Metabolic Fate of 13C-Labeled Polydextrose and Impact on the Gut Microbiome: A Triple-Phase Study in a Colon Simulator

Journal of Proteome Research

Volumn 17, Issue 3, 2018, Pages 1041-1053

  Lamichhane, Santosh ^a,d   Yde, Christian C ^a,b   Jensen, Henrik Max ^b   Morovic, Wesley ^b   Hibberd, Ashley A ^b   Ouwehand, Arthur C ^b   Saarinen, Markku T ^b   Forssten, Sofia D ^b   Wiebe, Lars ^b   Marcussen, Jørn ^b   Bertelsen, Kresten ^b,e   Meier, Sebastian ^c   Young, Jette F ^a   Bertram, Hanne Christine ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b DUPONT COMPANY   (United States)

^c TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^d UNIVERSITY OF TURKU   (Finland)

^e VESTAS WIND SYSTEMS A S   (Denmark)

Author keywords

13C NMR; 13C labeled metabolites; dietary fiber; gut microbiome

Indexed keywords

ACETIC ACID; ALCOHOL; BUTYRIC ACID; DNA 16S; FORMIC ACID; GLUCOSE; LACTIC ACID; POLYDEXTROSE; PROPIONIC ACID; RNA 16S; SHORT CHAIN FATTY ACID; SUCCINIC ACID; UNCLASSIFIED DRUG; VALERIC ACID; CARBON; FORMIC ACID DERIVATIVE; GLUCAN; VOLATILE FATTY ACID;

ANAEROBIC FERMENTATION; ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; COLON; CONTROLLED STUDY; DIETARY FIBER; ERYSIPELOTRICHACEAE; FERMENTATION; GAS; INTESTINE FLORA; LIQUID; MICROBIAL DIVERSITY; PRIORITY JOURNAL; SIMULATION; SOLID; ADMINISTRATION AND DOSAGE; ANAEROBIC GROWTH; BIOREACTOR; BIOTRANSFORMATION; ERYSIPELOTHRIX; FECES; GENETICS; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; METABOLOME; MICROBIAL CONSORTIUM; MICROBIOLOGY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHYSIOLOGY;

ANAEROBIOSIS; BIOREACTORS; BIOTRANSFORMATION; CARBON ISOTOPES; COLON; DIETARY FIBER; ERYSIPELOTHRIX; ETHANOL; FATTY ACIDS, VOLATILE; FECES; FERMENTATION; FORMATES; GASTROINTESTINAL MICROBIOME; GLUCANS; HUMANS; LACTIC ACID; MAGNETIC RESONANCE SPECTROSCOPY; METABOLOME; MICROBIAL CONSORTIA; RNA, RIBOSOMAL, 16S; SUCCINIC ACID;

EID: 85042854762     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.7b00683     Document Type: Article

References (66)

