Skip to main content Accessibility help
×
Home

Transglycosylated starch accelerated intestinal transit and enhanced bacterial fermentation in the large intestine using a pig model

  • Barbara U. Metzler-Zebeli (a1), Monica A. Newman (a1), Andrea Ladinig (a2), Wolfgang Kandler (a3), Dietmar Grüll (a4) and Qendrim Zebeli (a1)...

Abstract

Resistant starch can alter the intestinal nutrient availability and bulk of digesta, thereby modulating the substrate available for microbial metabolic activity along the gastrointestinal tract. This study elucidated the effect of transglycosylated starch (TGS) on the retention of digesta in the upper digestive tract, ileal flow and hindgut disappearance of nutrients, and subsequent bacterial profiles in pigs. Fourteen ileal-cannulated growing pigs were fed either the TGS or control (CON) diet in a complete crossover design. Each period consisted of a 10-d adaptation to the diets, followed by 3-d collection of faeces and ileal digesta. Consumption of TGS decreased the retention of digesta in the stomach and small intestine, and increased ileal DM, starch, Ca and P flow, leading to enhanced starch fermentation in the hindgut compared with CON-fed pigs. TGS increased ileal and faecal total SCFA, especially ileal and faecal acetate and faecal butyrate. Gastric retention time positively correlated to Klebsiella, which benefitted together with Selenomonas, Lactobacillus, Mitsuokella and Coriobacteriaceae from TGS feeding and ileal starch flow. Similar relationships existed in faeces with Coriobacteriaceae, Veillonellaceae and Megasphaera benefitting most, either directly or indirectly via cross-feeding, from TGS residuals in faeces. TGS, in turn, depressed genera within Ruminococcaceae, Clostridiales and Christensenellaceae compared with the CON diet. The present results demonstrated distinct ileal and faecal bacterial community and metabolite profiles in CON- and TGS-fed pigs, which were modulated by the type of starch, intestinal substrate flow and retention of digesta in the upper digestive tract.

Copyright

Corresponding author

*Corresponding author: B. U. Metzler-Zebeli, email barbara.metzler@vetmeduni.ac.at

