Polysaccharide Degradation by the Intestinal Microbiota and Its Influence on Human Health and Disease

Journal of Molecular Biology

Volumn 428, Issue 16, 2016, Pages 3230-3252

  Cockburn, Darrell W ^a   Koropatkin, Nicole M ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Bacteroidetes; carbohydrates; Firmicutes; microbiome; prebiotics

Indexed keywords

GLYCAN; MUCIN; MULTIENZYME COMPLEX; POLYSACCHARIDE; PREBIOTIC AGENT; STARCH;

BACTEROIDETES; CARBOHYDRATE METABOLISM; FIRMICUTES; HUMAN; INTESTINE FLORA; KEYSTONE SPECIES; MICROBIAL DEGRADATION; MOLECULAR BIOLOGY; NONHUMAN; PRIORITY JOURNAL; REVIEW; ANIMAL; BACTERIUM; DIET; GASTROINTESTINAL TRACT; METABOLISM; MICROBIOLOGY; MICROFLORA; PATHOGENICITY; PHYSIOLOGY; PROCEDURES;

ANIMALS; BACTERIA; DIET; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; HUMANS; MICROBIOTA; POLYSACCHARIDES;

EID: 84979556395     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2016.06.021     Document Type: Review

References (217)

1. [1] Koppel, N., Balskus, E.P., Exploring and understanding the biochemical diversity of the human microbiota. Cell Chem. Biol. 23 (2016), 18–30.
2. [2] Stappenbeck, T.S., Hooper, L.V., Gordon, J.I., Developmental regulation of intestinal angiogenesis by indigenous microbes via paneth cells. Proc. Natl. Acad. Sci. U. S. A. 99 (2002), 15,451–15,455.
3. [3] Matsuki, T., Pedron, T., Regnault, B., Mulet, C., Hara, T., Sansonetti, P.J., Epithelial cell proliferation arrest induced by lactate and acetate from Lactobacillus casei and Bifidobacterium breve. PLoS One, 8, 2013, e63053.
4. [4] Hooper, L.V., Wong, M.H., Thelin, A., Hansson, L., Falk, P.G., Gordon, J.I., Molecular analysis of commensal host-microbial relationships in the intestine. Science 291 (2001), 881–884.
5. [5] Round, J.L., Mazmanian, S.K., The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 9 (2009), 313–323.
6. [6] Reynolds, L.A., Finlay, B.B., A case for antibiotic perturbation of the microbiota leading to allergy development. Expert. Rev. Clin. Immunol. 9 (2013), 1019–1030.
7. [7] Peterson, D.A., Cardona, R.A., Specificity of the adaptive immune response to the gut microbiota. Adv. Immunol. 107 (2010), 71–107.
8. [8] Cameron, E.A., Sperandio, V., Frenemies: signaling and nutritional integration in pathogen–microbiota–host interactions. Cell Host Microbe 18 (2015), 275–284.
9. [9] Koropatkin, N.M., Cameron, E.A., Martens, E.C., How glycan metabolism shapes the human gut microbiota. Nat. Rev. Microbiol. 10 (2012), 323–335.
10. [10] Xu, Z., Knight, R., Dietary effects on human gut microbiome diversity. Br. J. Nutr. 113 Suppl (2015), S1–S5.
11. [11] 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 334 (2011), 105–108.
12. [12] David, L.A., Maurice, C.F., Carmody, R.N., Gootenberg, D.B., Button, J.E., Wolfe, B.E., Ling, A.V., Devlin, A.S., Varma, Y., Fischbach, M.A., Biddinger, S.B., Dutton, R.J., Turnbaugh, P.J., Diet rapidly and reproducibly alters the human gut microbiome. Nature 505 (2014), 559–563.
13. [13] Kashtanova, D.A., Popenko, A.S., Tkacheva, O.N., Tyakht, A.B., Alexeev, D.G., Boytsov, S.A., Association between the gut microbiota and diet: fetal life, early childhood, and further life. Nutrition, 2015, 10.1016/j.nut.2015.12.037.
14. [14] He, B., Nohara, K., Ajami, N.J., Michalek, R.D., Tian, X., Wong, M., Losee-Olson, S.H., Petrosino, J.F., Yoo, S.H., Shimomura, K., Chen, Z., Transmissible microbial and metabolomic remodeling by soluble dietary fiber improves metabolic homeostasis. Sci. Rep., 5, 2015, 10,604.
15. [15] El Kaoutari, A., Armougom, F., Gordon, J.I., Raoult, D., Henrissat, B., The abundance and variety of carbohydrate-active enzymes in the human gut microbiota. Nat. Rev. Microbiol. 11 (2013), 497–504.
16. [16] Scheller, H.V., Ulvskov, P., Hemicelluloses. Annu. Rev. Plant Biol. 61 (2010), 263–289.
17. [17] Hehemann, J.H., Correc, G., Barbeyron, T., Helbert, W., Czjzek, M., Michel, G., Transfer of carbohydrate-active enzymes from marine bacteria to japanese gut microbiota. Nature 464 (2010), 908–912.
18. [18] Hehemann, J.H., Kelly, A.G., Pudlo, N.A., Martens, E.C., Boraston, A.B., Bacteria of the human gut microbiome catabolize red seaweed glycans with carbohydrate-active enzyme updates from extrinsic microbes. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 19,786–19,791.
19. [19] Martens, E.C., Kelly, A.G., Tauzin, A.S., Brumer, H., The devil lies in the details: how variations in polysaccharide fine-structure impact the physiology and evolution of gut microbes. J. Mol. Biol. 426 (2014), 3851–3865.
20. [20] de Jesus Raposo, M.F., de Morais, A.M., de Morais, R.M., Emergent sources of prebiotics: seaweeds and microalgae. Mar. Drugs, 14, 2016.
21. [21] Imberty, A., Lortat-Jacob, H., Pérez, S., Structural view of glycosaminoglycan–protein interactions. Carbohydr. Res. 342 (2007), 430–439.
22. [22] Sodini, I., Remeuf, F., Haddad, S., Corrieu, G., The relative effect of milk base, starter, and process on yogurt texture: a review. Crit. Rev. Food Sci. Nutr. 44 (2004), 113–137.
23. [23] Percy, M.G., Grundling, A., Lipoteichoic acid synthesis and function in Gram-positive bacteria. Annu. Rev. Microbiol. 68 (2014), 81–100.
24. [24] Moynihan, P.J., Sychantha, D., Clarke, A.J., Chemical biology of peptidoglycan acetylation and deacetylation. Bioorg. Chem. 54 (2014), 44–50.
25. [25] Lammerts van Bueren, A., Saraf, A., Martens, E.C., Dijkhuizen, L., Differential metabolism of exopolysaccharides from probiotic Lactobacilli by the human gut symbiont Bacteroides thetaiotaomicron. Appl. Environ. Microbiol. 81 (2015), 3973–3983.
26. [26] Cuskin, F., Lowe, E.C., Temple, M.J., Zhu, Y., Cameron, E.A., Pudlo, N.A., Porter, N.T., Urs, K., Thompson, A.J., Cartmell, A., Rogowski, A., Hamilton, B.S., Chen, R., Tolbert, T.J., Piens, K., Bracke, D., Vervecken, W., Hakki, Z., Speciale, G., Munoz-Munoz, J.L., Day, A., Pena, M.J., McLean, R., Suits, M.D., Boraston, A.B., Atherly, T., Ziemer, C.J., Williams, S.J., Davies, G.J., Abbott, D.W., Martens, E.C., Gilbert, H.J., Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism. Nature 517 (2015), 165–169.
27. [27] Latgé, J.-P., The cell wall: a carbohydrate armour for the fungal cell. Mol. Microbiol. 66 (2007), 279–290.
28. [28] Prajapati, V.D., Jani, G.K., Khanda, S.M., Pullulan: an exopolysaccharide and its various applications. Carbohydr. Polym. 95 (2013), 540–549.
