Modulation of the microbial fermentation in the gut by fermentable carbohydrates

Bioactive Carbohydrates and Dietary Fibre

Volumn 2, Issue 2, 2013, Pages 133-142

  Hugenholtz, Floor ^a,b,c   Mullaney, Jane Adair ^d,e,f   Kleerebezem, Michiel ^a,b,c   Smidt, Hauke ^a,b,c   Rosendale, Douglas Ian ^d  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c TOP INSTITUTE FOOD AND NUTRITION   (Netherlands)

^d THE NEW ZEALAND INSTITUTE FOR PLANT AND FOOD RESEARCH LIMITED   (New Zealand)

^e AGRESEARCH GRASSLANDS   (New Zealand)

^f MASSEY UNIVERSITY   (New Zealand)

Author keywords

Fermentable carbohydrates; Health; Microbiota; Short chain fatty acids

Indexed keywords

ACETIC ACID; BUTYRIC ACID; CARBOHYDRATE; GLUCOSINOLATE; GLYCAN DERIVATIVE; LACTIC ACID; POLYPHENOL DERIVATIVE; PROPIONIC ACID; SHORT CHAIN FATTY ACID; SUCCINIC ACID;

ANAEROBIC FERMENTATION; CANCER RISK; CARBOHYDRATE DIET; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; DIETARY FIBER; GASTROINTESTINAL DISEASE; HEALTH; HUMAN; INTESTINE FLORA; MALIGNANT NEOPLASTIC DISEASE; MICROBIAL DIVERSITY; MODULATION; NONHUMAN; ORGANISMAL INTERACTION; PRIORITY JOURNAL; REVIEW;

EID: 84887054375     PISSN: 22126198     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcdf.2013.09.008     Document Type: Review

References (79)

