A refined palate: Bacterial consumption of host glycans in the gut

Glycobiology

Volumn 23, Issue 9, 2013, Pages 1038-1046

  Marcobal, Angela ^a   Southwick, Audrey M ^a   Earle, Kristen A ^a   Sonnenburg, Justin L ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Gut microbiota; Host microbial interaction; Microbiome; Mucin; Polysaccharide utilization

Indexed keywords

GLYCAN; MUCIN;

AMINO ACID SEQUENCE; BACTEROIDES; BACTEROIDES THETAIOTAOMICRON; BIFIDOBACTERIUM BIFIDUM; BIFIDOBACTERIUM LONGUM; CELIAC DISEASE; COMPARATIVE GENOMIC HYBRIDIZATION; CROHN DISEASE; ENERGY; FUCOSYLATION; FUNCTIONAL GENOMICS; GENETIC SCREENING; GNOTOBIOTICS; HORIZONTAL GENE TRANSFER; HOST PATHOGEN INTERACTION; HUMAN; INTESTINE FLORA; INTESTINE MUCOSA PERMEABILITY; LACTOBACILLUS FERMENTUM; LACTOBACILLUS PLANTARUM; LACTOBACILLUS RHAMNOSUS; METAGENOMICS; MICROBIAL COMMUNITY; MICROFLORA; MOLECULAR GENETICS; MUCUS; NONHUMAN; NUTRIENT SUPPLY; ORGANISMAL INTERACTION; PLANT CELL; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; PROTEIN STRUCTURE; PROTEOMICS; REVIEW; SIALYLATION; SULFATION; TRANSCRIPTOMICS; VERRUCOMICROBIA;

GUT MICROBIOTA; HOST-MICROBIAL INTERACTION; MICROBIOME; MUCIN; POLYSACCHARIDE UTILIZATION;

BACTERIA; HUMANS; INTESTINES; POLYSACCHARIDES;

EID: 84880958392     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwt040     Document Type: Review

References (104)

1. An G, Wei B, Xia B, McDaniel JM, Ju T, Cummings RD, Braun J, Xia L. 2007. Increased susceptibility to colitis and colorectal tumors in mice lacking core 3-derived O-glycans. J Exp Med. 204: 1417-1429.
2. Bayliss CE, Turner RJ. 1982. Examination of organisms associated with mucin in the colon by scanning electron-microscopy. Micron. 13: 35-40.
3. Benjdia A, Leprince J, Guillot A, Vaudry H, Rabot S, Berteau O. 2007. Anaerobic sulfatase-maturating enzymes: Radical SAM enzymes able to catalyze in vitro sulfatase post-translational modification. J Am Chem Soc. 129: 3462-3463.
4. Benjdia A, Martens EC, Gordon JI, Berteau O. 2011. Sulfatases and a radical S-adenosyl-L-methionine (Ado Met) enzyme are key for mucosal foraging and fitness of the prominent human gut symbiont, Bacteroides thetaiotaomicron. J Biol Chem. 286: 25973-25982.
5. Bjursell MK, Martens EC, Gordon JI. 2006. Functional genomic and metabolic studies of the adaptations of a prominent adult human gut symbiont, Bacteroides thetaiotaomicron, to the suckling period. J Biol Chem. 281: 36269-36279.
6. Bode L. 2012. Human milk oligosaccharides: Every baby needs a sugar mama. Glycobiology. 22: 1147-1162.
7. Boekhorst J, Helmer Q, Kleerebezem M, Siezen RJ. 2006. Comparative analysis of proteins with a mucus-binding domain found exclusively in lactic acid bacteria. Microbiology. 152: 273-280.
8. Bry L, Falk PG, Midtvedt T, Gordon JI. 1996. A model of host-microbial interactions in an open mammalian ecosystem. Science. 273: 1380-1383.