29. [29] Johansson, M.E., Larsson, J.M., Hansson, G.C., The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host-microbial interactions. Proc. Natl. Acad. Sci. U. S. A. 108:Suppl. 1 (2011), 4659–4665.
30. [30] Jakobsson, H.E., Rodriguez-Pineiro, A.M., Schutte, A., Ermund, A., Boysen, P., Bemark, M., Sommer, F., Backhed, F., Hansson, G.C., Johansson, M.E., The composition of the gut microbiota shapes the colon mucus barrier. EMBO Rep. 16 (2015), 164–177.
31. [31] Li, H., Limenitakis, J.P., Fuhrer, T., Geuking, M.B., Lawson, M.A., Wyss, M., Brugiroux, S., Keller, I., Macpherson, J.A., Rupp, S., Stolp, B., Stein, J.V., Stecher, B., Sauer, U., McCoy, K.D., Macpherson, A.J., The outer mucus layer hosts a distinct intestinal microbial niche. Nat. Commun., 6, 2015, 8292.
32. [32] Atuma, C., Strugala, V., Allen, A., Holm, L., The adherent gastrointestinal mucus gel layer: thickness and physical state in vivo. Am. J. Physiol. Gastrointest. Liver Physiol. 280 (2001), G922–G929.
33. [33] Donaldson, G.P., Lee, S.M., Mazmanian, S.K., Gut biogeography of the bacterial microbiota. Nat. Rev. Microbiol. 14 (2016), 20–32.
34. [34] Johansson, M.E., Phillipson, M., Petersson, J., Velcich, A., Holm, L., Hansson, G.C., The inner of the two MUC2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 15,064–15,069.
35. [35] Tailford, L.E., Crost, E.H., Kavanaugh, D., Juge, N., Mucin glycan foraging in the human gut microbiome. Front. Genet., 6, 2015, 81.
36. [36] Futuyma, D.J., Moreno, G., The evolution of ecological specialization. Annu. Rev. Ecol. Syst. 19 (1988), 207–233.
37. [37] Carbonero, F., Oakley, B.B., Purdy, K.J., Metabolic flexibility as a major predictor of spatial distribution in microbial communities. PLoS One, 9, 2014, e85105.
38. [38] Mariadassou, M., Pichon, S., Ebert, D., Microbial ecosystems are dominated by specialist taxa. Ecol. Lett. 18 (2015), 974–982.
39. [39] Salyers, A.A., Vercellotti, J.R., West, S.E., Wilkins, T.D., Fermentation of mucin and plant polysaccharides by strains of Bacteroides from the human colon. Appl. Environ. Microbiol. 33 (1977), 319–322.
40. [40] Salyers, A.A., West, S.E., Vercellotti, J.R., Wilkins, T.D., Fermentation of mucins and plant polysaccharides by anaerobic bacteria from the human colon. Appl. Environ. Microbiol. 34 (1977), 529–533.
41. [41] Voreades, N., Kozil, A., Weir, T.L., Diet and the development of the human intestinal microbiome. Front. Microbiol., 5, 2014, 494.
42. [42] Eckburg, P.B., Bik, E.M., Bernstein, C.N., Purdom, E., Dethlefsen, L., Sargent, M., Gill, S.R., Nelson, K.E., Relman, D.A., Diversity of the human intestinal microbial flora. Science 308 (2005), 1635–1638.
43. [43] Arumugam, M., Raes, J., Pelletier, E., Le Paslier, D., Yamada, T., Mende, D.R., Fernandes, G.R., Tap, J., Bruls, T., Batto, J.M., Bertalan, M., Borruel, N., Casellas, F., Fernandez, L., Gautier, L., Hansen, T., Hattori, M., Hayashi, T., Kleerebezem, M., Kurokawa, K., Leclerc, M., Levenez, F., Manichanh, C., Nielsen, H.B., Nielsen, T., Pons, N., Poulain, J., Qin, J., Sicheritz-Ponten, T., Tims, S., Torrents, D., Ugarte, E., Zoetendal, E.G., Junwang, Guarner, F., Pedersen, O., de Vos, W.M., Brunak, S., Dore, J., Consortium, M., Weissenbach, J., Ehrlich, S.D., Bork, P., Enterotypes of the human gut microbiome. Nature 473 (2011), 174–180.
44. [44] Ley, R.E., Turnbaugh, P.J., Klein, S., Gordon, J.I., Microbial ecology: human gut microbes associated with obesity. Nature 444 (2006), 1022–1023.
45. [45] Costello, E.K., Lauber, C.L., Hamady, M., Fierer, N., Gordon, J.I., Knight, R., Bacterial community variation in human body habitats across space and time. Science 326 (2009), 1694–1697.
46. [46] Schnorr, S.L., Candela, M., Rampelli, S., Centanni, M., Consolandi, C., Basaglia, G., Turroni, S., Biagi, E., Peano, C., Severgnini, M., Fiori, J., Gotti, R., De Bellis, G., Luiselli, D., Brigidi, P., Mabulla, A., Marlowe, F., Henry, A.G., Crittenden, A.N., Gut microbiome of the Hadza hunter-gatherers. Nat. Commun., 5, 2014, 3654.
47. [47] 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. 107 (2010), 14,691–14,696.
48. [48] Sonnenburg, E.D., Smits, S.A., Tikhonov, M., Higginbottom, S.K., Wingreen, N.S., Sonnenburg, J.L., Diet-induced extinctions in the gut microbiota compound over generations. Nature 529 (2016), 212–215.
49. [49] Lombard, V., Golaconda Ramulu, H., Drula, E., Coutinho, P.M., Henrissat, B., The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42 (2014), D490–D495.
50. [50] McNulty, N.P., Wu, M., Erickson, A.R., Pan, C., Erickson, B.K., Martens, E.C., Pudlo, N.A., Muegge, B.D., Henrissat, B., Hettich, R.L., Gordon, J.I., Effects of diet on resource utilization by a model human gut microbiota containing Bacteroides cellulosilyticus WH2, a symbiont with an extensive glycobiome. PLoS Biol., 11, 2013, e1001637.
51. [51] Martens, E.C., Koropatkin, N.M., Smith, T.J., Gordon, J.I., Complex glycan catabolism by the human gut microbiota: the Bacteroidetes sus-like paradigm. J. Biol. Chem. 284 (2009), 24,673–24,677.
52. [52] Rogers, T.E., Pudlo, N.A., Koropatkin, N.M., Bell, J.S., Moya Balasch, M., Jasker, K., Martens, E.C., Dynamic responses of Bacteroides thetaiotaomicron during growth on glycan mixtures. Mol. Microbiol. 88 (2013), 876–890.
53. [53] Pudlo, N.A., Urs, K., Kumar, S.S., German, J.B., Mills, D.A., Martens, E.C., Symbiotic human gut bacteria with variable metabolic priorities for host mucosal glycans. MBio., 6, 2015, e01282-15.
54. [54] Lynch, J.B., Sonnenburg, J.L., Prioritization of a plant polysaccharide over a mucus carbohydrate is enforced by a Bacteroides hybrid two-component system. Mol. Microbiol. 85 (2012), 478–491.
55. [55] Sonnenburg, J.L., Xu, J., Leip, D.D., Chen, C.H., Westover, B.P., Weatherford, J., Buhler, J.D., Gordon, J.I., Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science 307 (2005), 1955–1959.
56. [56] Martens, E.C., Lowe, E.C., Chiang, H., Pudlo, N.A., Wu, M., McNulty, N.P., Abbott, D.W., Henrissat, B., Gilbert, H.J., Bolam, D.N., Gordon, J.I., Recognition and degradation of plant cell wall polysaccharides by two human gut symbionts. PLoS Biol., 9, 2011, e1001221.
57. [57] Anderson, K.L., Salyers, A.A., Genetic evidence that outer membrane binding of starch is required for starch utilization by Bacteroides thetaiotaomicron. J. Bacteriol. 171 (1989), 3199–3204.
