 to 23 times higher (P<0.05) than in pigs fed the other diets. Whereas pigs fed diet WB had about 2 to 22 times higher abundance (P<0.05) of Megasphaera elsdenii in feces and about six times higher abundance (P<0.05) of Lactobacillus reuteri in ileal digesta than pigs fed the other diets. The total amount of digested NSP (r=0.57; P=0.002), xylose (r=0.53; P=0.004) and dietary fiber (r=0.60; P=0.001) in ileal digesta were positively correlated with an increased abundance of Bacteroides–Prevotella–Porphyromonas. The effect on SCFA was correlated to specific neutral sugars where xylose increased the ileal butyric acid proportion, whereas arabinose increased the fecal butyric acid proportion. Moreover, chicory pectin increased the acetic acid proportion in both ileal digesta and feces.

Keywords

pigpectinarabinoxylanmicrobiotashort-chain fatty acids
Type
Research Article
Information
animal , Volume 8 , Issue 11 , November 2014 , pp. 1777 - 1787
Copyright
© The Animal Consortium 2014 

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References

Andersson, R and Hedlund, B 1983. HPLC analysis of organic-acids in lactic-acid fermented vegetables. Zeitschrift fur Lebensmittel Untersuchung und Forschung 176, 440–443.Google Scholar
Awati, A, Bosch, MW, Tagliapietra, F, Williams, BA and Verstegen, MWA 2006. Difference in in vitro fermentability of four carbohydrates and two diets, using ileal and faecal inocula from unweaned piglets. Journal of the Science of Food and Agriculture 86, 573–582.CrossRefGoogle Scholar
Awati, A, Konstantinov, SR, Williams, BA, Akkermans, ADL, Bosch, MW, Smidt, H and Verstegen, MWA 2005. Effect of substrate adaptation on the microbial fermentation and microbial composition of faecal microbiota of weaning piglets studied in vitro. Journal of the Science of Food and Agriculture 85, 1765–1772.Google Scholar
Bach Knudsen, KE, Hedemann, MS and Laerke, HN 2012. The role of carbohydrates in intestinal health of pigs. Animal Feed Science and Technology 173, 41–53.Google Scholar
Barcenilla, A, Pryde, SE, Martin, JC, Duncan, SH, Stewart, CS, Henderson, C and Flit, HJ 2000. Phylogenetic relationships of butyrate-producing bacteria from the human gut. Applied and Environmental Microbiology 66, 1654–1661.Google Scholar
Begon, M, Harper, JL and Townsend, CR 2006. Ecology: from individuals to ecosystems, 4th edition. Blackwell, Oxford, United Kingdom.Google Scholar
Bikker, P, Dirkzwager, A, Fledderus, J, Trevisi, P, le Huerou-Luron, I, Lalles, JP and Awati, A 2006. The effect of dietary protein and fermentable carbohydrates levels on growth performance and intestinal characteristics in newly weaned piglets. Journal of Animal Science 84, 3337–3345.Google Scholar
Bindelle, J, Pieper, R, Leterme, P, Rossnagel, B and Van Kessel, AG 2010. Changes in intestinal microbial ecophysiology as related to the carbohydrate composition of barleys and oats cultivars in an in vitro model of the pig gastrointestinal tract. Livestock Science 133, 151–153.Google Scholar
Cleusix, V, Lacroix, C, Vollenweider, S and Le Blay, G 2008. Glycerol induces reuterin production and decreases Escherichia coli population in an in vitro model of colonic fermentation with immobilized human feces. FEMS Microbology Ecology 63, 56–64.Google Scholar
Cummings, JH and Englyst, HN 1987. Fermentation in the human large intestine and the available substrates. American Journal of Clinical Nutrition 145, 1243–1255.CrossRefGoogle Scholar