1. G.C. Abell, C.M. Cooke, C.N. Bennett, M.A. Conlon, and A.L. McOrist Phylotypes related to Ruminococcus bromii are abundant in the large bowel of humans and increase in response to a diet high in resistant starch FEMS Microbiology Ecology 66 3 2008 505 515
2. H.R. Attebery, V.L. Sutter, and S.M. Finegold Effect of a partially chemically defined diet on normal human fecal flora American Journal of Clinical Nutrition 25 12 1972 1391 1398
3. C.C. Booijink, E.G. Zoetendal, M. Kleerebezem, and W.M. de Vos Microbial communities in the human small intestine: Coupling diversity to metagenomics [review] Future Microbiology 2 3 2007 285 295
4. G. Bounous, and G.J. Devroede Effects of an elemental diet on human fecal flora Gastroenterology 66 2 1974 210 214
5. J.D. Brooks, V.G. Paton, and G. Vidanes Potent induction of phase 2 enzymes in human prostate cells by sulforaphane Cancer Epidemiology Biomarkers & Prevention 10 9 2001 949 954
6. Cook, and Sellin Review article: Short chain fatty acids in health and disease Alimentary Pharmacology & Therapeutics 12 6 1998 499 507
7. A. Costabile, S. Kolida, A. Klinder, E. Gietl, M. Bauerlein, and C. Frohberg A double-blind, placebo-controlled, cross-over study to establish the bifidogenic effect of a very-long-chain inulin extracted from globe artichoke (Cynara scolymus) in healthy human subjects British Journal of Nutrition 104 7 2010 1007 1017
8. J.H. Cummings Short chain fatty acids in the human colon [review] Gut 22 9 1981 763 779
9. J.H. Cummings, and G.T. Macfarlane The control and consequences of bacterial fermentation in the human colon [review] Journal of applied bacteriology 70 6 1991 443 459
10. S.H. Duncan, P. Louis, and H.J. Flint Lactate-utilizing bacteria, isolated from human feces, that produce butyrate as a major fermentation product Applied and Environmental Microbiology 70 10 2004 5810 5817
11. A. Everard, C. Belzer, L. Geurts, J.P. Ouwerkerk, C. Druart, and L.B. Bindels Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity Proceedings of the National Academy of Sciences USA 110 22 2013 9066 9071
12. F. Fava, J.A. Lovegrove, K.M. Tuohy, and G.R. Gibson The potential role of the intestinal gut microbiota in obesity and the metabolic syndrome Food Science and Technology Bulletin: Functional Foods 5 7 2008 71 92
13. L.R. Ferguson, C. Tasman-Jones, H. Englyst, and P.J. Harris Comparative effects of three resistant starch preparations on transit time and short-chain fatty acid production in rats Nutrition and Cancer 36 2 2000 230 237
14. W.M. Fernando, J.E. Hill, G.A. Zello, R.T. Tyler, W.J. Dahl, and A.G. Van Kessel Diets supplemented with chickpea or its main oligosaccharide component raffinose modify faecal microbial composition in healthy adults Beneficial Microbes 1 2 2010 197 207
15. S.M. Finegold, V.L. Sutter, and G.E. Mathisen Normal indigenous intestinal flora D.J. Hentges, Human Intestinal Flora in Health and Disease 1983 Academic Press London 3 31
16. H.J. Flint, and E.A. Bayer Plant cell wall breakdown by anaerobic microorganisms from the mammalian digestive tract Annals of the New York Academy of Sciences 1125 2008 280 288
17. H.J. Flint, K.P. Scott, S.H. Duncan, P. Louis, and E. Forano Microbial degradation of complex carbohydrates in the gut Gut Microbes 3 4 2012 289 306
18. H.J. Flint, K.P. Scott, P. Louis, and S.H. Duncan The role of the gut microbiota in nutrition and health Nature Reviews Gastroenterology & Hepatology 9 10 2012 577 589
19. G.R. Gibson, and M.B. Roberfroid Dietary modulation of the human colonic microbiota: Introducing the concept of prebiotics Journal of Nutrition 125 6 1995 1401 1412
20. S. Greenblum, P.J. Turnbaugh, and E. Borenstein Metagenomic systems biology of the human gut microbiome reveals topological shifts associated with obesity and inflammatory bowel disease Proceedings of the National Academy of Sciences USA 109 2 2012 594 599