1. Sonnenburg, J. L.; Backhed, F. Diet-microbiota interactions as moderators of human metabolism Nature 2016, 535 (7610) 56-64 10.1038/nature18846
2. Rooks, M. G.; Garrett, W. S. Gut microbiota, metabolites and host immunity Nat. Rev. Immunol. 2016, 16 (6) 341-352 10.1038/nri.2016.42
3. Nicholson, J. K.; Holmes, E.; Kinross, J.; Burcelin, R.; Gibson, G.; Jia, W.; Pettersson, S. Host-Gut Microbiota Metabolic Interactions Science 2012, 336 (6086) 1262-1267 10.1126/science.1223813
4. Nyangale, E. P.; Mottram, D. S.; Gibson, G. R. Gut Microbial Activity, Implications for Health and Disease: The Potential Role of Metabolite Analysis J. Proteome Res. 2012, 11 (12) 5573-5585 10.1021/pr300637d
5. Slavin, J. Fiber and prebiotics: mechanisms and health benefits Nutrients 2013, 5 (4) 1417-35 10.3390/nu5041417
6. Lamichhane, S.; Westerhuis, J. A.; Ouwehand, A. C.; Saarinen, M. T.; Forssten, S. D.; Jensen, H. M.; Young, J. F.; Bertram, H. C.; Yde, C. C. Gut microbial activity as influenced by fiber digestion: dynamic metabolomics in an in vitro colon simulator Metabolomics 2016, 12 (2) 25 10.1007/s11306-015-0936-y
7. De Leoz, M. L. A.; Kalanetra, K. M.; Bokulich, N. A.; Strum, J. S.; Underwood, M. A.; German, J. B.; Mills, D. A.; Lebrilla, C. B. Human Milk Glycomics and Gut Microbial Genomics in Infant Feces Show a Correlation between Human Milk Oligosaccharides and Gut Microbiota: A Proof-of-Concept Study J. Proteome Res. 2015, 14 (1) 491-502 10.1021/pr500759e
8. Scalabrin, D. M.; Mitmesser, S. H.; Welling, G. W.; Harris, C. L.; Marunycz, J. D.; Walker, D. C.; Bos, N. A.; Tolkko, S.; Salminen, S.; Vanderhoof, J. A. New prebiotic blend of Polydextrose and galacto-oligosaccharides has a bifidogenic effect in young infants J. Pediatr. Gastroenterol. Nutr. 2012, 54 (3) 343-352 10.1097/MPG.0b013e318237ed95
9. do Carmo, M. M.; Walker, J. C.; Novello, D.; Caselato, V. M.; Sgarbieri, V. C.; Ouwehand, A. C.; Andreollo, N. A.; Hiane, P. A.; Dos Santos, E. F. Polydextrose: Physiological Function, and Effects on Health Nutrients 2016, 8 (9) 553 10.3390/nu8090553
10. Oberbach, A.; Haange, S.-B.; Schlichting, N.; Heinrich, M.; Lehmann, S.; Till, H.; Hugenholtz, F.; Kullnick, Y.; Smidt, H.; Frank, K.; Seifert, J.; Jehmlich, N.; von Bergen, M. Metabolic in Vivo Labeling Highlights Differences of Metabolically Active Microbes from the Mucosal Gastrointestinal Microbiome between High-Fat and Normal Chow Diet J. Proteome Res. 2017, 16 (4) 1593-1604 10.1021/acs.jproteome.6b00973
11. de Graaf, A. A.; Maathuis, A.; de Waard, P.; Deutz, N. E.; Dijkema, C.; de Vos, W. M.; Venema, K. Profiling human gut bacterial metabolism and its kinetics using [U-13C]glucose and NMR NMR Biomed. 2010, 23 (1) 2-12 10.1002/nbm.1418
12. Yamazawa, A.; Iikura, T.; Shino, A.; Date, Y.; Kikuchi, J. Solid-, Solution-, and Gas-state NMR Monitoring of 13C-Cellulose Degradation in an Anaerobic Microbial Ecosystem Molecules 2013, 18 (8) 9021 10.3390/molecules18089021
13. Butts, C. A.; Paturi, G.; Tavendale, M. H.; Hedderley, D.; Stoklosinski, H. M.; Herath, T. D.; Rosendale, D.; Roy, N. C.; Monro, J. A.; Ansell, J. The fate of 13C-labelled and non-labelled inulin predisposed to large bowel fermentation in rats Food Funct. 2016, 7 (4) 1825-1832 10.1039/C5FO01056J