9. Buck BL, Altermann E, Svingerud T, Klaenhammer TR. 2005. Functional analysis of putative adhesion factors in Lactobacillus acidophilus NCFM. Appl Environ Microbiol. 71: 8344-8351.
10. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. 2009. The Carbohydrate-Active EnZymes database (CAZy): An expert resource for glycogenomics. Nucleic Acids Res. 37: D233-D238.
11. Capon C, Maes E, Michalski JC, Leffler H, Kim YS. 2001. Sd(a)-antigen-like structures carried on core 3 are prominent features of glycans from the mucin of normal human descending colon. Biochem J. 358: 657-664.
12. Carey HV, Walters WA, Knight R. 2013. Seasonal restructuring of the ground squirrel gut microbiota over the annual hibernation cycle. Am J Physiol Regul Integr Comp Physiol. 304: R33-R42.
13. Carlson BL, Ballister ER, Skordalakes E, King DS, Breidenbach MA, Gilmore SA, Berger JM, Bertozzi CR. 2008. Function and structure of a prokaryotic formylglycine-generating enzyme. J Biol Chem. 283: 20117-20125.
14. Comstock LE, Pantosti A, Kasper DL. 2000. Genetic diversity of the capsular polysaccharide C biosynthesis region of Bacteroides fragilis. Infect Immun. 68: 6182-6188.
15. Corfield AP, Carroll D, Myerscough N, Probert CSJ. 2001. Mucins in the gastrointestinal tract in health and disease. Front Biosci. 6: D1321-D1357.
16. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, Collini S, Pieraccini G, Lionetti P. 2010. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci USA. 107: 14691-14696.
17. D'Elia JN, Salyers AA. 1996. Effect of regulatory protein levels on utilization of starch by Bacteroides thetaiotaomicron. J Bacteriol. 178: 7180-7186.
18. Derrien M, Vaughan EE, Plugge CM, de Vos WM. 2004. Akkermansia muciniphila gen. nov., sp nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol. 54: 1469-1476.
19. Dierks T, Schmidt B, Borissenko LV, Peng JH, Preusser A, Mariappan M, von Figura K. 2003. Multiple sulfatase deficiency is caused by mutations in the gene encoding the human C-α-formylglycine generating enzyme. Cell. 113: 435-444.
20. Douillard FP, Ribbera A, Jarvinen HM, Kant R, Pietila TE, Randazzo C, Paulin L, Laine PK, Caggia C, von Ossowski I, et al. 2013. Comparative genomic and functional analysis of Lactobacillus casei and Lactobacillus rhamnosus strains marketed as probiotics. Appl Environ Microbiol. 79: 1923-1933.
21. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA. 2005. Diversity of the human intestinal microbial flora. Science. 308: 1635-1638.
22. Fabich AJ, Jones SA, Chowdhury FZ, Cernosek A, Anderson A, Smalley D, McHargue JW, Hightower GA, Smith JT, Autieri SM, et al. 2008. Comparison of carbon nutrition for pathogenic and commensal Escherichia coli strains in the mouse intestine. Infect Immun. 76: 1143-1152.
23. Franks I. 2012. Gut microbiota: FUT2 genotype influences the gut microbiota in patients with Crohn's disease and healthy individuals. Nat Rev Gastroenterol Hepatol. 9: 2-2.
24. Fu J, Wei B, Wen T, Johansson MEV, Liu X, Bradford E, Thomsson KA, McGee S, Mansour L, Tong M, et al. 2011. Loss of intestinal core 1-derived O-glycans causes spontaneous colitis in mice. J Clin Invest. 121: 1657-1666.
25. Garrido D, Kim JH, German JB, Raybould HE, Mills DA. 2011. Oligosaccharide binding proteins from Bifidobacterium longum subsp. infantis reveal a preference for host glycans. PLoS One. 6: e17315-e17315.