De Filippo, C, Cavalieri, D, Di Paola, M, Ramazzotti, M, Poullett, JB, Massart, S, Collini, S, Pieraccini, G and Lionetti, P 2010. Impact of diet in shaping gut microbiota revealed by comparative study in children from Europe and rural Africa. Proceedings of the National Academy of Sciences of the United States of America 107, 14691–14966.Google Scholar
Dicksved, J, Halfvarson, J, Rosenquist, M, Jarnerot, G, Tysk, C, Apajalahti, J, Engstrand, L and Jansson, JK 2008. Molecular analysis of the gut microbiota of identical twins with Crohn's disease. ISME Journal 2, 716–727.Google Scholar
Eckburg, PB, Bik, EM, Bernstein, CN, Purdom, E, Dethlefsen, L, Sargent, M, Gill, SR, Nelson, KE and Relman, DA 2005. Diversity of the human intestinal microbial flora. Science 308, 1635–1638.CrossRefGoogle ScholarPubMed
Fukada, S, Hidehiro, T, Hase, K, Oshima, K, Nakanishi, Y, Yoshimura, K, Tobe, T, Clarke, JM, Topping, DL, Suzuki, T, Taylor, TD, Itoh, K, Kikuchi, J, Morita, H, Hattori, M and Ohno, H 2011. Bifidobacteria can protect enteropathogenic infection through production of actetate. Nature 469, 543–549.Google Scholar
Gerritsen, J, Smidt, H, Rijkers, GT and de Vos, WM 2011. Intestinal microbiota in human health and disease: the impact of probiotics. Genes and Nutrition 6, 209–240.Google Scholar
Giuberti, G, Gallo, A, Moschini, M and Masoero, F 2013. In vitro production of short-chain fatty acids from resistant starch by pig faecal inoculum . Animal 7, 1446–1453.CrossRefGoogle ScholarPubMed
Högberg, A and Lindberg, JE 2006. The effect of level and type of cereal non-starch polysaccharides on the performance, nutrient utilization and gut environment of pigs around weaning. Animal Feed Science and Technology 127, 200–219.Google Scholar
Ivarsson, E, Liu, HY, Dicksved, J, Roos, S and Lindberg, JE 2012a. Impact of chicory inclusion in a cereal-based diet on digestibility, organ size and faecal microbiota in growing pigs. Animal 6, 1077–1087.Google Scholar
Ivarsson, E, Andersson, R and Lindberg, JE 2012b. Digestibility of fibre sources and molecular weight distribution of fibre fractions in ileal digesta of growing pigs. Archives of Animal Nutrition 66, 445–457.Google Scholar
Ivarsson, E, Andersson, R and Lindberg, JE 2012c. Molecular weight distribution of soluble fiber fractions and short chain fatty acids in ileal digesta of growing pigs. Journal of Animal Science 90, 65–67.Google Scholar
Jensen, BB 2001. Possible ways of modifying type and amount of products from microbial fermentation in the gut. In Gut environment of pigs (ed. A Piva, KE Bach Knudsen and JE Lindberg), pp. 181–200. Nottingham University Press, Nottingham, United Kingdom.Google Scholar
Karlsson, CLJ, Molin, G, Cilio, CM and Ahrne, S 2011. The pioneer gut microbiota in human neonates vaginally born at term – a pilot study. Pediatric Research 70, 282–286.Google Scholar
Konstantinov, SR, Zhu, W, Williams, BA, Tamminga, S, de Vos, WM and Akkermans, ADL 2003. Effect of fermentable carbohydrates on piglet faecal bacterial communities as revealed by denaturing gradient gel electrophoresis analysis of 16S ribosomal DNA. FEMS Microbiology Ecology 43, 225–235.Google Scholar
Leser, TD, Amenuvor, øZ, Jensen, TK, Rikke, H, Lindecrona, MB and Møller, K 2002. Culture- independent analysis of gut bacteria: the pig gastrointestinal tract microbiota revisited. Applied and Environmental Microbiology 68, 673–690.Google Scholar
Liu, HY, Ivarsson, E, Dicksved, J, Lundh, T and Lindberg, JE 2012. Inclusion of chicory (Cichorium intybus L.) in pigs’ diets affects the intestinal microenvironment and the gut microbiota. Applied and Environmental Microbiology 78, 4102–4109.CrossRefGoogle ScholarPubMed