14. Forssten, S. D.; Roytio, H.; Hibberd, A. A.; Ouwehand, A. C. The effect of Polydextrose and probiotic lactobacilli in a Clostridium difficile-infected human colonic model Microb. Ecol. Health Dis. 2015, 26, 27988 10.3402/mehd.v26.27988
15. van Zanten, G. C.; Knudsen, A.; Roytio, H.; Forssten, S.; Lawther, M.; Blennow, A.; Lahtinen, S. J.; Jakobsen, M.; Svensson, B.; Jespersen, L. The effect of selected synbiotics on microbial composition and short-chain fatty acid production in a model system of the human colon PLoS One 2012, 7 (10) e47212 10.1371/journal.pone.0047212
16. Mäkivuokko, H.; Nurmi, J.; Nurminen, P.; Stowell, J.; Rautonen, N. In vitro effects on Polydextrose by colonic bacteria and caco-2 cell cyclooxygenase gene expression Nutr. Cancer 2005, 52 (1) 94-104 10.1207/s15327914nc5201-12
17. Jacobs, D. M.; Deltimple, N.; van Velzen, E.; van Dorsten, F. A.; Bingham, M.; Vaughan, E. E.; van Duynhoven, J. 1H NMR metabolite profiling of feces as a tool to assess the impact of nutrition on the human microbiome NMR Biomed. 2008, 21 (6) 615-626 10.1002/nbm.1233
18. Wishart, D. S.; Jewison, T.; Guo, A. C.; Wilson, M.; Knox, C.; Liu, Y.; Djoumbou, Y.; Mandal, R.; Aziat, F.; Dong, E.; Bouatra, S.; Sinelnikov, I.; Arndt, D.; Xia, J.; Liu, P.; Yallou, F.; Bjorndahl, T.; Perez-Pineiro, R.; Eisner, R.; Allen, F.; Neveu, V.; Greiner, R.; Scalbert, A. HMDB 3.0-The Human Metabolome Database in 2013 Nucleic Acids Res. 2012, 41 (D11) 801-807 10.1093/nar/gks1065
19. Savorani, F.; Tomasi, G.; Engelsen, S. B. icoshift: A versatile tool for the rapid alignment of 1D NMR spectra J. Magn. Reson. 2010, 202 (2) 190-202 10.1016/j.jmr.2009.11.012
20. Morovic, W.; Hibberd, A. A.; Zabel, B.; Barrangou, R.; Stahl, B. Genotyping by PCR and High-Throughput Sequencing of Commercial Probiotic Products Reveals Composition Biases Front. Microbiol. 2016, 7 (1747) 328 10.3389/fmicb.2016.01747
21. Caporaso, J. G.; Kuczynski, J.; Stombaugh, J.; Bittinger, K.; Bushman, F. D.; Costello, E. K.; Fierer, N.; Peña, A. G.; Goodrich, J. K.; Gordon, J. I.; Huttley, G. A.; Kelley, S. T.; Knights, D.; Koenig, J. E.; Ley, R. E.; Lozupone, C. A.; McDonald, D.; Muegge, B. D.; Pirrung, M.; Reeder, J.; Sevinsky, J. R.; Turnbaugh, P. J.; Walters, W. A.; Widmann, J.; Yatsunenko, T.; Zaneveld, J.; Knight, R. QIIME allows analysis of high-throughput community sequencing data Nat. Methods 2010, 7 (5) 335-356 10.1038/nmeth.f.303
22. Aronesty, E. ea-utils: Command-line tools for processing biological sequencing data, 2011. https://expressionanalysis.github.io/ea-utils/.
23. Edgar, R. C. Search and clustering orders of magnitude faster than BLAST Bioinformatics 2010, 26 (19) 2460-1 10.1093/bioinformatics/btq461
24. DeSantis, T. Z.; Hugenholtz, P.; Larsen, N.; Rojas, M.; Brodie, E. L.; Keller, K.; Huber, T.; Dalevi, D.; Hu, P.; Andersen, G. L. Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB Appl. Environ. Microbiol. 2006, 72 (7) 5069-5072 10.1128/AEM.03006-05
25. Caporaso, J. G.; Bittinger, K.; Bushman, F. D.; DeSantis, T. Z.; Andersen, G. L.; Knight, R. PyNAST: a flexible tool for aligning sequences to a template alignment Bioinformatics 2010, 26 (2) 266-7 10.1093/bioinformatics/btp636
26. Price, M. N.; Dehal, P. S.; Arkin, A. P. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix Mol. Biol. Evol. 2009, 26 (7) 1641-1650 10.1093/molbev/msp077
27. Faith, D. P.; Baker, A. M. Phylogenetic diversity (PD) and biodiversity conservation: some bioinformatics challenges Evol. Bioinf. Online 2006, 2, 121-128 10.1177/117693430600200007
28. Lozupone, C.; Knight, R. UniFrac: a new phylogenetic method for comparing microbial communities Appl. Environ. Microbiol. 2005, 71 (12) 8228-8235 10.1128/AEM.71.12.8228-8235.2005
29. Koh, A.; De Vadder, F.; Kovatcheva-Datchary, P.; Bäckhed, F. From Dietary Fiber to Host Physiology: Short-Chain Fatty Acids as Key Bacterial Metabolites Cell 2016, 165 (6) 1332-1345 10.1016/j.cell.2016.05.041
30. Jie, Z.; Bang-yao, L.; Ming-jie, X.; Hai-wei, L.; Zu-kang, Z.; Ting-song, W.; Craig, S. A. S. Studies on the effects of Polydextrose intake on physiologic funtions in Chinese people Am. J. Clin. Nutr. 2000, 72 (6) 1503-1509
31. Beloshapka, A. N.; Wolff, A. K.; Swanson, K. S. Effects of feeding Polydextrose on faecal characteristics, microbiota and fermentative end products in healthy adult dogs Br. J. Nutr. 2012, 108 (4) 638-644 10.1017/S0007114511005927
32. Canani, R. B.; Costanzo, M. D.; Leone, L.; Pedata, M.; Meli, R.; Calignano, A. Potential beneficial effects of butyrate in intestinal and extraintestinal diseases World J. Gastroenterol 2011, 17 (12) 1519-1528 10.3748/wjg.v17.i12.1519
33. Leonel, A. J.; Alvarez-Leite, J. I. Butyrate: implications for intestinal function Curr. Opin. Clin. Nutr. Metab. Care 2012, 15 (5) 474-479 10.1097/MCO.0b013e32835665fa
34. Fernandes, J.; Su, W.; Rahat-Rozenbloom, S.; Wolever, T. M. S.; Comelli, E. M. Adiposity, gut microbiota and faecal short chain fatty acids are linked in adult humans Nutr. Diabetes 2014, 4, e121 10.1038/nutd.2014.23
35. Wang, J.; Tang, H.; Zhang, C.; Zhao, Y.; Derrien, M.; Rocher, E.; van-Hylckama Vlieg, J. E.; Strissel, K.; Zhao, L.; Obin, M.; Shen, J. Modulation of gut microbiota during probiotic-mediated attenuation of metabolic syndrome in high fat diet-fed mice ISME J. 2015, 9 (1) 1-15 10.1038/ismej.2014.99
36. De Filippo, C.; Cavalieri, D.; Di Paola, M.; Ramazzotti, M.; Poullet, J. B.; Massart, S.; Collini, S.; Pieraccini, G.; Lionetti, P. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa Proc. Natl. Acad. Sci. U. S. A. 2010, 107 (33) 14691-6 10.1073/pnas.1005963107
37. Bourriaud, C.; Robins, R. J.; Martin, L.; Kozlowski, F.; Tenailleau, E.; Cherbut, C.; Michel, C. Lactate is mainly fermented to butyrate by human intestinal microfloras but inter-individual variation is evident J. Appl. Microbiol. 2005, 99 (1) 201-12 10.1111/j.1365-2672.2005.02605.x
38. Belenguer, A.; Duncan, S. H.; Holtrop, G.; Anderson, S. E.; Lobley, G. E.; Flint, H. J. Impact of pH on lactate formation and utilization by human fecal microbial communities Appl. Environ. Microbiol. 2007, 73 (20) 6526-33 10.1128/AEM.00508-07
39. Macfarlane, S.; Macfarlane, G. T. Regulation of short-chain fatty acid production Proc. Nutr. Soc. 2003, 62 (1) 67-72 10.1079/PNS2002207
40. Vodonik, S. A.; Gray, G. R. Analysis by the reductive-cleavage method of linkage positions in a polysaccharide containing 4-linked D-glucopyranosyluronic residues Carbohydr. Res. 1988, 175 (1) 93-102 10.1016/0008-6215(88)80159-9