21. C. Grootaert, P. Van den Abbeele, M. Marzorati, W.F. Broekaert, C.M. Courtin, and J.A. Delcour Comparison of prebiotic effects of arabinoxylan oligosaccharides and inulin in a simulator of the human intestinal microbial ecosystem FEMS Microbiology Ecology 69 2 2009 231 242
22. D. Haenen, J. Zhang, C. Souza da Silva, G. Bosch, I.M. van der Meer, and J. van Arkel A diet high in resistant starch modulates microbiota composition, SCFA concentrations, and gene expression in pig intestine Journal of Nutrition 143 3 2013 274 283
23. L.V. Hooper, T. Midtvedt, and J.I. Gordon How host-microbial interactions shape the nutrient environment of the mammalian intestine [review] Annual Review of Nutrition 22 2002 283 307
24. L.C. Hoskins, and E.T. Boulding Degradation of blood group antigens in human colon ecosystems I. In vitro production of ABO blood group-degrading enzymes by enteric bacteria Journal of Clinical Investigation 57 1976 63 73
25. L.C. Hoskins, M. Agustines, W.B. McKee, E.T. Boulding, M. Kriaris, and G. Neidermeyer Mucin degradation in human colon ecosystems. Isolation and properties of fecal strains that degrade ABH blood group antigens and oligosaccharides from mucin glycoproteins Journal of Clinical Investigations 75 1985 944 953
26. M. Hudson, S. Borriello, and M. Hill Elemental diets and the bacterial flora of the gastrointestinal tract 1981 CRC Press Boca Raton, FL
27. B. Kleessen, S. Schwarz, A. Boehm, H. Fuhrmann, A. Richter, and T. Henle Jerusalem artichoke and chicory inulin in bakery products affect faecal microbiota of healthy volunteers British Journal of Nutrition 98 3 2007 540 549
28. P. Kovatcheva-Datchary, M. Egert, A. Maathuis, R. Rajilic-Stojanovic, A.A. de Graat, and H. Smidt Linking phylogenetic identities of bacteria to starch fermentation in an in vitro model of the large intestine by RNA-based stable isotope probing Environmental Microbiology 11 4 2009 914 926
29. P.A. Kroon, M.N. Clifford, A. Crozier, A.J. Day, J.L. Donovan, and C. Manach How should we assess the effects of exposure to dietary polyphenols in vitro? American Journal of Clinical Nutrition 80 1 2004 15 21
30. F.M. Larsen, P.J. Moughan, and M.N. Wilson Dietary fiber viscosity and endogenous protein excretion at the terminal ileum of growing rats Journal of Nutrition 123 11 1993 1898 1904
31. H.V. Lin, A. Frassetto, E.J. Kowalik Jr., A.R. Nawrocki, M.M. Lu, and J.R. Kosinski Butyrate and propionate protect against diet-induced obesity and regulate gut hormones via free fatty acid receptor 3-independent mechanisms PLoS ONE 7 4 2012 e35240
32. P. Louis, K.P. Scott, S.H. Duncan, and H.J. Flint Understanding the effects of diet on bacterial metabolism in the large intestine Journal of Applied Microbiology 102 5 2007 1197 1208
33. G.T. Macfarlane, S. Hay, and G.R. Gibson Influence of mucin on glycosidase, protease and arylamidase activities of human gut bacteria grown in a 3-stage continuous culture system Journal of Applied Microbiology 66 5 1989 407 417
34. S. Macfarlane, and G.T. Macfarlane Regulation of short-chain fatty acid production Proceedings of the Nutrition Society 62 1 2003 67 72
35. S. Macfarlane, and G.T. Macfarlane Composition and metabolic activities of bacterial biofilms colonizing food residues in the human gut Applied and Environmental Microbiology 72 9 2006 6204 6211
36. H. Makivuokko, S. Lahtinen, P. Wacklin, E. Tuovinen, H. Tenkanen, and J. Nikkila Association between the ABO blood group and the human intestinal microbiota composition BMC Microbiology 12 1 2012 94
37. C. Manach, A. Scalbert, C. Morand, C. Rémésy, and L. Jiménez Polyphenols: Food sources and bioavailability American Journal of Clinical Nutrition 79 5 2004 727 747
38. E.C. Martens, R. Roth, J.E. Heuser, and J.I. Gordon Coordinate regulation of glycan degradation and polysaccharide capsule biosynthesis by a prominent human gut symbiont Journal of Biological Chemistry 284 27 2009 18445 18457
39. F.P. Martin, M.E. Dumas, Y. Wang, C. Legido-Quigley, I.K. Yap, and H. Tang A top-down systems biology view of microbiome-mammalian metabolic interactions in a mouse model Molecular Systems Biology 3 2007 112