26. Gnoth MJ, Kunz C, Kinne-Saffran E, Rudloff S. 2000. Human milk oligosaccharides are minimally digested in vitro. J Nutr. 130: 3014-3020.
27. Goh YJ, Klaenhammer TR. 2010. Functional roles of aggregation- promotinglike factor in stress tolerance and adherence of Lactobacillus acidophilus NCFM. Appl Environ Microbiol. 76: 5005-5012.
28. Gonzalez-Rodriguez I, Sanchez B, Ruiz L, Turroni F, Ventura M, Ruas-Madiedo P, Gueimonde M, Margolles A. 2012. Role of extracellular transaldolase from Bifidobacterium bifidum in mucin adhesion and aggregation. Appl Environ Microbiol. 78: 3992-3998.
29. Gorbach SL. 2000. Probiotics and gastrointestinal health. Am J Gastroenterol. 95: S2-S4.
30. Hanisch FG, Chai WG, Rosankiewicz JR, Lawson AM, Stoll MS, Feizi T. 1993. Core-typing of O-linked glycans from human gastric mucins-lack of evidence for the occurrence of the core sequence Gal1-6-GalNAc. Eur J Biochem. 217: 645-655.
31. Hansson GC. 2012. Role of mucus layers in gut infection and inflammation. Curr Opin Microbiol. 15: 57-62.
32. Hehemann J-H, Correc G, Barbeyron T, Helbert W, Czjzek M, Michel G. 2010. Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota. Nature. 464: 908-U123.
33. Hehemann J-H, Kelly AG, Pudlo NA, Martens EC, Boraston AB. 2012. Bacteria of the human gut microbiome catabolize red seaweed glycans with carbohydrate-active enzyme updates from extrinsic microbes. Proc Natl Acad Sci USA. 109: 19786-19791.
34. Hooper LV, Xu J, Falk PG, Midtvedt T, Gordon JI. 1999. A molecular sensor that allows a gut commensal to control its nutrient foundation in a competitive ecosystem. Proc Natl Acad Sci USA. 96: 9833-9838.
35. Hoskins LC, Zamcheck N. 1968. Bacterial degradation of gastrointestinal mucins. Comparison of mocus constituents in stools of germ-free and conventional rats. Gastroenterology. 54: 210.
36. Huang JY, Lee SM, Mazmanian SK. 2011. The human commensal Bacteroides fragilis binds intestinal mucin. Anaerobe. 17: 137-141.
37. Ismail MN, Stone EL, Panico M, Lee SH, Luu Y, Ramirez K, Ho SB, Fukuda M, Marth JD, Haslam SM, et al. 2011. High-sensitivity O-glycomic analysis of mice deficient in core 2 beta 1, 6-N-acetylglucosaminyltransferases. Glycobiology. 21: 82-98.
38. Johansson MEV, Gustafsson JK, Holmen-Larsson J, Jabbar KS, Xia L, Ghishan FK, Carvalho FA, Gewirtz AT, Sjovall H, Hannson GC. 2013. Bacteria penetrate the normally impenetrable inner colon mucus layer in both murine colitis models and patients with ulcerative colitis. Gut. [Epub ahead of print 20 February 2013].
39. Johansson MEV, Larsson JMH, Hansson GC. 2011. 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 USA. 108: 4659-4665.
40. Kankainen M, Paulin L, Tynkkynen S, von Ossowski I, Reunanen J, Partanen P, Satokari R, Vesterlund S, Hendrickx APA, Lebeer S, et al. 2009. Comparative genomic analysis of Lactobacillus rhamnosus GG reveals pili containing a human-mucus binding protein. Proc Natl Acad Sci USA. 106: 17193-17198.
41. Karlsson NG, Herrmann A, Karlsson H, Johansson MEV, Carlstedt I, Hansson GC. 1997. The glycosylation of rat intestinal Muc2 mucin varies between rat strains and the small and large intestine-A study of O-linked oligosaccharides by a mass spectrometric approach. J Biol Chem. 272: 27025-27034.