58. [58] Reeves, A.R., Wang, G.R., Salyers, A.A., Characterization of four outer membrane proteins that play a role in utilization of starch by Bacteroides thetaiotaomicron. J. Bacteriol. 179 (1997), 643–649.
59. [59] Terrapon, N., Lombard, V., Gilbert, H.J., Henrissat, B., Automatic prediction of polysaccharide utilization loci in Bacteroidetes species. Bioinformatics 31 (2015), 647–655.
60. [60] Martens, E.C., Chiang, H.C., Gordon, J.I., Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host Microbe 4 (2008), 447–457.
61. [61] Wu, M., McNulty, N.P., Rodionov, D.A., Khoroshkin, M.S., Griffin, N.W., Cheng, J., Latreille, P., Kerstetter, R.A., Terrapon, N., Henrissat, B., Osterman, A.L., Gordon, J.I., Genetic determinants of in vivo fitness and diet responsiveness in multiple human gut Bacteroides. Science, 350, 2015, aac5992.
62. [62] Brigham, C.J., Malamy, M.H., Characterization of the RokA and HexA broad-substrate-specificity hexokinases from Bacteroides fragilis and their role in hexose and N-acetylglucosamine utilization. J. Bacteriol. 187 (2005), 890–901.
63. [63] Tancula, E., Feldhaus, M.J., Bedzyk, L.A., Salyers, A.A., Location and characterization of genes involved in binding of starch to the surface of Bacteroides thetaiotaomicron. J. Bacteriol. 174 (1992), 5609–5616.
64. [64] D'Elia, J.N., Salyers, A.A., Effect of regulatory protein levels on utilization of starch by Bacteroides thetaiotaomicron. J. Bacteriol. 178 (1996), 7180–7186.
65. [65] Shipman, J.A., Berleman, J.E., Salyers, A.A., Characterization of four outer membrane proteins involved in binding starch to the cell surface of Bacteroides thetaiotaomicron. J. Bacteriol. 182 (2000), 5365–5372.
66. [66] Shipman, J.A., Cho, K.H., Siegel, H.A., Salyers, A.A., Physiological characterization of SusG, an outer membrane protein essential for starch utilization by Bacteroides thetaiotaomicron. J. Bacteriol. 181 (1999), 7206–7211.
67. [67] Koropatkin, N.M., Smith, T.J., SusG: a unique cell-membrane-associated alpha-amylase from a prominent human gut symbiont targets complex starch molecules. Structure 18 (2010), 200–215.
68. [68] Cameron, E.A., Maynard, M.A., Smith, C.J., Smith, T.J., Koropatkin, N.M., Martens, E.C., Multidomain carbohydrate-binding proteins involved in Bacteroides thetaiotaomicron starch metabolism. J. Biol. Chem. 287 (2012), 34,614–34,625.
69. [69] Cameron, E.A., Kwiatkowski, K.J., Lee, B.H., Hamaker, B.R., Koropatkin, N.M., Martens, E.C., Multifunctional nutrient-binding proteins adapt human symbiotic bacteria for glycan competition in the gut by separately promoting enhanced sensing and catalysis. MBio, 5, 2014, e01441-14.
70. [70] Reeves, A.R., D'Elia, J.N., Frias, J., Salyers, A.A., A Bacteroides thetaiotaomicron outer membrane protein that is essential for utilization of maltooligosaccharides and starch. J. Bacteriol. 178 (1996), 823–830.
71. [71] D'Elia, J.N., Salyers, A.A., Contribution of a neopullulanase, a pullulanase, and an alpha-glucosidase to growth of Bacteroides thetaiotaomicron on starch. J. Bacteriol. 178 (1996), 7173–7179.
72. [72] Kitamura, M., Okuyama, M., Tanzawa, F., Mori, H., Kitago, Y., Watanabe, N., Kimura, A., Tanaka, I., Yao, M., Structural and functional analysis of a glycoside hydrolase family 97 enzyme from Bacteroides thetaiotaomicron. J. Biol. Chem. 283 (2008), 36,328–36,337.
73. [73] Foley, M.H., Cockburn, D., Koropatkin, N.M., The sus operon—a model system for starch uptake by the human gut Bacteroidetes. Cell. Mol. Life Sci., 2016, 10.1007/s00018-016-2242-x.
74. [74] Cho, K.H., Salyers, A.A., Biochemical analysis of interactions between outer membrane proteins that contribute to starch utilization by Bacteroides thetaiotaomicron. J. Bacteriol. 183 (2001), 7224–7230.
75. [75] Renzi, F., Manfredi, P., Mally, M., Moes, S., Jeno, P., Cornelis, G.R., The N-glycan glycoprotein deglycosylation complex (Gpd) from Capnocytophaga canimorsus deglycosylates human IgG. PLoS Pathog., 7, 2011, e1002118.
76. [76] Noinaj, N., Guillier, M., Barnard, T.J., Buchanan, S.K., TonB-dependent transporters: regulation, structure, and function. Annu. Rev. Microbiol. 64 (2010), 43–60.
77. [77] Bolam, D.N., Koropatkin, N.M., Glycan recognition by the Bacteroidetes sus-like systems. Curr. Opin. Struct. Biol. 22 (2012), 563–569.
78. [78] Koropatkin, N., Martens, E.C., Gordon, J.I., Smith, T.J., Structure of a SusD homologue, BT1043, involved in mucin O-glycan utilization in a prominent human gut symbiont. Biochemistry 48 (2009), 1532–1542.
79. [79] Tauzin, A.S., Kwiatkowski, K.J., Orlovsky, N.I., Smith, C.J., Creagh, A.L., Haynes, C.A., Wawrzak, Z., Brumer, H., Koropatkin, N.M., Molecular dissection of xyloglucan recognition in a prominent human gut symbiont. MBio, 2016, 10.1128/mBio.02134-15.
80. [80] Sonnenburg, E.D., Zheng, H., Joglekar, P., Higginbottom, S.K., Firbank, S.J., Bolam, D.N., Sonnenburg, J.L., Specificity of polysaccharide use in intestinal Bacteroides species determines diet-induced microbiota alterations. Cell 141 (2010), 1241–1252.
81. [81] Larsbrink, J., Rogers, T.E., Hemsworth, G.R., McKee, L.S., Tauzin, A.S., Spadiut, O., Klinter, S., Pudlo, N.A., Urs, K., Koropatkin, N.M., Creagh, A.L., Haynes, C.A., Kelly, A.G., Cederholm, S.N., Davies, G.J., Martens, E.C., Brumer, H., A discrete genetic locus confers xyloglucan metabolism in select human gut Bacteroidetes. Nature 506 (2014), 498–502.
82. [82] Rogowski, A., Briggs, J.A., Mortimer, J.C., Tryfona, T., Terrapon, N., Lowe, E.C., Basle, A., Morland, C., Day, A.M., Zheng, H., Rogers, T.E., Thompson, P., Hawkins, A.R., Yadav, M.P., Henrissat, B., Martens, E.C., Dupree, P., Gilbert, H.J., Bolam, D.N., Glycan complexity dictates microbial resource allocation in the large intestine. Nat. Commun., 6, 2015, 7481.
83. [83] Xie, G., Bruce, D.C., Challacombe, J.F., Chertkov, O., Detter, J.C., Gilna, P., Han, C.S., Lucas, S., Misra, M., Myers, G.L., Richardson, P., Tapia, R., Thayer, N., Thompson, L.S., Brettin, T.S., Henrissat, B., Wilson, D.B., McBride, M.J., Genome sequence of the cellulolytic gliding bacterium Cytophaga hutchinsonii. Appl. Environ. Microbiol. 73 (2007), 3536–3546.
84. [84] McBride, M.J., Xie, G., Martens, E.C., Lapidus, A., Henrissat, B., Rhodes, R.G., Goltsman, E., Wang, W., Xu, J., Hunnicutt, D.W., Staroscik, A.M., Hoover, T.R., Cheng, Y.Q., Stein, J.L., Novel features of the polysaccharide-digesting gliding bacterium Flavobacterium johnsoniae revealed by genome sequence analysis. Appl. Environ. Microbiol. 75 (2009), 6864–6875.