Metzler, BU, Vahjen, W, Baumgartel, T, Rodehutscord, M and Mosenthin, R 2009. Changes in bacterial populations in the ileum of pigs fed low-phosphorus diets supplemented with different sources of fermentable carbohydrates. Animal Feed Science and Technology 148, 68–89.Google Scholar
Metzler-Zebeli, BU, Hooda, S, Pieper, R, Zijlstra, RT, Van Kessel, AG, Mosenthin, R and Ganzle, MG 2010. Nonstarch polysaccharides modulate bacterial microbiota, pathways for butyrate production, and abundance of pathogenic Escherichia coli in the pig gastrointestinal tract. Applied and Environmental Microbiology 76, 3692–3701.CrossRefGoogle ScholarPubMed
Mølbak, L, Thomsen, LE, Jensen, TK, Bach Knudsen, KE and Boye, M 2007. Increased amount of Bifidobacterium thermacidophilum and Megasphaera elsdenii in the colonic microbiota of pigs fed a swine dysentery preventive diet containing chicory roots and sweet lupine. Journal of Applied Microbiology 103, 1853–1867.CrossRefGoogle ScholarPubMed
Montagne, L, Pluske, JR and Hampson, DJ 2003. A review of interactions between dietary fibre and the intestinal mucosa, and their consequences on digestive health in young non-ruminant animals. Animal Feed Science and Technology 108, 95–117.Google Scholar
National Research Council (NRC) 1998. Nutrient requirements of domestic animals. Nutrient requirements of swine, 10th edition. National Academic Press, Washington, DC.Google Scholar
Noblet, J and Le Goff, G 2001. Effect of dietary fibre on the energy value of feeds for pigs. Animal Feed Science and Technology 90, 35–52.Google Scholar
Tajima, K, Aminov, RI, Nagamine, T, Matsui, H, Nakamura, M and Benno, Y 2001. Diet-dependent shifts in the bacterial population of the rumen revealed with real-time PCR. Applied and Environmental Microbiology 67, 2766–2774.Google Scholar
Van Laere, KMJ, Hartemink, R, Bosveld, M, Schols, HA and Voragen, AGJ 2000. Fermentation of plant cell wall derived polysaccharides and their corresponding oligosaccharides by Intestinal bacteria. Journal of Agriculture Food and Chemistry 48, 1644–1652.CrossRefGoogle ScholarPubMed
Van Leeuwen, P, Van Kleef, D, van Kempen, K, Huisman, J and Verstegen, MWA 1991. Post-valve T-caecum cannulation technique in pigs applicated to determine the digestibility of amino acid in maize, groundnut and sunflower meal. Journal of Animal Physiology and Nutrition 65, 183–193.Google Scholar
Voragen, F, Beldman, G and Schols, H 2001. Chemistry and enzymology of pectins. In Advanced dietary fibre technology (ed. BV McCleary and L Prosky), pp. 379–398. Blackwell Science Ltd, Oxford, UK.Google Scholar
Walker, AW, Ince, J, Duncan, SH, Webster, LM, Holtrop, G, Ze, X, Brown, D, Stares, MD, Scott, P, Bergerat, A, Louis, P, McIntosh, F, Johnstone, AM, Lobley, GE, Parkhill, J and Flint, HJ 2011. Dominant and diet-responsive groups of bacteria within the human colonic microbiota. The ISME Journal 5, 220–230.Google Scholar
Wang, JF, Zhu, YH, Li, DF, Wang, M and Jensen, BB 2004. Effect of type and level of dietary fibre and starch on ileal and faecal microbial activity and short-chain fatty acid concentrations in growing pigs. Animal Science 78, 109–117.CrossRefGoogle Scholar
Williams, BA, Verstegen, MWA and Tamminga, S 2001. Fermentation in the large intestine of single-stomached animals and its relationship to animal health. Nutrition Research Reviews 14, 207–227.Google Scholar
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