[en] Although fermentable carbohydrates (CHO) can reduce metabolites derived from dietary protein fermentation in the intestine of pigs, the interaction between site of fermentation and substrate availability along the gut is still unclear. The current study aimed at determining the impact of two different sources of carbohydrates in diets with low or very high protein content on microbial metabolite profiles along the gastrointestinal tract of piglets. Thirty-six piglets (n = 6 per group) were fed diets high (26%, HP) or low (18%, LP) in dietary protein and with or without two different sources of carbohydrates (12% sugar beet pulp, SBP, or 8% lignocellulose, LNC) in a 2 × 3 factorial design. After 3 weeks, contents from stomach, jejunum, ileum, caecum, proximal and distal colon were taken and analysed for major bacterial metabolites (D-lactate, L-lactate, short chain fatty acids, ammonia, amines, phenols and indols). Results indicate considerable fermentation of CHO and protein already in the stomach. HP diets increased the formation of ammonia, amines, phenolic and indolic compounds throughout the different parts of the intestine with most pronounced effects in the distal colon. Dietary SBP inclusion in LP diets favoured the formation of cadaverine in the proximal parts of the intestine. SBP mainly increased CHO-derived metabolites such as SCFA and lactate and decreased protein-derived metabolites in the large intestine. Based on metabolite profiles, LNC was partly fermented in the distal large intestine and reduced mainly phenols, indols and cadaverine, but not ammonia. Multivariate analysis confirmed more diet-specific metabolite patterns in the stomach, whereas the CHO addition was the main determinant in the caecum and proximal colon. The protein level mainly influenced the metabolite patterns in the distal colon. The results confirm the importance of CHO source to influence the formation of metabolites derived from protein fermentation along the intestinal tract of the pig.
Al-Tamimi MA, Palframan RJ, Cooper JM, Gibson GR, Rastall RA. 2006. In vitro fermentation of sugar beet arabinan and arabino-oligosaccharides by the human gut microflora. J Appl Microbiol. 100:407-414.
Anguita M, Gasa J, Nofrarias M, Martín-Orúe SM, Pérez JF. 2007. Effect of coarse ground corn, sugar beet pulp and wheat bran on the voluntary intake and physicochemical characteristics of digesta of growing pigs. Livest Sci. 107:182-191.
Bach Knudsen KE. 1997. Carbohydrate and lignin contents of plant materials used in animal feeding. Anim Feed Sci Technol. 67:319-338.
Bach Knudsen KE, Hedemann MS, Lærke HN. 2012. The role of carbohydrates in intestinal health of pigs. Anim Feed Sci Technol. 173:41-53.
Bikker P, Dirkzwager A, Fledderus J, Trevisi P, Le Huerou-Luron I, Lalles JP, Awati A. 2006. The effect of dietary protein and fermentable carbohydrates levels on growth performance and intestinal characteristics in newly weaned piglets. J Anim Sci. 84:3337-3345.
Bindelle J, Buldgen A, Delacollette M, Wavreille J, Agneessens R, Destain JP, Leterme P. 2009. Influence of source and concentrations of dietary fiber on in vivo nitrogen excretion pathways in pigs as reflected by in vitro fermentation and nitrogen incorporation by fecal bacteria. J Anim Sci. 87:583-593.
Bindelle J, Leterme P, Buldgen A. 2008. Nutritional and environmental consequences of dietary fibre in pig nutrition: a review. Biotechnol Agron Soc Environ. 12:69-80.
Blaut M, Clavel T. 2007. Metabolic diversity of the intestinal microbiota: implications for health and disease. J Nutr. 137:751S-755S.
Castillo M, Skene G, Roca M, Anguita M, Badiola I, Duncan SH, Flint HJ, Martín-Orúe SM. 2007. Application of 16S rRNA gene-targetted fluorescence in situ hybridization and restriction fragment length polymorphism to study porcine microbiota along the gastrointestinal tract in response to different sources of dietary fibre. FEMS Microbiol Ecol. 59:138-146.
Clemens ET, Stevens CE, Southworth M. 1975. Sites of organic acid production and pattern of digesta movement in the gastrointestinal tract of swine. J Nutr. 105:759-768.