References

Hide All
1.Bach Knudsen, KE, Lærke, HN, Hedemann, MS, et al. (2018) Impact of diet-modulated butyrate production on intestinal barrier function and inflammation. Nutrients 10, E1499.
2.Topping, DL & Clifton, PM (2001) Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol Rev 81, 10311064.
3.Birt, DF, Boylston, T, Hendrich, S, et al. (2013) Resistant starch: promise for improving human health. Adv Nutr 4, 587601.
4.McKenzie, C, Tan, J, Macia, L, et al. (2017) The nutrition–gut microbiome–physiology axis and allergic diseases. Immunol Rev 278, 277295.
5.Wilfart, A, Montagne, L, Simmins, H, et al. (2007) Digesta transit in different segments of the gastrointestinal tract of pigs as affected by insoluble fibre supplied by wheat bran. Br J Nutr 98, 5462.
6.Souza da Silva, C, Haenen, D, Koopmans, SJ, et al. (2014) Effects of resistant starch on behaviour, satiety-related hormones and metabolites in growing pigs. Animal 8, 14021411.
7.Ingerslev, AK, Mutt, SJ, Lærke, HN, et al. (2017) Postprandial PYY increase by resistant starch supplementation is independent of net portal appearance of short-chain fatty acids in pigs. PLOS ONE 12, e0185927.
8.Newman, MA, Zebeli, Q, Eberspächer, E, et al. (2017) Transglycosylated starch improves insulin response and alters lipid and amino acid metabolome in a growing pig model. Nutrients 9, 291.
9.Newman, MA, Petri, RM, Grüll, D, et al. (2018) Transglycosylated starch modulates the gut microbiome and expression of genes related to lipid synthesis in liver and adipose tissue of pigs. Front Microbiol 9, 224.
10.Guilloteau, P, Zabielski, R, Hammon, HM, et al. (2010) Nutritional programming of gastrointestinal tract development: is the pig a good model for man? Nutr Res Rev 23, 422.
11.Nielsen, KL, Hartvigsen, ML, Hedemann, MS, et al. (2014) Similar metabolic responses in pigs and humans to breads with different contents and compositions of dietary fibers: a metabolomics study. Am J Clin Nutr 99, 941949.
12.Patterson, JK, Lei, XG & Miller, DD (2008) The pig as an experimental model for elucidating the mechanisms governing dietary influence on mineral absorption. Exp Biol Med (Maywood) 233, 651664.
13.Newman, MA, Zebeli, Q, Velde, K, et al. (2016) Enzymatically modified starch favorably modulated intestinal transit time and hindgut fermentation in growing pigs. PLOS ONE 11, e0167784.
14.Metzler, BU, Mosenthin, R, Baumgärtel, T, et al. (2008) The effect of dietary phosphorus and calcium level, phytase supplementation, and ileal infusion of pectin on the chemical composition and carbohydrase activity of fecal bacteria and the level of microbial metabolites in the gastrointestinal tract of pigs. J Anim Sci 86, 15441555.
15.National Research Council (2012) Nutrient Requirements of Swine, 11th ed. Washington, DC: National Academies Press.
16.Metzler-Zebeli, BU, Newman, MA, Grüll, D, et al. (2018) Consumption of transglycosylated starch down-regulates expression of mucosal innate immune response genes in the large intestine using a pig model. Br J Nutr 119, 13661377.
17.AOAC (2006) Official Methods of Analysis, 18th ed. Arlington, VA: Association of Official Analytical Chemists.
18.Naumann, C & Basler, R (2012) Die Chemische Untersuchung von Futtermitteln (The Chemical Investigation of Feed), 3rd ed. Darmstadt, Germany: VDLUFA Verlag.
19.Khol-Parisini, A, Humer, E, Sizmaz, Ö, et al. (2015) Ruminal disappearance of phosphorus and starch, reticuloruminal pH and total tract nutrient digestibility in dairy cows fed diets differing in grain processing. Anim Feed Sci Technol 210, 7485.
20.Zebeli, Q, Tafaj, M, Weber, I, et al. (2007) Effects of varying dietary forage particle size in two concentrate levels on chewing activity, ruminal mat characteristics, and passage in dairy cows. J Dairy Sci 90, 19291942.
21.Metzler-Zebeli, BU, Lawlor, PG, Magowan, E, et al. (2016) Effect of freezing conditions on fecal bacterial composition in pigs. Animals (Basel) 6, E18.
22.Caporaso, JG, Kuczynski, J, Stombaugh, J, et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7, 335336.
23.Edgar, RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 24602461.
24.Edgar, RC, Haas, BJ, Clemente, JC, et al. (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 21942200.
25.Love, MI, Huber, W & Anders, S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology 15, 550.