42. Karlsson NG, Nordman H, Karlsson H, Carlstedt I, Hansson GC. 1997. Glycosylation differences between pig gastric mucin populations: A comparative study of the neutral oligosaccharides using mass spectrometry. Biochem J. 326: 911-917.
43. Koropatkin NM, Martens EC, Gordon JI, Smith TJ. 2008. Starch catabolism by a prominent human gut symbiont is directed by the recognition of amylose helices. Structure. 16: 1105-1115.
44. Larsson JMH, Karlsson H, Crespo JG, Johansson MEV, Eklund L, Sjovall H, Hansson GC. 2011. Altered O-glycosylation profile of MUC2 mucin occurs in active ulcerative colitis and is associated with increased inflammation. Inflamm Bowel Dis. 17: 2299-2307.
45. Larsson JMH, Karlsson H, Sjovall H, Hansson GC. 2009. A complex, but uniform O-glycosylation of the human MUC2 mucin from colonic biopsies analyzed by nano LC/MSn. Glycobiology. 19: 1568-1569.
46. Lowe EC, Basle A, Czjzek M, Firbank SJ, Bolam DN. 2012. A scissor bladelike closing mechanism implicated in transmembrane signaling in a Bacteroides hybrid two-component system. Proc Natl Acad Sci USA. 109: 7298-7303.
47. Lozupone C, Faust K, Raes J, Faith JJ, Frank DN, Zaneveld J, Gordon JI, Knight R. 2012. Identifying genomic and metabolic features that can underline early successional and opportunistic lifestyles of human gut symbionts. Genome Res. 22: 1974-1984.
48. Lynch JB, Sonnenburg JL. 2012. Prioritization of a plant polysaccharide over a mucus carbohydrate is enforced by a Bacteroides hybrid two-component system. Mol Microbiol. 85: 478-491.
49. Macfarlane GT, Gibson GR. 1991. Formation of glycoprotein degrading enzymes by Bacteroides fragilis. FEMS Microbiol Lett. 77: 289-293.
50. Macias-Rodriguez ME, Zagorec M, Ascencio F, Vazquez-Juarez R, Rojas M. 2009. Lactobacillus fermentum BCS87 expresses mucus- and mucin-binding proteins on the cell surface. J Appl Microbiol. 107: 1866-1874.
51. MacKenzie DA, Jeffers F, Parker ML, Vibert-Vallet A, Bongaerts RJ, Roos S, Walter J, Juge N. 2010. Strain-specific diversity of mucus-binding proteins in the adhesion and aggregation properties of Lactobacillus reuteri. Microbiology. 156: 3368-3378.
52. Mahowald MA, Rey FE, Seedorf H, Turnbaugh PJ, Fulton RS, Wollam A, Shah N, Wang C, Magrini V, Wilson RK, et al. 2009. Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla. Proc Natl Acad Sci USA. 106: 5859-5864.
53. Manzi AE, Norgard-Sumnicht K, Argade S, Marth JD, van Halbeek H, Varki A. 2000. Exploring the glycan repertoire of genetically modified mice by isolation and profiling of the major glycan classes and nano-NMR analysis of glycan mixtures. Glycobiology. 10: 669-689.
54. Marcobal A, Barboza M, Sonnenburg ED, Pudlo N, Martens EC, Desai P, Lebrilla CB, Weimer BC, Mills DA, German JB, et al. 2011. Bacteroides in the infant gut consume milk oligosaccharides via mucus-utilization pathways. Cell Host Microbe. 10: 507-514.
55. Martens EC, Chiang HC, Gordon JI. 2008. Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host Microbe. 4: 447-457.
56. Martens EC, Lowe EC, Chiang H, Pudlo NA, Wu M, McNulty NP, Abbott DW, Henrissat B, Gilbert HJ, Bolam DN, et al. 2011. Recognition and degradation of plant cell wall polysaccharides by two human gut symbionts. PLoS Biol. 9.