85. [85] Chen, J., Molecular mechanism of the Escherichia coli maltose transporter. Curr. Opin. Struct. Biol. 23 (2013), 492–498.
86. [86] Deutscher, J., Ake, F.M., Derkaoui, M., Zebre, A.C., Cao, T.N., Bouraoui, H., Kentache, T., Mokhtari, A., Milohanic, E., Joyet, P., The bacterial phosphoenolpyruvate:carbohydrate phosphotransferase system: regulation by protein phosphorylation and phosphorylation-dependent protein–protein interactions. Microbiol. Mol. Biol. Rev. 78 (2014), 231–256.
87. [87] Yan, N., Structural biology of the major facilitator superfamily transporters. Annu. Rev. Biophys. 44 (2015), 257–283.
88. [88] Ethayathulla, A.S., Yousef, M.S., Amin, A., Leblanc, G., Kaback, H.R., Guan, L., Structure-based mechanism for Na(+)/melibiose symport by MelB. Nat. Commun., 5, 2014, 3009.
89. [89] Heinken, A., Khan, M.T., Paglia, G., Rodionov, D.A., Harmsen, H.J., Thiele, I., Functional metabolic map of Faecalibacterium prausnitzii, a beneficial human gut microbe. J. Bacteriol. 196 (2014), 3289–3302.
90. [90] Cockburn, D.W., Orlovsky, N.I., Foley, M.H., Kwiatkowski, K.J., Bahr, C.M., Maynard, M., Demeler, B., Koropatkin, N.M., Molecular details of a starch utilization pathway in the human gut symbiont Eubacterium rectale. Mol. Microbiol. 95 (2015), 209–230.
91. [91] Ramsay, A.G., Scott, K.P., Martin, J.C., Rincon, M.T., Flint, H.J., Cell-associated alpha-amylases of butyrate-producing Firmicute bacteria from the human colon. Microbiology 152 (2006), 3281–3290.
92. [92] Lammerts van Bueren, A., Ficko-Blean, E., Pluvinage, B., Hehemann, J.-H.H., Higgins, M.A., Deng, L., Ogunniyi, a.D., Stroeher, U.H., El Warry, N., Burke, R.D., Czjzek, M., Paton, J.C., Vocadlo, D.J., Boraston, A.B., The conformation and function of a multimodular glycogen-degrading pneumococcal virulence factor. Structure 19 (2011), 640–651.
93. [93] Perez, S., Samain, D., Structure and engineering of celluloses. Adv. Carbohydr. Chem. Biochem. 64 (2010), 25–116.
94. [94] Bayer, E.a., Lamed, R., White, B.a., Flint, H.J., From cellulosomes to cellulosomics. Chem. Rec. 8 (2008), 364–377.
95. [95] Bayer, E.A., Belaich, J.P., Shoham, Y., Lamed, R., The cellulosomes: multienzyme machines for degradation of plant cell wall polysaccharides. Annu. Rev. Microbiol. 58 (2004), 521–554.
96. [96] Pages, S., Belaich, A., Belaich, J.P., Morag, E., Lamed, R., Shoham, Y., Bayer, E.A., Species-specificity of the cohesin-dockerin interaction between Clostridium thermocellum and Clostridium cellulolyticum: prediction of specificity determinants of the dockerin domain. Proteins 29 (1997), 517–527.
97. [97] Fierobe, H.-P., Bayer, E.A., Tardif, C., Czjzek, M., Mechaly, A., Bélaïch, A., Lamed, R., Shoham, Y., Bélaïch, J.-P., Degradation of cellulose substrates by cellulosome chimeras. Substrate targeting versus proximity of enzyme components. J. Biol. Chem. 277 (2002), 49,621–49,630.
98. [98] Chassard, C., Delmas, E., Robert, C., Lawson, P.A., Bernalier-Donadille, A., Ruminococcus champanellensis sp. Nov., a cellulose-degrading bacterium from human gut microbiota. Int. J. Syst. Evol. Microbiol. 62 (2012), 138–143.
99. [99] Ben David, Y., Dassa, B., Borovok, I., Lamed, R., Koropatkin, N.M., Martens, E.C., White, B.A., Bernalier-Donadille, A., Duncan, S.H., Flint, H.J., Bayer, E.A., Moraïs, S., Ruminococcal cellulosome systems from rumen to human. Environ. Microbiol., 2015, 10.1111/1462-2920.12868.
100. [100] Buléon, A., Colonna, P., Planchot, V., Ball, S., Starch granules: structure and biosynthesis. Int. J. Biol. Macromol. 23 (1998), 85–112.
101. [101] Ze, X., David, B., Laverde-gomez, J.a., Dassa, B., Sheridan, P.O., Duncan, S.H., Louis, P., Henrissat, B., Juge, N., Koropatkin, N.M., Bayer, E.a., Flint, J., Unique organization of extracellular amylases into amylosomes in the resistant starch-utilizing human colonic Firmicutes bacterium Ruminococcus bromii. mBio 6 (2015), 1–11.
102. [102] Heinken, A., Thiele, I., Anoxic conditions promote species-specific mutualism between gut microbes in silico. Appl. Environ. Microbiol. 81 (2015), 4049–4061.
103. [103] Chassard, C., Delmas, E., Robert, C., Bernalier-Donadille, A., The cellulose-degrading microbial community of the human gut varies according to the presence or absence of methanogens. FEMS Microbiol. Ecol. 74 (2010), 205–213.
104. [104] Robert, C., Bernalier-Donadille, A., The cellulolytic microflora of the human colon: evidence of microcrystalline cellulose-degrading bacteria in methane-excreting subjects. FEMS Microbiol. Ecol. 46 (2003), 81–89.
105. [105] Chassard, C., Bernalier-Donadille, A., H2 and acetate transfers during xylan fermentation between a butyrate-producing xylanolytic species and hydrogenotrophic microorganisms from the human gut. FEMS Microbiol. Lett. 254 (2006), 116–122.
106. [106] Rey, F.E., Gonzalez, M.D., Cheng, J., Wu, M., Ahern, P.P., Gordon, J.I., Metabolic niche of a prominent sulfate-reducing human gut bacterium. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 13,582–13,587.
107. [107] Stams, A.J., Plugge, C.M., Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nat. Rev. Microbiol. 7 (2009), 568–577.
108. [108] 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. 73 (2007), 6526–6533.
109. [109] Belenguer, A., Duncan, S.H., Calder, A.G., Holtrop, G., Louis, P., Lobley, G.E., Flint, H.J., Two routes of metabolic cross-feeding between Bifidobacterium adolescentis and butyrate-producing anaerobes from the human gut. Appl. Environ. Microbiol. 72 (2006), 3593–3599.
110. [110] Rios-Covian, D., Gueimonde, M., Duncan, S.H., Flint, H.J., de Los Reyes-Gavilan, C.G., Enhanced butyrate formation by cross-feeding between Faecalibacterium prausnitzii and Bifidobacterium adolescentis. FEMS Microbiol. Lett., 362, 2015.
111. [111] Turroni, F., Özcan, E., Milani, C., Mancabelli, L., Viappiani, A., van Sinderen, D., Sela, D.a., Ventura, M., Glycan cross-feeding activities between Bifidobacteria under in vitro conditions. Front. Microbiol. 6 (2015), 1–8.
112. [112] Turroni, F., Milani, C., Duranti, S., Mancabelli, L., Mangifesta, M., Viappiani, A., Andrea Lugli, G., Ferrario, C., Gioiosa, L., Ferrarini, A., Li, J., Palanza, P., Delledonne, M., van Sinderen, D., Ventura, M., Deciphering Bifidobacterial-mediated metabolic interactions and their impact on gut microbiota by a multi-omics approach. ISME J., 2016, 10.1038/ismej.2015.236.