41. Lahtinen, S. J.; Knoblock, K.; Drakoularakou, A.; Jacob, M.; Stowell, J.; Gibson, G. R.; Ouwehand, A. C. Effect of molecule branching and glycosidic linkage on the degradation of Polydextrose by gut microbiota Biosci., Biotechnol., Biochem. 2010, 74 (10) 2016-21 10.1271/bbb.100251
42. Roslund, M. U.; Tahtinen, P.; Niemitz, M.; Sjoholm, R. Complete assignments of the (1)H and (13)C chemical shifts and J(H,H) coupling constants in NMR spectra of D-glucopyranose and all D-glucopyranosyl-D-glucopyranosides Carbohydr. Res. 2008, 343 (1) 101-12 10.1016/j.carres.2007.10.008
43. Satoh, T.; Imai, T.; Ishihara, H.; Maeda, T.; Kitajyo, Y.; Sakai, Y.; Kaga, H.; Kaneko, N.; Ishii, F.; Kakuchi, T. Synthesis, Branched Structure, and Solution Property of Hyperbranched d-Glucan and d-Galactan Macromolecules 2005, 38 (10) 4202-4210 10.1021/ma0475479
44. Jain, D.; Stark, A. Y.; Niewiarowski, P. H.; Miyoshi, T.; Dhinojwala, A. NMR spectroscopy reveals the presence and association of lipids and keratin in adhesive gecko setae Sci. Rep. 2015, 5, 9594 10.1038/srep09594
45. Pimentel, M.; Gunsalus, R. P.; Rao, S. S. C.; Zhang, H. Methanogens in Human Health and Disease Am. J. Gastroenterol. Suppl. 2012, 1 (1) 28-33 10.1038/ajgsup.2012.6
46. Kaakoush, N. O. Insights into the Role of Erysipelotrichaceae in the Human Host Front. Cell. Infect. Microbiol. 2015, 5 (84) 84 10.3389/fcimb.2015.00084
47. Zhang, C.; Zhang, M.; Wang, S.; Han, R.; Cao, Y.; Hua, W.; Mao, Y.; Zhang, X.; Pang, X.; Wei, C.; Zhao, G.; Chen, Y.; Zhao, L. Interactions between gut microbiota, host genetics and diet relevant to development of metabolic syndromes in mice ISME J. 2010, 4 (2) 232-41 10.1038/ismej.2009.112
48. Zhu, Q.; Jin, Z.; Wu, W.; Gao, R.; Guo, B.; Gao, Z.; Yang, Y.; Qin, H. Analysis of the intestinal lumen microbiota in an animal model of colorectal cancer PLoS One 2014, 9 (3) e90849 10.1371/journal.pone.0090849
49. Craven, M.; Egan, C. E.; Dowd, S. E.; McDonough, S. P.; Dogan, B.; Denkers, E. Y.; Bowman, D.; Scherl, E. J.; Simpson, K. W. Inflammation drives dysbiosis and bacterial invasion in murine models of ileal Crohn's disease PLoS One 2012, 7 (7) e41594 10.1371/journal.pone.0041594
50. Martinez, I.; Perdicaro, D. J.; Brown, A. W.; Hammons, S.; Carden, T. J.; Carr, T. P.; Eskridge, K. M.; Walter, J. Diet-induced alterations of host cholesterol metabolism are likely to affect the gut microbiota composition in hamsters Appl. Environ. Microbiol. 2013, 79 (2) 516-24 10.1128/AEM.03046-12
51. Umu, Ö. C. O.; Frank, J. A.; Fangel, J. U.; Oostindjer, M.; da Silva, C. S.; Bolhuis, E. J.; Bosch, G.; Willats, W. G. T.; Pope, P. B.; Diep, D. B. Resistant starch diet induces change in the swine microbiome and a predominance of beneficial bacterial populations Microbiome 2015, 3 (1) 16 10.1186/s40168-015-0078-5
52. Cox, L. M.; Cho, I.; Young, S. A.; Anderson, W. H. K.; Waters, B. J.; Hung, S.-C.; Gao, Z.; Mahana, D.; Bihan, M.; Alekseyenko, A. V.; Methé, B. A.; Blaser, M. J. The nonfermentable dietary fiber hydroxypropyl methylcellulose modulates intestinal microbiota FASEB J. 2013, 27 (2) 692-702 10.1096/fj.12-219477
53. Vital, M.; Howe, A. C.; Tiedje, J. M. Revealing the bacterial butyrate synthesis pathways by analyzing (meta)genomic data mBio 2014, 5 (2) e00889-14 10.1128/mBio.00889-14
54. Pozuelo, M.; Panda, S.; Santiago, A.; Mendez, S.; Accarino, A.; Santos, J.; Guarner, F.; Azpiroz, F.; Manichanh, C. Reduction of butyrate- and methane-producing microorganisms in patients with Irritable Bowel Syndrome Sci. Rep. 2015, 5, 12693 10.1038/srep12693
55. Lecomte, V.; Kaakoush, N. O.; Maloney, C. A.; Raipuria, M.; Huinao, K. D.; Mitchell, H. M.; Morris, M. J. Changes in Gut Microbiota in Rats Fed a High Fat Diet Correlate with Obesity-Associated Metabolic Parameters PLoS One 2015, 10 (5) e0126931 10.1371/journal.pone.0126931
56. Turnbaugh, P. J.; Backhed, F.; Fulton, L.; Gordon, J. I. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome Cell Host Microbe 2008, 3 (4) 213-23 10.1016/j.chom.2008.02.015
57. Duvallet, C.; Gibbons, S. M.; Gurry, T.; Irizarry, R. A.; Alm, E. J. Meta-analysis of gut microbiome studies identifies disease-specific and shared responses Nat. Commun. 2017, 8 (1) 1784 10.1038/s41467-017-01973-8
58. Wu, G. D.; Chen, J.; Hoffmann, C.; Bittinger, K.; Chen, Y. Y.; Keilbaugh, S. A.; Bewtra, M.; Knights, D.; Walters, W. A.; Knight, R.; Sinha, R.; Gilroy, E.; Gupta, K.; Baldassano, R.; Nessel, L.; Li, H.; Bushman, F. D.; Lewis, J. D. Linking long-term dietary patterns with gut microbial enterotypes Science 2011, 334 (6052) 105-8 10.1126/science.1208344
59. Zhang, C.; Zhao, L. Strain-level dissection of the contribution of the gut microbiome to human metabolic disease Genome Med. 2016, 8, 41 10.1186/s13073-016-0304-1
60. Takahashi, K.; Nishida, A.; Fujimoto, T.; Fujii, M.; Shioya, M.; Imaeda, H.; Inatomi, O.; Bamba, S.; Sugimoto, M.; Andoh, A. Reduced Abundance of Butyrate-Producing Bacteria Species in the Fecal Microbial Community in Crohn's Disease Digestion 2016, 93 (1) 59-65 10.1159/000441768
61. Rajilic-Stojanovic, M.; de Vos, W. M. The first 1000 cultured species of the human gastrointestinal microbiota FEMS Microbiol Rev. 2014, 38 (5) 996-1047 10.1111/1574-6976.12075
62. Polansky, O.; Sekelova, Z.; Faldynova, M.; Sebkova, A.; Sisak, F.; Rychlik, I. Important Metabolic Pathways and Biological Processes Expressed by Chicken Cecal Microbiota Appl. Environ. Microbiol. 2016, 82 (5) 1569-76 10.1128/AEM.03473-15
63. Flint, H. J.; Duncan, S. H.; Scott, K. P.; Louis, P. Links between diet, gut microbiota composition and gut metabolism Proc. Nutr. Soc. 2015, 74 (1) 13-22 10.1017/S0029665114001463
64. Coakley, M.; Ross, R. P.; Nordgren, M.; Fitzgerald, G.; Devery, R.; Stanton, C. Conjugated linoleic acid biosynthesis by human-derived Bifidobacterium species J. Appl. Microbiol. 2003, 94 (1) 138-45 10.1046/j.1365-2672.2003.01814.x
65. Riviere, A.; Selak, M.; Lantin, D.; Leroy, F.; De Vuyst, L. Bifidobacteria and Butyrate-Producing Colon Bacteria: Importance and Strategies for Their Stimulation in the Human Gut Front. Microbiol. 2016, 7, 979 10.3389/fmicb.2016.00979
66. De Vuyst, L.; Leroy, F. Cross-feeding between bifidobacteria and butyrate-producing colon bacteria explains bifdobacterial competitiveness, butyrate production, and gas production Int. J. Food Microbiol. 2011, 149 (1) 73-80 10.1016/j.ijfoodmicro.2011.03.003