De Lange CFM, Pluske J, Gong J, Nyachoti CM. 2010. Strategic use of feed ingredients and feed additives to stimulate gut health and development in young pigs. Livest Sci. 134:124-134.
Drochner W, Kerler A, Zacharias B. 2004. Pectin in pig nutrition, a comparative review. J Anim Physiol Anim Nutr. 88:367-380.
GfE [Gesellschaft für Ernährungsphysiologie]. 2006. Empfehlungen zur Energie- und Nährstoffversorgung von Schweinen. Frankfurt am Main: DLG-Verlag.
Graham H, Hesselman K, Aman P. 1986. The influence of wheat bran and sugar beet pulp on the digestibility of dietary components in a cereal-based pig diet. J Nutr. 116:242-251.
Hamer HM, De Preter V, Windey K, Verbeke K. 2012. Functional analysis of colonic bacterial metabolism: relevant to health? Am J Physiol Gastrointest Liver Physiol. 302:G1-G9.
Hansen LL, Stolzenbach S, Jensen JA, Henckel P, Hansen-Møller J, Syriopoulos K, Byrne DV. 2008. Effect of feeding fermentable fibre-rich feedstuffs on meat quality with emphasis on chemical and sensory boar taint in entire male and female pigs. Meat Sci. 80:1165-1173.
Heo JM, Opapeju FO, Pluske JR, Kim JC, Hampson DJ, Nyachoti CM. 2013. Gastrointestinal health and function in weaned pigs: a review of feeding strategies to control post-weaning diarrhoea without using in-feed antimicrobial compounds. J Anim Physiol Anim Nutr. 97:207-237.
Hermes RG, Molist F, Ywazaki M, Nofrarias M, Gomez De Segura A, Gasa J, Perez JF. 2009. Effect of dietary level of protein and fiber on the productive performance and health status of piglets. J Anim Sci. 87:3569-3577.
Jensen BB. 2006. Prevention of boar taint in pig production. Factors affecting the level of skatole. Acta Vet Scand. 48:S6.
Kanjee U, Gutsche I, Alexopoulos E, Zhao B, El Bakkouri M, Thibault G, Liu K, Ramachandran S, Snider J, Pai EF, Houry WA. 2011. Linkage between the bacterial acid stress and stringent responses: the structure of the inducible lysine decarboxylase. EMBO J. 30:931-944.
Konstantinov SR, Awati A, Smidt H, Williams BA, Akkermans AD, De Vos WM. 2004. Specific response of a novel and abundant Lactobacillus amylovorus-like phylotype to dietary prebiotics in the guts of weaning piglets. Appl Environ Microbiol. 70:3821-3830.
Kröger S, Pieper R, Schwelberger HG, Wang J, Villodre Tudela C, Aschenbach JR, Van Kessel AG, Zentek J. 2013. Diets high in heat-treated soybean meal reduce the histamine-induced epithelial response in the colon of weaned piglets and increase epithelial catabolism of histamine. PLoS One. 8:e80612.
Kuley E, Bali{dotless}kci{dotless} E, Özoǧul I, Gökdogan S, Özoǧul F. 2012. Stimulation of cadaverine production by food borne pathogens in the presence of Lactobacillus, Lactococcus, and Streptococcus spp. J Food Sci. 77:M650-M658.
Mair C, Plitzner C, Domig KJ, Schedle K, Windisch W. 2010. Impact of inulin and a multispecies probiotic formulation on performance, microbial ecology and concomitant fermentation patterns in newly weaned piglets. J Anim Physiol Anim Nutr. 94:e164-e177.
Metzler-Zebeli BU, Mosenthin R. 2008. A review of interactions between dietary fiber and the gastrointestinal microbiota and their consequences on intestinal phosphorus metabolism in growing pigs. Asian-Aust J Anim Sci. 21:603-615.
Miller DN, Varel VH. 2002. An in vitro study of manure composition on the biochemical origins, composition, and accumulation of odorous compounds in cattle feedlots. J Anim Sci. 80:2214-2222.
Molist F, Van Oostrum M, Pérez JF, Mateos GG, Nyachoti CM, Van Der Aar PJ. 2014. Relevance of functional properties of dietary fibre in diets for weanling pigs. Anim Feed Sci Technol. 189:1-10.