40. F.P. Martin, N. Sprenger, I.K. Yap, Y. Wang, R. Bibiloni, and F. Rochat Panorganismal gut microbiome-host metabolic crosstalk Journal of Proteome Research 8 4 2009 2090 2105
41. F.-P.J. Martin, Y. Wang, N. Sprenger, I.K.S. Yap, T. Lundstedt, and P. Lek Probiotic modulation of symbiotic gut microbial-host metabolic interactions in a humanized microbiome mouse model Molecular Systems Biology 4 2008 1 15
42. C.L. Maynard, C.O. Elson, R.D. Hatton, and C.T. Weaver Reciprocal interactions of the intestinal microbiota and immune system Nature 489 7415 2012 231 241
43. A.L. McOrist, R.B. Miller, A.R. Bird, J.B. Keogh, M. Noakes, and D.L. Topping Fecal butyrate levels vary widely among individuals but are usually increased by a diet high in resistant starch Journal of Nutrition 141 5 2011 883 889
44. T.L. Miller, and M.J. Wolin Fermentations by saccharolytic intestinal bacteria American Journal of Clinical Nutrition 32 1 1979 164 172
45. W.E. Moore, and L.V. Holdeman Human fecal flora: The normal flora of 20 Japanese-Hawaiians Applied Microbiology 27 5 1974 961 979
46. B.D. Muegge, J. Kuczynski, D. Knights, J.C. Clemente, A. Gonzalez, and L. Fontana Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans Science 332 6032 2011 970 974
47. J.A. Mullaney The biotransformation of glucosinolates from a bacterial perspective 2013 Massey Palmerston North ([Ph.D. thesis])
48. J.A. Mullaney, J. Ansell, W.J. Kelly, and J.A. Heyes The biotransformation of glucosinolates from a bacterial perspective [review] CAB Reviews, 8 034 2013 1 15 10.1079/PAVSNNR20138034
49. R. Muñoz-Tamayo, B. Laroche, É. Walter, J. Doré, S.H. Duncan, and H.J. Flint Kinetic modelling of lactate utilization and butyrate production by key human colonic bacterial species FEMS Microbiology Ecology 76 3 2011 615 624
50. A.C. Ouwehand, M. Derrien, W. de Vos, K. Tiihonen, and N. Rautonen Prebiotics and other microbial substrates for gut functionality [review] Current Opinion in Biotechnology 16 2 2005 212 217
51. M. Parter, N. Kashtan, and U. Alon Environmental variability and modularity of bacterial metabolic networks BMC Evolutionary Biology 7 2007 169
52. J.L. Pluznick, R.J. Protzko, H. Gevorgyan, Z. Peterlin, A. Sipos, and J. Han Olfactory receptor responding to gut microbiota-derived signals plays a role in renin secretion and blood pressure regulation Proceedings of the National Academy of Sciences of the United States of America 110 11 2013 4410 4415
53. J. Qin, R. Li, J. Raes, M. Arumugam, K.S. Burgdorf, and C. Manichanh A human gut microbial gene catalogue established by metagenomic sequencing Nature 464 7285 2010 59 65
54. M. Rajilic-Stojanovic, H. Smidt, and W.M. de Vos Diversity of the human gastrointestinal tract microbiota revisited [review] Environmental Microbiology 9 9 2007 2125 2136
55. C. Ramirez-Farias, K. Slezak, Z. Fuller, A. Duncan, G. Holtrop, and P. Louis Effect of inulin on the human gut microbiota: Stimulation of Bifidobacterium adolescentis and Faecalibacterium prausnitzii British Journal of Nutrition 101 4 2009 541 550
56. J.F. Rawls, M.A. Mahowald, R.E. Ley, and J.I. Gordon Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection Cell 127 2 2006 423 433
57. A. Reyes, M. Haynes, N. Hanson, F.E. Angly, A.C. Heath, and F. Rohwer Viruses in the faecal microbiota of monozygotic twins and their mothers Nature 466 7304 2010 334 338
58. D.I. Rosendale, A. Cookson, N. Roy, and I. Vetharaniam Opportunities for predictive modelling and gut health. Conceptually exploring an in silico tool for quantifying the benefits of dietary fibre consumption [review] AgroFOOD industry hi-tech 22 6 2011 18 22
59. J.L. Round, and S.K. Mazmanian The gut microbiota shapes intestinal immune responses during health and disease Nature Reviews Immunology 9 5 2009 313 323
60. D. Scharlau, A. Borowicki, N. Habermann, T. Hofmann, S. Klenow, and C. Miene Mechanisms of primary cancer prevention by butyrate and other products formed during gut flora-mediated fermentation of dietary fibre Mutation Research 682 1 2009 39 53