113. [113] Milani, C., Andrea Lugli, G., Duranti, S., Turroni, F., Mancabelli, L., Ferrario, C., Mangifesta, M., Hevia, A., Viappiani, A., Scholz, M., Arioli, S., Sanchez, B., Lane, J., Ward, D.V., Hickey, R., Mora, D., Segata, N., Margolles, A., van Sinderen, D., Ventura, M., Bifidobacteria exhibit social behavior through carbohydrate resource sharing in the gut. Sci. Rep., 5, 2015, 15,782.
114. [114] Rivière, A., Gagnon, M., Weckx, S., Roy, D., De Vuyst, L., Mutual cross-feeding interactions between Bifidobacterium longum NCC2705 and Eubacterium rectale ATCC33656 explain the bifidogenic and butyrogenic effects of arabinoxylan-oligosaccharides. Appl. Environ. Microbiol., 2015, 10.1128/AEM.02089-15 (AEM.02089-15).
115. [115] Duncan, S.H., Holtrop, G., Lobley, G.E., Calder, a.G., Stewart, C.S., Flint, H.J., Contribution of acetate to butyrate formation by human faecal bacteria. Br J Nutr 91 (2004), 915–923.
116. [116] Mahowald, M.A.a., Rey, F.E., Seedorf, H., Turnbaugh, P.J., Fulton, R.S., Wollam, A., Shah, N., Wang, C., Magrini, V., Wilson, R.K., Cantarel, B.L., Coutinho, P.M., Henrissat, B., Crock, L.W., Russell, A., Verberkmoes, N.C., Hettich, R.L., Gordon, J.I., Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 5859–5864.
117. [117] Rakoff-Nahoum, S., Coyne, M.J., Comstock, L.E., An ecological network of polysaccharide utilization among human intestinal symbionts. Curr. Biol. 24 (2014), 40–49.
118. [118] Hickey, C.A., Kuhn, K.A., Donermeyer, D.L., Porter, N.T., Jin, C., Cameron, E.A., Jung, H., Kaiko, G.E., Wegorzewska, M., Malvin, N.P., Glowacki, R.W., Hansson, G.C., Allen, P.M., Martens, E.C., Stappenbeck, T.S., Colitogenic Bacteroides thetaiotaomicron antigens access host immune cells in a sulfatase-dependent manner via outer membrane vesicles. Cell Host Microbe 17 (2015), 672–680.
119. [119] Elhenawy, W., Debelyy, M.O., Feldman, M.F., Preferential packing of acidic glycosidases and proteases into Bacteroides outer membrane vesicles. mBio, 5, 2014 e00909-14.
120. [120] Allen-Vercoe, E., Daigneault, M., White, A., Panaccione, R., Duncan, S.H., Flint, H.J., O'Neal, L., Lawson, P.A., Anaerostipes hadrus comb. Nov., a dominant species within the human colonic microbiota; reclassification of Eubacterium hadrum Moore et al. 1976. Anaerobe 18 (2012), 523–529.
121. [121] Ze, X., Duncan, S.H., Louis, P., Flint, H.J., Ruminococcus bromii is a keystone species for the degradation of resistant starch in the human colon. ISME J. 6 (2012), 1535–1543.
122. [122] Ze, X., Le Mougen, F., Duncan, S.H., Louis, P., Flint, H.J., Some are more equal than others: the role of “keystone” species in the degradation of recalcitrant substrates. Gut Microbes 4 (2013), 236–240.
123. [123] Hajishengallis, G., Darveau, R.P., Curtis, M.A., The keystone-pathogen hypothesis. Nat. Rev. Microbiol. 10 (2012), 717–725.
124. [124] Trosvik, P., de Muinck, E.J., Ecology of bacteria in the human gastrointestinal tract—identification of keystone and foundation taxa. Microbiome, 3, 2015, 44.
125. [125] Fisher, C.K., Mehta, P., Identifying keystone species in the human gut microbiome from metagenomic timeseries using sparse linear regression. PLoS One, 9, 2014, e102451.
126. [126] Martínez, I., Kim, J., Duffy, P.R., Schlegel, V.L., Walter, J., Resistant starches types 2 and 4 have differential effects on the composition of the fecal microbiota in human subjects. PLoS One, 5, 2010, e15046.
127. [127] Kang, S., Denman, S.E., Morrison, M., Yu, Z., Dore, J., Leclerc, M., McSweeney, C.S., Dysbiosis of fecal microbiota in Crohn's disease patients as revealed by a custom phylogenetic microarray. Inflamm. Bowel Dis. 16 (2010), 2034–2042.
128. [128] Rajilic-Stojanovic, M., Shanahan, F., Guarner, F., de Vos, W.M., Phylogenetic analysis of dysbiosis in ulcerative colitis during remission. Inflamm. Bowel Dis. 19 (2013), 481–488.
129. [129] Arike, L., Hansson, G.C., The densely O-glycosylated MUC2 mucin protects the intestine and provides food for the commensal bacteria. J. Mol. Biol., 2016, 10.1016/j.jmb.2016.02.010.
130. [130] Derrien, M., Vaughan, E.E., Plugge, C.M., de Vos, W.M., Akkermansia muciniphila gen. Nov., sp. Nov., a human intestinal mucin-degrading bacterium. Int. J. Syst. Evol. Microbiol. 54 (2004), 1469–1476.
131. [131] Chang, S.K., Dohrman, A.F., Basbaum, C.B., Ho, S.B., Tsuda, T., Toribara, N.W., Gum, J.R., Kim, Y.S., Localization of mucin (MUC2 and MUC3) messenger RNA and peptide expression in human normal intestine and colon cancer. Gastroenterology 107 (1994), 28–36.
132. [132] Gum, J.R. Jr., Hicks, J.W., Toribara, N.W., Siddiki, B., Kim, Y.S., Molecular cloning of human intestinal mucin (muc2) cDNA. Identification of the amino terminus and overall sequence similarity to prepro-von Willebrand factor. J. Biol. Chem. 269 (1994), 2440–2446.
133. [133] Petersson, J., Schreiber, O., Hansson, G.C., Gendler, S.J., Velcich, A., Lundberg, J.O., Roos, S., Holm, L., Phillipson, M., Importance and regulation of the colonic mucus barrier in a mouse model of colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 300 (2011), G327–G333.
134. [134] Van der Sluis, M., De Koning, B.A., De Bruijn, A.C., Velcich, A., Meijerink, J.P., Van Goudoever, J.B., Buller, H.A., Dekker, J., Van Seuningen, I., Renes, I.B., Einerhand, A.W., MUC2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology 131 (2006), 117–129.
135. [135] Larsson, J.M., Karlsson, H., Crespo, J.G., Johansson, M.E., Eklund, L., Sjovall, H., Hansson, G.C., Altered O-glycosylation profile of MUC2 mucin occurs in active ulcerative colitis and is associated with increased inflammation. Inflamm. Bowel Dis. 17 (2011), 2299–2307.
136. [136] An, G., Wei, B., Xia, B., McDaniel, J.M., Ju, T., Cummings, R.D., Braun, J., Xia, L., Increased susceptibility to colitis and colorectal tumors in mice lacking core 3-derived O-glycans. J. Exp. Med. 204 (2007), 1417–1429.
137. [137] Fu, J., Wei, B., Wen, T., Johansson, M.E., Liu, X., Bradford, E., Thomsson, K.A., McGee, S., Mansour, L., Tong, M., McDaniel, J.M., Sferra, T.J., Turner, J.R., Chen, H., Hansson, G.C., Braun, J., Xia, L., Loss of intestinal core 1-derived O-glycans causes spontaneous colitis in mice. J. Clin. Invest. 121 (2011), 1657–1666.
138. [138] Bergstrom, K., Liu, X., Zhao, Y., Gao, N., Wu, Q., Song, K., Cui, Y., Li, Y., McDaniel, J.M., McGee, S., Chen, W., Huycke, M.M., Houchen, C.W., Zenewicz, L.A., West, C.M., Chen, H., Braun, J., Fu, J., Xia, L., Defective intestinal mucin-type O-glycosylation causes spontaneous colitis-associated cancer in mice. Gastroenterology, 2016, 10.1053/j.gastro.2016.03.039.