Morris DR, Fillingame RH. 1974. Regulation of amino acid decarboxylation. Annu Rev Biochem. 43:303-321.
Naumann K, Bassler R. 2004. Methodenbuch band III: Die chemische Untersuchung von Futtermitteln. Melsungen: Neumann-Neudamm.
Nyachoti CM, Omogbenigun FO, Rademacher M, Blank G. 2006. Performance responses and indicators of gastrointestinal health in early-weaned pigs fed low-protein amino acid-supplemented diets. J Anim Sci. 84:125-134.
Owusu-Asiedu A, Patience JF, Laarveld B, Van Kessel AG, Simmins PH, Zijlstra RT. 2006. Effects of guar gum and cellulose on digesta passage rate, ileal microbial populations, energy and protein digestibility, and performance of grower pigs. J Anim Sci. 84:843-852.
Pieper R, Janczyk P, Zeyner A, Smidt H, Guiard V, Souffrant WB. 2008. Ecophysiology of the developing total bacterial and lactobacillus communities in the terminal small intestine of weaning piglets. Microb Ecol. 56:474-483.
Pieper R, Kröger S, Richter JF, Wang J, Martin L, Bindelle J, Htoo JK, Von Smolinski D, Vahjen W, Zentek J, Van Kessel AG. 2012. Fermentable fiber ameliorates fermentable protein-induced changes in microbial ecology, but not the mucosal response, in the colon of piglets. J Nutr. 142:661-667.
Pieper R, Vahjen W, Neumann K, Van Kessel AG, Zentek J. 2012. Dose-dependent effects of dietary zinc oxide on bacterial communities and metabolic profiles in the ileum of weaned pigs. J Anim Physiol Anim Nutr. 96:825-833.
Regina DC, Eisemann JH, Lang JA, Argenzio RA. 1999. Changes in gastric contents in pigs fed a finely ground and pelleted or coarsely ground meal diet. J Anim Sci. 77:2721-2729.
Richter JF, Pieper R, Zakrzewski SS, Günzel D, Schulzke JD, Van Kessel AG. 2014. Diets high in fermentable protein and fibre alter tight junction protein composition with minor effects on barrier function in piglet colon. Br J Nutr. 111:1040-1049.
Rideout TC, Fan MZ, Cant JP, Wagner-Riddle C, Stonehouse P. 2004. Excretion of major odor-causing and acidifying compounds in response to dietary supplementation of chicory inulin in growing pigs. J Anim Sci. 82:1678-1684.
Rist VTS, Weiss E, Eklund M, Mosenthin R. 2013. Impact of dietary protein on microbiota composition and activity in the gastrointestinal tract of piglets in relation to gut health: a review. Animal. 7:1067-1078.
Stumpff F, Lodemann U, Van Kessel AG, Pieper R, Klingspor S, Wolf K, Martens H, Zentek J, Aschenbach JR. 2013. Effects of dietary fibre and protein on urea transport across the cecal mucosa of piglets. J Comp Physiol B. 183:1053-1063.
Tabor CW, Tabor H. 1985. Polyamines in microorganisms. Microbiol Rev. 49:81-99.
Ter Braak CJF, Šmilauer P. 2002. CANOCO reference manual and CanoDraw for Windows user's guide: software for canonical community ordination (version 4.5). Ithaca: Microcomputer Power.
Vahjen W, Pieper R, Zentek J. 2010. Bar-coded pyrosequencing of 16S rRNA gene amplicons reveals changes in ileal porcine bacterial communities due to high dietary zinc intake. Appl Environ Microbiol. 76:6689-6691.
Willing B, Van Kessel AG. 2010. Host pathways for recognition: establishing gastrointestinal microbiota as relevant in animal health and nutrition. Livest Sci. 133:82-91.
Windey K, De Preter V, Verbeke K. 2012. Relevance of protein fermentation to gut health. Mol Nutr Food Res. 56:184-196.
Zentek J, Ferrara F, Pieper R, Tedin L, Meyer W, Vahjen W. 2013. Effects of dietary combinations of organic acids and medium chain fatty acids on the gastrointestinal microbial ecology and bacterial metabolites in the digestive tract of weaning piglets. J Anim Sci. 91:3200-3210.