57. McGovern DPB, Jones MR, Taylor KD, Marciante K, Yan X, Dubinsky M, Ippoliti A, Vasiliauskas E, Berel D, Derkowski C, et al. 2010. Fucosyltransferase 2 (FUT2) non-secretor status is associated with Crohn's disease. Hum Mol Genet. 19: 3468-3476.
58. Miller JB, McVeagh P. 1999. Human milk oligosaccharides: 130 reasons to breast-feed. Br J Nutr. 82: 333-335.
59. Miyoshi Y, Okada S, Uchimura T, Satoh E. 2006. A mucus adhesion promoting protein, Map A, mediates the adhesion of Lactobacillus reuteri to Caco-2 human intestinal epithelial cells. Biosci Biotechnol Biochem. 70: 1622-1628.
60. Moran AP, Gupta A, Joshi L. 2011. Sweet-talk: Role of host glycosylation in bacterial pathogenesis of the gastrointestinal tract. Gut. 60: 1412-1425.
61. Ninonuevo MR, Park Y, Yin H, Zhang J, Ward RE, Clowers BH, German JB, Freeman SL, Killeen K, Grimm R, et al. 2006. A strategy for annotating the human milk glycome. J Agric Food Chem. 54: 7471-7480.
62. Nordman H, Davies JR, Herrmann A, Karlsson NG, Hansson GC, Carlstedt I. 1997. Mucus glycoproteins from pig gastric mucose: Identification of different mucin populations from the surface epithelium. Biochem J. 326: 903-910.
63. Nyholm SV, Stabb EV, Ruby EG, McFall-Ngai MJ. 2000. Establishment of an animal-bacterial association: Recruiting symbiotic vibrios from the environment. Proc Natl Acad Sci USA. 97: 10231-10235.
64. O'Connell Motherway M, Zomer A, Leahy SC, Reunanen J, Bottacini F, Claesson MJ, O'Brien F, Flynn K, Casey PG, Munoz JAM, et al. 2011. Functional genome analysis of Bifidobacterium breve UCC2003 reveals type IVb tight adherence (Tad) pili as an essential and conserved host-colonization factor. Proc Natl Acad Sci USA. 108: 11217-11222.
65. Pacheco AR, Curtis MM, Ritchie JM, Munera D, Waldor MK, Moreira CG, Sperandio V. 2012. Fucose sensing regulates bacterial intestinal colonization. Nature. 492: 113-117.
66. Parmar AS, Lappalainen M, Paavola-Sakki P, Halme L, Farkkila M, Turunen U, Kontula K, Aromaa A, Salomaa V, Peltonen L, et al. 2012. Association of celiac disease genes with inflammatory bowel disease in Finnish and Swedish patients. Genes Immun. 13: 474-480.
67. Patsos G, Corfield A. 2009. Management of the human mucosal defensive barrier: Evidence for glycan legislation. Biol Chem. 390: 581-590.
68. Png CW, Linden SK, Gilshenan KS, Zoetendal EG, McSweeney CS, Sly LI, McGuckin MA, Florin THJ. 2010. Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria. Am J Gastroenterol. 105: 2420-2428.
69. Podolsky DK. 1985a. Oligosaccharides structures of huma colonic mucin. J Biol Chem. 260: 8264-8271.
70. Podolsky DK. 1985b. Oligosaccharides structures of isolated human colonic mucin species. J Biol Chem. 260: 5510-5515.
71. Pultz NJ, Vesterlund S, Ouwehand AC, Donskey CJ. 2006. Adhesion of vancomycin-resistant Enterococcus to human intestinal mucus. Curr Microbiol. 52: 221-224.