26.Huber, W, Carey, JV, Gentleman, R, et al. (2015) Orchestrating high-throughput genomic analysis with Bioconductor. Nat Methods 12, 115121.
27.Benjamini, Y & Hochberg, Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 57, 289300.
28.Oksanen, J, Blanchet, FG, Friendly, M, et al. (2018) Vegan: Community Ecology Package. R Package Version 2.4-3. https://cran.r-project.org/web/packages/vegan/index.html (accessed October 2018)
29.Lê Cao, K-A, Costello, M-E, Lakis, VA, et al. (2016) MixMC: a multivariate statistical framework to gain insight into microbial communities. PLOS ONE 11, e0160169.
30.Rohart, F, Gautier, B, Singh, A, et al. (2017) mixOmics: an R package for ‘omics feature selection and multiple data integration. PLoS Comput Biol 13, e1005752.
31.Kononoff, PJ & Hanford, KJ (2006) Technical note: estimating statistical power of mixed models used in dairy nutrition experiments. J Dairy Sci 89, 39683971.
32.Regmi, PR, Metzler-Zebeli, BU, Gänzle, MG, et al. (2011) Starch with high amylose content and low in vitro digestibility increases intestinal nutrient flow and microbial fermentation and selectively promotes bifidobacteria in pigs. J Nutr 141, 398405.
33.Fouhse, JM, Gänzle, MG, Beattie, AD, et al. (2017) Whole-grain starch and fiber composition modifies ileal flow of nutrients and nutrient availability in the hindgut, shifting fecal microbial profiles in pigs. J Nutr 147, 20312040.
34.Rashid, T, Wilson, C & Ebringer, A (2013) The link between ankylosing spondylitis, Crohn’s disease, Klebsiella, and starch consumption. Clin Dev Immunol 2013, 872632.
35.Metzler-Zebeli, BU, Newman, MA & Zebeli, Q (2018) Transglycosylated starch modifies the cecal bacterial metagenome and gene abundance of key catabolic enzymes for bacterial starch metabolism in pigs. In 11th Rowett-INRA Conference - Gut Microbiology. Aberdeen, UK, p. 29.
36.Prins, RA (1971) Isolation, culture, and fermentation characteristics of Selenomonas ruminantium var. bryantivar. n. from the rumen of sheep. J Bacteriol 105, 820825.
37.Gänzle, MG & Follador, R (2012) Metabolism of oligosaccharides and starch in lactobacilli: a review. Front Microbiol 3, 340.
38.Clavel, T, Lepage, P & Charrier, F (2014) The family Coriobacteriaceae. In The Prokaryotes, 4th ed., pp. 201238 [Rosenberg, E, DeLong, EF, Lory, S, Stackebrandt, E and Thompson, F, editors]. Berlin Heidelberg, Germany: Springer-Verlag.
39.Walter, J, Martínez, I & Rose, DJ (2013) Holobiont nutrition: considering the role of the gastrointestinal microbiota in the health benefits of whole grains. Gut Microbes 4, 340346.
40.Carlson, JL, Erickson, JM, Hess, JM, et al. (2017) Prebiotic dietary fiber and gut health: comparing the in vitro fermentations of beta-Glucan, inulin and xylooligosaccharide. Nutrients 9, E1361.
41.Martínez, I, Lattimer, JM, Hubach, KL, et al. (2013) Gut microbiome composition is linked to whole grain-induced immunological improvements. ISME J 7, 269280.
42.Flint, HJ, Duncan, SH, Scott, KP, et al. (2015) Links between diet, gut microbiota composition and gut metabolism. Proc Nutr Soc 74, 1322.
43.Shetty, SA, Marathe, NP, Lanjekar, V, et al. (2013) Comparative genome analysis of Megasphaera sp. reveals niche specialization and its potential role in the human gut. PLOS ONE 8, e79353.
44.Gophna, U, Konikoff, T & Nielsen, HB (2017) Oscillospira and related bacteria - from metagenomic species to metabolic features. Environ Microbiol 19, 835841.
45.O’Hea, EK & Leveille, GA (1969) Significance of adipose tissue and liver as sites of fatty acid synthesis in pig and efficiency of utilization of various substrates for lipogenesis. J Nutr 99, 338344.
46.Morrison, DJ & Preston, T (2016) Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism. Gut Microbes 7, 189200.
47.Windey, K, De Preter, V & Verbeke, K (2016) Relevance of protein fermentation to gut health. Mol Nutr Food Res 56, 184196.
48.Yao, CK, Muir, JG & Gibson, PR (2016) Review article: insights into colonic protein fermentation, its modulation and potential health implications. Aliment Pharmacol Ther 43, 181196.
49.Metzler, 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, 603615.

Keywords

Type Description Title
PDF
Supplementary materials

Metzler-Zebeli et al. supplementary material
Tables S1-S7 and Figures S1-S3

 PDF (321 KB)
321 KB

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed