Biochemistry (Moscow)

, Volume 82, Issue 9, pp 973–989 | Cite as

How fucose of blood group glycotypes programs human gut microbiota

Review

Abstract

Formation of appropriate gut microbiota is essential for human health. The first two years of life is the critical period for this process. Selection of mutualistic microorganisms of the intestinal microbiota is controlled by the FUT2 and FUT3 genes that encode fucosyltransferases, enzymes responsible for the synthesis of fucosylated glycan structures of mucins and milk oligosaccharides. In this review, the mechanisms of the selection and maintenance of intestinal microorganisms that involve fucosylated oligosaccharides of breast milk and mucins of the newborn’s intestine are described. Possible reasons for the use of fucose, and not sialic acid, as the major biological signal for the selection are also discussed.

Keywords

intestinal microbiota FUT2 and FUT3 genes fucosyltransferases fucose sialic acids plant polysaccharides glycotopes 

Abbreviations

CAZy

Carbohydrate-Active Enzymes database (http://afmb.cnrs-mrs.fr/CAZY)

Fuc

fucose

FucT

fucosyltransferase

Gal

galactose

GalN

D-galactosamine

GalNAc

N-acetyl-D-galactosamine

GH

glycoside hydrolase

GlcN

Dglucosamine

GlcNAc

N-acetyl-D-glucosamine

GT

glycoside transferase

Le

Lewis antigen

Man

mannose

Neu5Ac

Nacetylneuraminic acid

Neu5Gc

N-glycolylneuraminic acid

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References

  1. 1.
    Zilber-Rosenberg, I., and Rosenberg, E. (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution, FEMS Microbiol. Rev., 32, 723–735.PubMedCrossRefGoogle Scholar
  2. 2.
    Eckburg, P. B., Bik, E. M., Bernstein, C. N., Purdom, E., Dethlefsen, L., Sargent, M., Gill, S. R., Nelson, K. E., and Relman, D. A. (2005) Diversity of the human intestinal microbial flora, Science, 308, 1635–1638.PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Tremaroli, V., and Backhed, F. (2012) Functional interactions between the gut microbiota and host metabolism, Nature, 489, 242–249.PubMedCrossRefGoogle Scholar
  4. 4.
    Flint, H. J., Scott, K. P., Duncan, S. H., Louis, P., and Forano, E. (2012) Microbial degradation of complex carbohydrates in the gut, Gut Microbes, 3, 289–306.PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Fischbach, M. A., and Sonnenburg, J. L. (2011) Eating for two: how metabolism establishes interspecies interactions in the gut, Cell Host Microbe, 10, 336–347.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Backhed, F., Ley, R. E., Sonnenburg, J. L., Peterson, D. A., and Gordon, J. I. (2005) Host–bacterial mutualism in the human intestine, Science, 307, 1915–1920.PubMedCrossRefGoogle Scholar
  7. 7.
    Den Besten, G., Van Eunen, K., Groen, A. K., Venema, K., Reijngoud, D. J., and Bakker, B. M. (2013) The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism, J. Lipid Res., 54, 2325–2340.CrossRefGoogle Scholar
  8. 8.
    Ley, R. E., Peterson, D. A., and Gordon, J. I. (2006) Ecological and evolutionary forces shaping microbial diversity in the human intestine, Cell, 124, 837–848.PubMedCrossRefGoogle Scholar
  9. 9.
    Wopereis, H., Oozeer, R., Knipping, K., Belzer, C., and Knol, J. (2014) The first thousand days-intestinal microbiology of early life: establishing a symbiosis, Pediatr. Allergy Immunol., 25, 428–438.PubMedCrossRefGoogle Scholar
  10. 10.
    Ajslev, T. A., Andersen, C. S., Gamborg, M., Sorensen, T. I. A., and Jess, T. (2011) Childhood overweight after establishment of the gut microbiota: the role of delivery mode, pre-pregnancy weight and early administration of antibiotics, Int. J. Obes., 35, 522–529.CrossRefGoogle Scholar
  11. 11.
    Bercik, P., Collins, S. M., and Verdu, E. F. (2012) Microbes and the gut−brain axis, Neurogastroenterol. Motil., 24, 405–413.PubMedCrossRefGoogle Scholar
  12. 12.
    Spor, A., Koren, O., and Ley, R. (2011) Unravelling the effects of the environment and host genotype on the gut microbiome, Nat. Rev. Microbiol., 9, 279–290.PubMedCrossRefGoogle Scholar
  13. 13.