72. Rausch P, Rehman A, Kuenzel S, Haesler R, Ott SJ, Schreiber S, Rosenstiel P, Franke A, Baines JF. 2011. Colonic mucosa-associated microbiota is influenced by an interaction of Crohn disease and FUT2 (Secretor) genotype. Proc Natl Acad Sci USA. 108: 19030-19035.
73. Reeves AR, Delia JN, Frias J, Salyers AA. 1996. A Bacteroides thetaiotaomicron outer membrane protein that is essential for utilization of maltooligosaccharides and starch. J Bacteriol. 178: 823-830.
74. Robbe C, Capon C, Coddeville B, Michalski JC. 2004. Structural diversity and specific distribution of O-glycans in normal human mucins along the intestinal tract. Biochem J. 384: 307-316.
75. Robbe C, Capon C, Maes E, Rousset M, Zweibaum A, Zanetta JP, Michalski JC. 2003. Evidence of regio-specific glycosylation in human intestinal mucins-Presence of an acidic gradient along the intestinal tract. J Biol Chem. 278: 46337-46348.
76. Robbe-Masselot C, Maes E, Rousset M, Michalski J-C, Capon C. 2009. Glycosylation of human fetal mucins: A similar repertoire of O-glycans along the intestinal tract. Glycoconj J. 26: 397-413.
77. Roberton AM, Stanley RA. 1982. In vitro utilization of mucin by Bacteroides fragilis. Appl Environ Microbiol. 43: 325-330.
78. Rojas M, Ascencio F, Conway PL. 2002. Purification and characterization of a surface protein from Lactobacillus fermentum 104R that binds to porcine small intestinal mucus and gastric mucin. Appl Environ Microbiol. 68: 2330-2336.
79. Roos S, Jonsson H. 2002. A high-molecular-mass cell-surface protein from Lactobacillus reuteri 1063 adheres to mucus components. Microbiology. 148: 433-442.
80. Ruas-Madiedo P, Gueimonde M, Fernandez-Garcia M, de los Reyes-Gavilan CG, Margolles A. 2008. Mucin degradation by Bifidobacterium strains isolated from the human intestinal microbiota. Appl Environ Microbiol. 74: 1936-1940.
81. Ruhaak LR, Lebrilla CB. 2012. Analysis and role of oligosaccharides in milk. BMB Rep. 45: 442-451.
82. Salyers AA, West SEH, Vercellotti JR, Wilkins TD. 1977. Fermentation of mucins and plant polysaccharides by anaerobic bacteria from human colon. Appl Environ Microbiol. 34: 529-533.
83. Schell MA, Karmirantzou M, Snel B, Vilanova D, Berger B, Pessi G, Zwahlen MC, Desiere F, Bork P, Delley M, et al. 2002. The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proc Natl Acad Sci USA. 99: 14422-14427.
84. Sela DA, Mills DA. 2010. Nursing our microbiota: Molecular linkages between bifidobacteria and milk oligosaccharides. Trends Microbiol. 18: 298-307.
85. Shipman JA, Berleman JE, Salyers AA. 2000. Characterization of four outer membrane proteins involved in binding starch to the cell surface of Bacteroides thetaiotaomicron. J Bacteriol. 182: 5365-5372.
86. Slomiany BL, Murty VLN, Slomiany A. 1980. Isolation and characterization of oligosaccharides from rat colonic mucus glycoprotein. J Biol Chem. 255: 9719-9723.
87. Sonnenburg JL, Angenent LT, Gordon JI. 2004. Getting a grip on things: How do communities of bacterial symbionts become established in our intestine? Nat Immunol. 5: 569-573.
88. Sonnenburg JL, Xu J, Leip DD, Chen CH, Westover BP, Weatherford J, Buhler JD, Gordon JI. 2005. Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science. 307: 1955-1959.
89. Sonnenburg ED, Zheng H, Joglekar P, Higginbottom SK, Firbank SJ, Bolam DN, Sonnenburg JL. 2010. Specificity of polysaccharide use in intestinal Bacteroides species determines diet-induced microbiota alterations. Cell. 141: 1241-U1256.