139. [139] Png, C.W., Linden, S.K., Gilshenan, K.S., Zoetendal, E.G., McSweeney, C.S., Sly, L.I., McGuckin, M.A., Florin, T.H., Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria. Am. J. Gastroenterol. 105 (2010), 2420–2428.
140. [140] Willing, B.P., Dicksved, J., Halfvarson, J., Andersson, A.F., Lucio, M., Zheng, Z., Jarnerot, G., Tysk, C., Jansson, J.K., Engstrand, L., A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology 139 (2010), 1844–1854, e1.
141. [141] Joossens, M., Huys, G., Cnockaert, M., De Preter, V., Verbeke, K., Rutgeerts, P., Vandamme, P., Vermeire, S., Dysbiosis of the faecal microbiota in patients with Crohn's disease and their unaffected relatives. Gut 60 (2011), 631–637.
142. [142] Derrien, M., Belzer, C., de Vos, W.M., Akkermansia muciniphila and its role in regulating host functions. Microb. Pathog., 2016, 10.1016/j.micpath.2016.02.005.
143. [143] Bloom, S.M., Bijanki, V.N., Nava, G.M., Sun, L., Malvin, N.P., Donermeyer, D.L., Dunne, W.M. Jr., Allen, P.M., Stappenbeck, T.S., Commensal Bacteroides species induce colitis in host-genotype-specific fashion in a mouse model of inflammatory bowel disease. Cell Host Microbe 9 (2011), 390–403.
144. [144] Earle, K.A., Billings, G., Sigal, M., Lichtman, J.S., Hansson, G.C., Elias, J.E., Amieva, M.R., Huang, K.C., Sonnenburg, J.L., Quantitative imaging of gut microbiota spatial organization. Cell Host Microbe 18 (2015), 478–488.
145. [145] Shin, N.R., Lee, J.C., Lee, H.Y., Kim, M.S., Whon, T.W., Lee, M.S., Bae, J.W., An increase in the Akkermansia spp. population induced by metformin treatment improves glucose homeostasis in diet-induced obese mice. Gut 63 (2014), 727–735.
146. [146] Larsen, N., Vogensen, F.K., van den Berg, F.W., Nielsen, D.S., Andreasen, A.S., Pedersen, B.K., Al-Soud, W.A., Sorensen, S.J., Hansen, L.H., Jakobsen, M., Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One, 5, 2010, e9085.
147. [147] He, C., Shan, Y., Song, W., Targeting gut microbiota as a possible therapy for diabetes. Nutr. Res. 35 (2015), 361–367.
148. [148] Everard, A., Belzer, C., Geurts, L., Ouwerkerk, J.P., Druart, C., Bindels, L.B., Guiot, Y., Derrien, M., Muccioli, G.G., Delzenne, N.M., de Vos, W.M., Cani, P.D., Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 9066–9071.
149. [149] Lee, S.M., Donaldson, G.P., Mikulski, Z., Boyajian, S., Ley, K., Mazmanian, S.K., Bacterial colonization factors control specificity and stability of the gut microbiota. Nature 501 (2013), 426–429.
150. [150] Swidsinski, A., Loening-Baucke, V., Herber, A., Mucosal flora in Crohn's disease and ulcerative colitis—an overview. J. Physiol. Pharmacol. 60 (2009), 61–71.
151. [151] Van den Abbeele, P., Belzer, C., Goossens, M., Kleerebezem, M., De Vos, W.M., Thas, O., De Weirdt, R., Kerckhof, F.M., Van de Wiele, T., Butyrate-producing Clostridium cluster XIVa species specifically colonize mucins in an in vitro gut model. ISME J. 7 (2013), 949–961.
152. [152] Mackenzie, D.A., Jeffers, F., Parker, M.L., Vibert-Vallet, A., Bongaerts, R.J., Roos, S., Walter, J., Juge, N., Strain-specific diversity of mucus-binding proteins in the adhesion and aggregation properties of Lactobacillus reuteri. Microbiology 156 (2010), 3368–3378.
153. [153] Jensen, H., Roos, S., Jonsson, H., Rud, I., Grimmer, S., van Pijkeren, J.P., Britton, R.A., Axelsson, L., Role of Lactobacillus reuteri cell and mucus-binding protein a (CmbA) in adhesion to intestinal epithelial cells and mucus in vitro. Microbiology 160 (2014), 671–681.
154. [154] Etzold, S., Juge, N., Structural insights into bacterial recognition of intestinal mucins. Curr. Opin. Struct. Biol. 28 (2014), 23–31.
155. [155] Walsham, A.D., MacKenzie, D.A., Cook, V., Wemyss-Holden, S., Hews, C.L., Juge, N., Schuller, S., Lactobacillus reuteri inhibition of enteropathogenic Escherichia coli adherence to human intestinal epithelium. Front. Microbiol., 7, 2016, 244.
156. [156] Gibson, G.R., Roberfroid, M.B., Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J. Nutr. 125 (1995), 1401–1412.
157. [157] Tanaka, R., Takayama, H., Morotomi, M., Kuroshima, T., Ueyama, S., Matsumoto, K., Kuroda, A., Mutai, M., Effects of administration of TOS and Bifidobacterium breve 4006 on the human fecal flora. Bifidobacteria and Microflora 2 (1983), 17–24.
158. [158] Hutkins, R.W., Krumbeck, J.A., Bindels, L.B., Cani, P.D., Fahey, G., Goh, Y.J., Hamaker, B., Martens, E.C., Mills, D.A., Rastal, R.A., Vaughan, E., Sanders, M.E., Prebiotics: why definitions matter. Curr. Opin. Biotechnol. 37 (2016), 1–7.
159. [159] Roberfroid, M., Gibson, G.R., Hoyles, L., McCartney, A.L., Rastall, R., Rowland, I., Wolvers, D., Watzl, B., Szajewska, H., Stahl, B., Guarner, F., Respondek, F., Whelan, K., Coxam, V., Davicco, M.-J., Léotoing, L., Wittrant, Y., Delzenne, N.M., Cani, P.D., Neyrinck, A.M., Meheust, A., Prebiotic effects: metabolic and health benefits. Br. J. Nutr. 104 (2010), S1–S63.
160. [160] Koenig, J.E., Spor, A., Scalfone, N., Fricker, A.D., Stombaugh, J., Knight, R., Angenent, L.T., Ley, R.E., Succession of microbial consortia in the developing infant gut microbiome. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 4578–4585.
161. [161] Bergstrom, A., Skov, T.H., Bahl, M.I., Roager, H.M., Christensen, L.B., Ejlerskov, K.T., Molgaard, C., Michaelsen, K.F., Licht, T.R., Establishment of intestinal microbiota during early life: a longitudinal, explorative study of a large cohort of danish infants. Appl. Environ. Microbiol. 80 (2014), 2889–2900.
162. [162] Duncan, S.H., Flint, H.J., Probiotics and prebiotics and health in ageing populations. Maturitas 75 (2013), 44–50.
163. [163] Varankovich, N.V., Nickerson, M.T., Korber, D.R., Probiotic-based strategies for therapeutic and prophylactic use against multiple gastrointestinal diseases. Front. Microbiol., 6, 2015, 685.
164. [164] Wong, J.M.W., de Souza, R., Kendall, C.W.C., Emam, A., Jenkins, D.J.A., Colonic health: fermentation and short-chain fatty acids. J. Clin. Gastroenterol. 40 (2006), 235–243.
165. [165] Macfarlane, S., Macfarlane, G.T., Regulation of short-chain fatty acid production. Proc. Nutr. Soc. 62 (2003), 67–72.
166. [166] Rios-Covian, D., Ruas-Madiedo, P., Margolles, A., Gueimonde, M., de Los Reyes-Gavilan, C.G., Salazar, N., Intestinal short chain fatty acids and their link with diet and human health. Front. Microbiol., 7, 2016, 185.