    Gabius, H. J. (2000) Biological information transfer beyond the genetic code: the sugar code, Naturwissenschaften, 87, 108–121.PubMedCrossRefGoogle Scholar
  14. 14.
    Varki, A., and Lowe, J. B. (2009) in Essentials of Glycobiology (Varki, A., Cummings, R. D., Esko, J. D., Freeze, H. H., Stanley, P., Bertozzi, C. R., Hart, G. W., and Etzler, M. E., eds.) 2nd Edn., Cold Spring Harbor Laboratory Press, New York, Chap.6.Google Scholar
  15. 15.
    Bishop, J. R., and Gagneux, P. (2007) Evolution of carbohydrate antigens–microbial forces shaping host glycomes? Glycobiology, 17, 23R–34R.PubMedCrossRefGoogle Scholar
  16. 16.
    Gabius, H. J. (2001) Eukaryotic glycosylation and lectins: hardware of the sugar code (glycocode) in biological information transfer, Electr. J. Pathol. Histol., 7, 05.Google Scholar
  17. 17.
    Andre, S., Kaltner, H., Manning, J. C., Murphy, P. V., and Gabius, H. J. (2015) Lectins: getting familiar with translators of the sugar code, Molecules, 20, 1788–1823.PubMedCrossRefGoogle Scholar
  18. 18.
    Varki, A. (2006) Nothing in glycobiology makes sense, except in the light of evolution, Cell, 126, 841–845.PubMedCrossRefGoogle Scholar
  19. 19.
    Varki, A. (2011) Evolutionary forces shaping the Golgi glycosylation machinery: why cell surface glycans are universal to living cells, Cold Spring Harb. Perspect. Biol., 3, a005462.PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Angata, T., and Varki, A. (2002) Chemical diversity in the sialic acids and related α-keto acids: an evolutionary perspective, Chem. Rev., 102, 439–470.PubMedCrossRefGoogle Scholar
  21. 21.
    Buddington, R. K., and Weiher, E. (1999) The application of ecological principles and fermentable fibers to manage the gastrointestinal tract ecosystem, J. Nutr., 129, 1446S1450S.Google Scholar
  22. 22.
    Rabiu, B. A., and Gibson, G. R. (2002) Carbohydrates: a limit on bacterial diversity within the colon, Biol. Rev. Camb. Philos. Soc., 77, 443–453.PubMedCrossRefGoogle Scholar
  23. 23.
    Tailford, L. E., Crost, E. H., Kavanaugh, D., and Juge, N. (2015) Mucin glycan foraging in the human gut microbiome, Front. Genet., 6, 81.PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Hennet, T., Weiss, A., and Borsig, L. (2014) Decoding breast milk oligosaccharides, Swiss Med. Wkly, 144, w13927.PubMedGoogle Scholar
  25. 25.
    Nguema-Ona, E., Vicre-Gibouin, M., Gotte, M., Plancot, B., Lerouge, P., Bardor, M., and Driouich, A. (2015) in Plant Glycobiology–A Sweet World of Lectins, Glycoproteins, Glycolipids and Glycans (Van Damme Els, J. M., Lannoo, N., Albenne, C., and Jamet, E., eds.) Vol. 5, Frontiers Media SA, Lausanne, pp. 8–19.Google Scholar
  26. 26.
    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., and Gordon, J. I. (2011) Recognition and degradation of plant cell wall polysaccharides by two human gut symbionts, PLoS Biol., 9, e1001221.PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Martens, E. C., Chiang, H. C., and Gordon, J. I. (2008) Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont, Cell Host Microbe, 4, 447–457.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Allen, C. A., and Torres, A. G. (2008) in GIMicrobiota and Regulation of the Immune System. Advances in Experimental Medicine and Biology (Huffnagle, G. B., and Noverr, M. C., eds.) Vol. 635, Springer, New York, pp. 93–101.CrossRefGoogle Scholar
  29. 29.
    Mahowald, M. 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., and Gordon, J. I. (2009) Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla, Proc. Natl. Acad. Sci. USA, 106, 5859–5864.PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Vallender, E. J., and Lahn, B. T. (2004) Positive selection on the human genome, Hum. Mol. Genet., 13 (Suppl. 2), R245–R254.PubMedCrossRefGoogle Scholar
  31. 31.
    Hoskins, L. C. (1969) Ecological studies of intestinal bacteria. Relation between the specificity of fecal ABO blood group antigen-degrading enzymes from enteric bacteria and the ABO blood group of the human host, J. Clin. Invest., 48, 664–673.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Hoskins, L. C. (1968) Bacterial degradation of gastrointestinal mucins. II. Bacterial origin of fecal ABH(O) blood group antigen-destroying enzymes, Gastroenterology, 54, 218–224.PubMedGoogle Scholar
  33. 33.
    Harduin-Lepers, A., Vallejo-Ruiz, V., Krzewinski-Recchi, M. A., Samyn-Petit, B., Julien, S., and Delannoy, P. (2001) The human sialyltransferase family, Biochimie, 83, 727–737.PubMedCrossRefGoogle Scholar
  34. 34.
    Harduin-Lepers, A., Mollicone, R., Delannoy, P., and Oriol, R. (2005) The animal sialyltransferases and sialyltransferase-related genes: a phylogenetic approach, Glycobiology, 15, 805–817.PubMedCrossRefGoogle Scholar
  35. 35.
    Li, Y., and Chen, X. (2012) Sialic acid metabolism and sialyltransferases: natural functions and applications, Appl. Microbiol. Biotechnol., 94, 887–905.PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Severi, E., Hood, D. W., and Thomas, G. H. (2007) Sialic acid utilization by bacterial pathogens, Microbiology, 153, 2817–2822.PubMedCrossRefGoogle Scholar
  37. 37.
    Vimr, E. R., Kalivoda, K. A., Deszo, E. L., and Steenbergen, S. M. (2004) Diversity of microbial sialic acid metabolism, Microbiol. Mol. Biol. Rev., 68, 132–153.PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Almagro-Moreno, S., and Boyd, E. F. (2009) Insights into the evolution of sialic acid catabolism among bacteria, BMC Evol. Biol., 9, 118.PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Vimr, E. R. (2013) Unified theory of bacterial sialometabolism: how and why bacteria metabolize host sialic acids, ISRN Microbiol., 2013, 816713–816739.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Chokhawala, H. A., Yu, H., and Chen, X. (2007) Highthroughput substrate specificity studies of sialidases by using chemoenzymatically synthesized sialoside libraries, Chembiochem, 8, 194–201.PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Moncla, B. J., Braham, P., and Hillier, S. L. (1990) Sialidase (neuraminidase) activity among Gram-negative anaerobic and capnophilic bacteria, J. Clin. Microbiol., 28, 422–425.PubMedPubMedCentralGoogle Scholar
  42. 42.
    Sela, D. A., Li, Y., Lerno, L., Wu, S., Marcobal, A. M., German, J. B., Chen, X., Lebrilla, C. B., and Mills, D. A. (2011) An infant-associated bacterial commensal utilizes breast milk sialyloligosaccharides, J. Biol. Chem., 286, 11909–11918.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Egan, M., Motherway, M. O. C., Ventura, M., and Van Sinderen, D. (2014) Metabolism of sialic acid by Bifidobacterium breve UCC2003, Appl. Environ. Microbiol., 80, 4414–4426.PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Anba-Mondoloni, J., Chaillou, S., Zagorec, M., and Champomier-Verges, M. C. (2013) Catabolism of Nacetylneuraminic acid, a fitness function of the food-borne lactic acid bacterium Lactobacillus sakei, involves two newly characterized proteins, Appl. Environ. Microbiol., 79, 2012–2018.PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Egan, M., Motherway, M. O. C., Kilcoyne, M., Kane, M., Joshi, L., Ventura, M., and Van Sinderen, D. (2014) Crossfeeding by Bifidobacterium breve UCC2003 during co-cultivation with Bifidobacterium bifidum PRL2010 in a mucinbased medium, BMC Microbiol., 14, 282.PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Kampmann, C., Dicksved, J., Engstrand, L., and Rautelin, H. (2016) Composition of human fecal microbiota in resistance to Campylobacter infection, Clin. Microbiol. Infect., 22, 61.e1-61.e8.Google Scholar
  47. 47.
    Ma, B., Simala-Grant, J. L., and Taylor, D. E. (2006) Fucosylation in prokaryotes and eukaryotes, Glycobiology, 16, 158R–184R.PubMedCrossRefGoogle Scholar
  48. 48.
    Oriol, R., Mollicone, R., Cailleau, A., Balanzino, L., and Breton, C. (1999) Divergent evolution of fucosyltransferase genes from vertebrates, invertebrates, and bacteria, Glycobiology, 9, 323–334.PubMedCrossRefGoogle Scholar
  49. 49.
    Juliant, S., Harduin-Lepers, A., Monjaret, F., Catieau, B., Violet, M. L., Cerutti, P., Ozil, A., and Duonor-Cerutti, M. (2014) The α1, 6-fucosyltransferase gene (fut8) from the Sf 9 lepidopteran insect cell line: insights into fut8 evolution, PLoS One, 9, e110422.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Javaud, C., Dupuy, F., Maftah, A., Julien, R., and Petit, J. M. (2003) in Origin and Evolution of New Gene Functions (Long, M., ed.) Vol. 10, Springer, Netherlands, pp. 157–170.CrossRefGoogle Scholar