90. Stahl M, Friis LM, Nothaft H, Liu X, Li J, Szymanski CM, Stintzi A. 2011. L-Fucose utilization provides Campylobacter jejuni with a competitive advantage. Proc Natl Acad Sci USA. 108: 7194-7199.
91. Thomsson KA, Hinojosa-Kurtzberg M, Axelsson KA, Domino SE, Lowe JB, Gendler SJ, Hansson GC. 2002. Intestinal mucins from cystic fibrosis mice show increased fucosylation due to an induced Fuc α1-2 glycosyltransferase. Biochem J. 367: 609-616.
92. Thomsson KA, Holmen-Larsson JM, Angstrom J, Johansson MEV, Xia L, Hansson GC. 2012. Detailed O-glycomics of the Muc2 mucin from colon of wild-type, core 1-and core 3-transferase-deficient mice highlights differences compared with human MUC2. Glycobiology. 22: 1128-1139.
93. Troy EB, Carey VJ, Kasper DL, Comstock LE. 2010. Orientations of the Bacteroides fragilis capsular polysaccharide biosynthesis locus promoters during symbiosis and infection. J Bacteriol. 192: 5832-5836.
94. Turroni F, Milani C, van Sinderen D, Ventura M. 2011. Genetic strategies for mucin metabolism in Bifidobacterium bifidum PRL2010: An example of possible human-microbe co-evolution. Gut microbes. 2: 183-189.
95. Urashima T, Asakuma S, Leo F, Fukuda K, Messer M, Oftedal OT. 2012. The predominance of type I oligosaccharides is a feature specific to human breast milk. Adv Nutr. 3: 473S-482S.
96. Varki A, Cummings JH, Esko JD, Freeze HH, Stanley P, Bertozzi CR, Hart GW, Etzler ME. 2009. O-GalNAc glycans. In: Essentials of Glycobiology, 2nd ed. Cold Spring Harbor (NY): CSHL Press.
97. Velez MP, De Keersmaecker SCJ, Vanderleyden J. 2007. Adherence factors of Lactobacillus in the human gastrointestinal tract. FEMS Microbiol Lett. 276: 140-148.
98. Wada J, Ando T, Kiyohara M, Ashida H, Kitaoka M, Yamaguchi M, Kumagai H, Katayama T, Yamamoto K. 2008. Bifidobacterium bifidum lacto-N-biosidase, a critical enzyme for the degradation of human milk oligosaccharides with a type 1 structure. Appl Environ Microbiol. 74: 3996-4004.
99. Wasilewska E, Markiewicz LH, Bielecka M. 2008. Stimulation of Bifidobacteria growth by oligofructose and mucin. Polish J Food Nutr Sci. 58: 443-449.
100. Willis CL, Cummings JH, Neale G, Gibson GR. 1996. In vitro effects of mucin fermentation on the growth of human colonic sulphate-reducing bacteria. Anaerobe. 2: 117-122.
101. Wu S, Tao N, German JB, Grimm R, Lebrilla CB. 2010. Development of an annotated library of neutral human milk oligosaccharides. J Proteome Res. 9: 4138-4151.
102. Xu J, Mahowald MA, Ley RE, Lozupone CA, Hamady M, Martens EC, Henrissat B, Coutinho PM, Minx P, Latreille P, et al. 2007. Evolution of symbiotic bacteria in the distal human intestine. PLoS Biol. 5: 1574-1586.
103. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP, et al. 2012. Human gut microbiome viewed across age and geography. Nature. 486: 222.
104. Yu Z-T, Chen C, Kling DE, Liu B, McCoy JM, Merighi M, Heidtman M, Newburg DS. 2013. The principal fucosylated oligosaccharides of human milk exhibit prebiotic properties on cultured infant microbiota. Glycobiology. 23: 169-177.