167. [167] Roediger, W.E., Role of anaerobic bacteria in the metabolic welfare of the colonic mucosa in man. Gut 21 (1980), 793–798.
168. [168] Fung, K.Y.C., Cosgrove, L., Lockett, T., Head, R., Topping, D.L., A review of the potential mechanisms for the lowering of colorectal oncogenesis by butyrate. Br. J. Nutr. 108 (2012), 820–831.
169. [169] Nastasi, C., Candela, M., Bonefeld, C.M., Geisler, C., Hansen, M., Krejsgaard, T., Biagi, E., Andersen, M.H., Brigidi, P., Ødum, N., Litman, T., Woetmann, A., The effect of short-chain fatty acids on human monocyte-derived dendritic cells. Sci. Rep., 5, 2015, 16,148.
170. [170] Wang, H.B., Wang, P.Y., Wang, X., Wan, Y.L., Liu, Y.C., Butyrate enhances intestinal epithelial barrier function via up-regulation of tight junction protein Claudin-1 transcription. Dig. Dis. Sci. 57 (2012), 3126–3135.
171. [171] Willemsen, L.E., Koetsier, M.A., van Deventer, S.J., van Tol, E.A., Short chain fatty acids stimulate epithelial mucin 2 expression through differential effects on prostaglandin E1 and E2 production by intestinal myofibroblasts. Gut 52 (2003), 1442–1447.
172. [172] Canfora, E.E., Jocken, J.W., Blaak, E.E., Short-chain fatty acids in control of body weight and insulin sensitivity. Nat. Rev. Endocrinol., 2015, 10.1038/nrendo.2015.128.
173. [173] Guilloteau, P., Martin, L., Eeckhaut, V., Ducatelle, R., Zabielski, R., Van Immerseel, F., From the gut to the peripheral tissues: the multiple effects of butyrate. Nutr. Res. Rev. 23 (2010), 366–384.
174. [174] Berni Canani, R., Di Costanzo, M., Leone, L., The epigenetic effects of butyrate: potential therapeutic implications for clinical practice. Clin. Epigenetics, 4, 2012, 4.
175. [175] Pacheco, A.R., Barile, D., Underwood, M.A., Mills, D.A., The impact of the milk glycobiome on the neonate gut microbiota. Annu. Rev. Anim. Biosci. 3 (2015), 419–445.
176. [176] Marcobal, A., Barboza, M., Froehlich, J.W., Block, D.E., German, J.B., Lebrilla, C.B., Mills, D.A., Consumption of human milk oligosaccharides by gut-related microbes. J. Agric. Food Chem. 58 (2010), 5334–5340.
177. [177] Depeint, F., Tzortzis, G., Vulevic, J., I'Anson, K., Gibson, G.R., Prebiotic evaluation of a novel galactooligosaccharide mixture produced by the enzymatic activity of Bifidobacterium bifidum NCIMB 41171, in healthy humans: a randomized, double-blind, crossover, placebo-controlled intervention study. Am. J. Clin. Nutr. 87 (2008), 785–791.
178. [178] Davis, L.M., Martinez, I., Walter, J., Goin, C., Hutkins, R.W., Barcoded pyrosequencing reveals that consumption of galactooligosaccharides results in a highly specific bifidogenic response in humans. PLoS One, 6, 2011, e25200.
179. [179] Vulevic, J., Juric, A., Walton, G.E., Claus, S.P., Tzortzis, G., Toward, R.E., Gibson, G.R., Influence of galacto-oligosaccharide mixture (B-GOS) on gut microbiota, immune parameters and metabonomics in elderly persons. Br. J. Nutr. 114 (2015), 586–595.
180. [180] Scott, K.P., Martin, J.C., Duncan, S.H., Flint, H.J., Prebiotic stimulation of human colonic butyrate-producing bacteria and Bifidobacteria in vitro. FEMS Microbiol. Ecol. 87 (2014), 30–40.
181. [181] Harmsen, H.J.M., Raangs, G.C., Franks, A.H., Wildeboer-Veloo, A.C.M., Welling, G.W., The effect of the prebiotic inulin and the probiotic Bifidobacterium longum on the fecal microflora of healthy volunteers measured by FISH and DGGE. Microb. Ecol. Health Dis., 14, 2011.
182. [182] Everard, A., Lazarevic, V., Gaia, N., Johansson, M., Stahlman, M., Backhed, F., Delzenne, N.M., Schrenzel, J., Francois, P., Cani, P.D., Microbiome of prebiotic-treated mice reveals novel targets involved in host response during obesity. ISME J. 8 (2014), 2116–2130.
183. [183] Ballongue, J., Schumann, C., Quignon, P., Effects of lactulose and lactitol on colonic microflora and enzymatic activity. Scand. J. Gastroenterol. Suppl. 222 (1997), 41–44.
184. [184] Kaneko, T., Kohmoto, T., Kikuchi, H., Shiota, M., Iino, H., Mitsuoka, T., Effects of isomaltooligosaccharides with different degrees of polymerization on human fecal Bifidobacteria. Biosci. Biotechnol. Biochem. 58 (1994), 2288–2290.
185. [185] Yen, C.H., Tseng, Y.H., Kuo, Y.W., Lee, M.C., Chen, H.L., Long-term supplementation of isomalto-oligosaccharides improved colonic microflora profile, bowel function, and blood cholesterol levels in constipated elderly people—a placebo-controlled, diet-controlled trial. Nutrition 27 (2011), 445–450.
186. [186] Childs, C.E., Roytio, H., Alhoniemi, E., Fekete, A.A., Forssten, S.D., Hudjec, N., Lim, Y.N., Steger, C.J., Yaqoob, P., Tuohy, K.M., Rastall, R.A., Ouwehand, A.C., Gibson, G.R., Xylo-oligosaccharides alone or in synbiotic combination with Bifidobacterium animalis subsp. lactis induce bifidogenesis and modulate markers of immune function in healthy adults: a double-blind, placebo-controlled, randomised, factorial cross-over study. Br. J. Nutr., 2014, 1–12, 10.1017/s0007114513004261.
187. [187] Finegold, S.M., Li, Z., Summanen, P.H., Downes, J., Thames, G., Corbett, K., Dowd, S., Krak, M., Heber, D., Xylooligosaccharide increases Bifidobacteria but not Lactobacilli in human gut microbiota. Food Funct. 5 (2014), 436–445.
188. [188] Troy, E.B., Kasper, D.L., Beneficial effects of Bacteroides fragilis polysaccharides on the immune system. Front. Biosci. 15 (2010), 25–34.
189. [189] Cloetens, L., Broekaert, W.F., Delaedt, Y., Ollevier, F., Courtin, C.M., Delcour, J.A., Rutgeerts, P., Verbeke, K., Tolerance of arabinoxylan-oligosaccharides and their prebiotic activity in healthy subjects: a randomised, placebo-controlled cross-over study. Br. J. Nutr. 103 (2010), 703–713.
190. [190] Walton, G.E., Lu, C., Trogh, I., Arnaut, F., Gibson, G.R., A randomised, double-blind, placebo controlled cross-over study to determine the gastrointestinal effects of consumption of arabinoxylan-oligosaccharides enriched bread in healthy volunteers. Nutr. J., 11, 2012, 36.
191. [191] Gomez, B., Gullon, B., Remoroza, C., Schols, H.A., Parajo, J.C., Alonso, J.L., Purification, characterization, and prebiotic properties of pectic oligosaccharides from orange peel wastes. J. Agric. Food Chem. 62 (2014), 9769–9782.
192. [192] McOrist, A.L., Miller, R.B., Bird, A.R., Keogh, J.B., Noakes, M., Topping, D.L., Conlon, M.A., Fecal butyrate levels vary widely among individuals but are usually increased by a diet high in resistant starch. J. Nutr. 141 (2011), 883–889.