61. W. Scheppach Effects of short chain fatty acids on gut morphology and function Gut 35 Suppl. 1 1994 S35 S38
62. W. Scheppach, J.G. Müller, F. Boxberger, G. Dusel, F. Richter, and H.P. Bartram Histological changes in the colonic mucosa following irrigation with short-chain fatty acids European Journal of Gastroenterology and Hepatology 2 9 1997 163 168
63. W. Scheppach, H. Sommer, T. Kirchner, G.M. Paganelli, P. Bartram, and S. Christl Effect of butyrate enemas on the colonic mucosa in distal ulcerative colitis Gastroenterology 1 103 1992 51 56
64. A. Schwiertz, U. Lehmann, G. Jacobasch, and M. Blaut Influence of resistant starch on the SCFA production and cell counts of butyrate-producing Eubacterium spp. in the human intestine Journal of Applied Microbiology 93 1 2002 157 162
65. J.L. Sonnenburg, J. Xu, D.D. Leip, C.H. Chen, B.P. Westover, and J. Weatherford Glycan foraging in vivo by an intestine-adapted bacterial symbiont Science 307 5717 2005 1955 1959
66. C.E. Stevens, and I.D. Hume Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients [review] Physiological Reviews 78 2 1998 393 427
67. L. Tasse, J. Bercovici, S. Pizzut-Serin, P. Robe, J. Tap, and C. Klopp Functional metagenomics to mine the human gut microbiome for dietary fiber catabolic enzymes Genome Research 20 11 2010 1605 1612
68. O. Thompson-Chagoyán, J. Maldonado, and A. Gil Colonization and impact of disease and other factors on intestinal microbiota Digestive Diseases and Sciences 52 9 2007 2069 2077
69. B. Tirosh, and A. Rubinstein Migration of adhesive and nonadhesive particles in the rat intestine under altered mucus secretion conditions Journal of Pharmaceutical Sciences 87 4 1998 453 456
70. D.L. Topping, and P.M. Clifton Short-chain fatty acids and human colonic function: Roles of resistant starch and nonstarch polysaccharides [review] Physiological Reviews 81 3 2001 1031 1064
71. P. Van den Abbeele, P. Gerard, S. Rabot, A. Bruneau, S. El Aidy, and M. Derrien Arabinoxylans and inulin differentially modulate the mucosal and luminal gut microbiota and mucin-degradation in humanized rats Environmental Microbiology 13 10 2011 2667 2680
72. B. van den Bogert, W.M. de Vos, E.G. Zoetendal, and M. Kleerebezem Microarray analysis and barcoded pyrosequencing provide consistent microbial profiles depending on the source of human intestinal samples Applied and Environmental Microbiology 77 6 2011 2071 2080
73. G.C. van Zanten, A. Knudsen, H. Röytiö, S. Forssten, M. Lawther, and A. Blennow The effect of selected synbiotics on microbial composition and short-chain fatty acid production in a model system of the human colon PLoS ONE 7 10 2012 e47212
74. E. Variyam, and L. Hoskins In vitro degradation of gastric mucin. Carbohydrate side chains protect glycopeptides core from pancreatic proteases Gastroenterology 84 1983 533 537
75. J. Walter, and R. Ley The human gut microbiome: Ecology and recent evolutionary changes Annual Review of Microbiology 65 2011 411 429
76. G.E. Walton, C. Lu, I. Trogh, F. Arnaut, and G.R. Gibson A randomised, double-blind, placebo controlled cross-over study to determine the gastrointestinal effects of consumption of arabinoxylan-oligosaccharides enriched bread in healthy volunteers Nutrition Journal 11 2012 36
77. M. Winitz, R.F. Adams, D.A. Seedman, P.N. Davis, L.G. Jayko, and J.A. Hamilton Studies in metabolic nutrition employing chemically defined diets. II. Effects on gut microflora populations American Journal of Clinical Nutrition 23 5 1970 546 559
78. J.M. Wong, R. de Souza, C.W. Kendall, A. Emam, and D.J. Jenkins Colonic health: Fermentation and short chain fatty acids [review] Journal of Clinical Gastroenterology 40 3 2006 235 243
79. E.G. Zoetendal, J. Raes, B. van den Bogert, M. Arumugam, C.C. Booijink, and F.J. Troost The human small intestinal microbiota is driven by rapid uptake and conversion of simple carbohydrates ISME Journal 6 7 2012 1415 1426