193. [193] Goh, Y.J., Klaenhammer, T.R., Genetic mechanisms of prebiotic oligosaccharide metabolism in probiotic microbes. Annu. Rev. Food Sci. Technol. 6 (2015), 137–156.
194. [194] Bujacz, A., Jedrzejczak-Krzepkowska, M., Bielecki, S., Redzynia, I., Bujacz, G., Crystal structures of the apo form of beta-fructofuranosidase from Bifidobacterium longum and its complex with fructose. FEBS J. 278 (2011), 1728–1744.
195. [195] Rossi, M., Corradini, C., Amaretti, A., Nicolini, M., Pompei, A., Zanoni, S., Matteuzzi, D., Fermentation of fructooligosaccharides and inulin by Bifidobacteria: a comparative study of pure and fecal cultures. Appl. Environ. Microbiol. 71 (2005), 6150–6158.
196. [196] Barrangou, R., Altermann, E., Hutkins, R., Cano, R., Klaenhammer, T.R., Functional and comparative genomic analyses of an operon involved in fructooligosaccharide utilization by Lactobacillus acidophilus. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 8957–8962.
197. [197] O'Donnell, M.M., Forde, B.M., Neville, B., Ross, P.R., O'Toole, P.W., Carbohydrate catabolic flexibility in the mammalian intestinal commensal Lactobacillus ruminis revealed by fermentation studies aligned to genome annotations. Microb. Cell Factories, 10(Suppl. 1), 2011, S12.
198. [198] Saulnier, D.M., Molenaar, D., de Vos, W.M., Gibson, G.R., Kolida, S., Identification of prebiotic fructooligosaccharide metabolism in Lactobacillus plantarum WCFS1 through microarrays. Appl. Environ. Microbiol. 73 (2007), 1753–1765.
199. [199] Goh, Y.J., Lee, J.H., Hutkins, R.W., Functional analysis of the fructooligosaccharide utilization operon in Lactobacillus paracasei 1195. Appl. Environ. Microbiol. 73 (2007), 5716–5724.
200. [200] Andersen, J.M., Barrangou, R., Abou Hachem, M., Lahtinen, S., Goh, Y.J., Svensson, B., Klaenhammer, T.R., Transcriptional and functional analysis of galactooligosaccharide uptake by lacS in Lactobacillus acidophilus. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 17,785–17,790.
201. [201] Francl, A.L., Hoeflinger, J.L., Miller, M.J., Identification of lactose phosphotransferase systems in Lactobacillus gasseri ATCC 33323 required for lactose utilization. Microbiology 158 (2012), 944–952.
202. [202] O'Connell Motherway, M., Fitzgerald, G.F., van Sinderen, D., Metabolism of a plant derived galactose-containing polysaccharide by Bifidobacterium breve UCC2003. Microb. Biotechnol. 4 (2011), 403–416.
203. [203] Andersen, J.M., Barrangou, R., Abou Hachem, M., Lahtinen, S.J., Goh, Y.J., Svensson, B., Klaenhammer, T.R., Transcriptional analysis of oligosaccharide utilization by Bifidobacterium lactis Bl-04. BMC Genomics, 14, 2013, 312.
204. [204] Viborg, A.H., Fredslund, F., Katayama, T., Nielsen, S.K., Svensson, B., Kitaoka, M., Lo Leggio, L., Abou Hachem, M., A beta1-6/beta1-3 galactosidase from Bifidobacterium animalis subsp. lactis Bl-04 gives insight into sub-specificities of beta-galactoside catabolism within Bifidobacterium. Mol. Microbiol., 2014, 10.1111/mmi.12815.
205. [205] Viborg, A.H., Katayama, T., Abou Hachem, M., Andersen, M.C., Nishimoto, M., Clausen, M.H., Urashima, T., Svensson, B., Kitaoka, M., Distinct substrate specificities of three glycoside hydrolase family 42 beta-galactosidases from Bifidobacterium longum subsp. infantis ATCC 15697. Glycobiology 24 (2014), 208–216.
206. [206] Hinz, S.W., Pastink, M.I., van den Broek, L.A., Vincken, J.P., Voragen, A.G., Bifidobacterium longum endogalactanase liberates galactotriose from type I galactans. Appl. Environ. Microbiol. 71 (2005), 5501–5510.
207. [207] O'Connell Motherway, M., Kinsella, M., Fitzgerald, G.F., van Sinderen, D., Transcriptional and functional characterization of genetic elements involved in galacto-oligosaccharide utilization by Bifidobacterium breve UCC2003. Microb. Biotechnol. 6 (2013), 67–79.
208. [208] Sela, D.A., Mills, D.A., Nursing our microbiota: molecular linkages between Bifidobacteria and milk oligosaccharides. Trends Microbiol. 18 (2010), 298–307.
209. [209] Andersen, J.M., Barrangou, R., Hachem, M.A., Lahtinen, S.J., Goh, Y.J., Svensson, B., Klaenhammer, T.R., Transcriptional analysis of prebiotic uptake and catabolism by Lactobacillus acidophilus NCFM. PLoS One, 7, 2012, e44409.
210. [210] Moller, M.S., Fredslund, F., Majumder, A., Nakai, H., Poulsen, J.C., Lo Leggio, L., Svensson, B., Abou Hachem, M., Enzymology and structure of the GH13_31 glucan 1,6-alpha-glucosidase that confers isomaltooligosaccharide utilization in the probiotic Lactobacillus acidophilus NCFM. J. Bacteriol. 194 (2012), 4249–4259.
211. [211] Nakai, H., Baumann, M.J., Petersen, B.O., Westphal, Y., Schols, H., Dilokpimol, A., Hachem, M.A., Lahtinen, S.J., Duus, J.Ø., Svensson, B., The maltodextrin transport system and metabolism in Lactobacillus acidophilus NCFM and production of novel alpha-glucosides through reverse phosphorolysis by maltose phosphorylase. FEBS J. 276 (2009), 7353–7365.
212. [212] Abou Hachem, M., Møller, M.S., Andersen, J.M., Fredslund, F., Majumder, A., Nakai, H., Lo Leggio, L., Goh, Y.-J., Barrangou, R., Klaenhammer, T.R., Svensson, B., A snapshot into the metabolism of isomalto-oligosaccharides in probiotic bacteria. J. Appl. Glycosci. 60 (2013), 95–100.
213. [213] O'Connell Motherway, M., Fitzgerald, G.F., Neirynck, S., Ryan, S., Steidler, L., van Sinderen, D., Characterization of apuB, an extracellular type II amylopullulanase from Bifidobacterium breve UCC2003. Appl. Environ. Microbiol. 74 (2008), 6271–6279.
214. [214] Ejby, M., Fredslund, F., Vujicic-Zagar, A., Svensson, B., Slotboom, D.J., Abou Hachem, M., Structural basis for arabinoxylo-oligosaccharide capture by the probiotic Bifidobacterium animalis subsp. lactis Bl-04. Mol. Microbiol. 90 (2013), 1100–1112.
215. [215] Gilad, O., Jacobsen, S., Stuer-Lauridsen, B., Pedersen, M.B., Garrigues, C., Svensson, B., Combined transcriptome and proteome analysis of Bifidobacterium animalis subsp lactis BB-12 grown on xylo-oligosaccharides and a model of their utilization. Appl. Environ. Microbiol. 76 (2010), 7285–7291.
216. [216] Li, Z., Summanen, P.H., Komoriya, T., Finegold, S.M., In vitro study of the prebiotic xylooligosaccharide (XOS) on the growth of Bifidobacterium spp and Lactobacillus spp. Int. J. Food Sci. Nutr. 66 (2015), 919–922.
217. [217] Michlmayr, H., Hell, J., Lorenz, C., Bohmdorfer, S., Rosenau, T., Kneifel, W., Arabinoxylan oligosaccharide hydrolysis by family 43 and 51 glycosidases from Lactobacillus brevis DSM 20054. Appl. Environ. Microbiol. 79 (2013), 6747–6754.