  51. 51.
    Bakker, H., Schijlen, E., De Vries, T., Schiphorst, W. E., Jordi, W., Lommen, A., Bocsh, D., and Van Die, I. (2001) Plant members of the α1→3/4-fucosyltransferase gene family encode an α1→4-fucosyltransferase, potentially involved in Lewisa biosynthesis, and two core α1→3-fucosyltransferases, FEBS Lett., 507, 307–312.PubMedCrossRefGoogle Scholar
  52. 52.
    Leonard, R., Costa, G., Darrambide, E., Lhernould, S., Fleurat-Lessard, P., Carlue, M., Gomord, V., Faye, L., and Maftah, A. (2002) The presence of Lewisa epitopes in Arabidopsis thaliana glycoconjugates depends on an active α4-fucosyltransferase gene, Glycobiology, 12, 299–306.PubMedCrossRefGoogle Scholar
  53. 53.
    Palma, A. S., Vila-Verde, C., Pires, A. S., Fevereiro, P. S., and Costa, J. (2001) A novel plant α4-fucosyltransferase (Vaccinium myrtillus L.) synthesizes the Lewisa adhesion determinant, FEBS Lett., 499, 235–238.PubMedCrossRefGoogle Scholar
  54. 54.
    Caffall, K. H., and Mohnen, D. (2009) The structure, function, and biosynthesis of plant cell wall pectic polysaccharides, Carbohydr. Res., 344, 1879–1900.PubMedCrossRefGoogle Scholar
  55. 55.
    Glushka, J. N., Terrell, M., York, W. S., O’Neill, M. A., Gucwa, A., Darvill, A. G., Albersheim, P., and Prestegard, J. H. (2003) Primary structure of the 2-O-methyl-α-Lfucose-containing side chain of the pectic polysaccharide, rhamnogalacturonan II, Carbohydr. Res., 338, 341–352.PubMedCrossRefGoogle Scholar
  56. 56.
    Reiter, W. D. (2002) Biosynthesis and properties of the plant cell wall, Curr. Opin. Plant Biol., 5, 536–542.PubMedCrossRefGoogle Scholar
  57. 57.
    Perez, S., Rodriguez-Carvajal, M. A., and Doco, T. (2003) A complex plant cell wall polysaccharide: rhamnogalacturonan II. A structure in quest of a function, Biochimie, 85, 109–121.PubMedCrossRefGoogle Scholar
  58. 58.
    Fitchette-Laine, A. C., Gomord, V., Cabanes, M., Michalski, J. C., Saint-Macary, M., Foucher, B., Cavelier, B., Hawes, C., Lerouge, P., and Faye, L. (1997) N-glycans harboring the Lewisa epitope are expressed at the surface of plant cells, Plant J., 12, 1411–1417.PubMedCrossRefGoogle Scholar
  59. 59.
    Pena, M. J., Vergara, C. E., and Carpita, N. C. (2008) in Advanced Dietary Fibre Technology (McCleary, B., and Prosky, L., eds.) John Wiley & Sons, N. Y., pp. 42–60.Google Scholar
  60. 60.
    Sarkar, P., Bosneaga, E., and Auer, M. (2009) Plant cell walls throughout evolution: towards a molecular understanding of their design principles, J. Exp. Bot., 60, 36153635.CrossRefGoogle Scholar
  61. 61.
    Nguema-Ona, E., Vicre-Gibouin, M., Gotte, M., Plancot, B., Lerouge, P., Bardor, M., and Driouich, A. (2014) Cell wall O-glycoproteins and N-glycoproteins: aspects of biosynthesis and function, Front. Plant Sci., 5, 8.CrossRefGoogle Scholar
  62. 62.
    Moran, A. P., and Prendergast, M. M. (2001) Molecular mimicry in Campylobacter jejuni and Helicobacter pylori lipopolysaccharides: contribution of gastrointestinal infections to autoimmunity, J. Autoimmun., 16, 241–256.PubMedCrossRefGoogle Scholar
  63. 63.
    Whitfield, C., and Roberts, I. S. (1999) Structure, assembly and regulation of expression of capsules in Escherichia coli, Mol. Microbiol., 31, 1307–1319.PubMedCrossRefGoogle Scholar
  64. 64.
    Barua, S., Yamashino, T., Hasegawa, T., Yokoyama, K., Torii, K., and Ohta, M. (2002) Involvement of surface polysaccharides in the organic acid resistance of Shiga toxin-producing Escherichia coli O157:H7, Mol. Microbiol., 43, 629–640.PubMedCrossRefGoogle Scholar
  65. 65.
    Skurnik, M., and Zhang, L. (1996) Molecular genetics and biochemistry of Yersinia lipopolysaccharide, APMIS, 104, 849–872.PubMedCrossRefGoogle Scholar
  66. 66.
    Becker, D. J., and Lowe, J. B. (2003) Fucose: biosynthesis and biological function in mammals, Glycobiology, 13, 41R–53R.PubMedCrossRefGoogle Scholar
  67. 67.
    Mollicone, R., Cailleau, A., and Oriol, R. (1995) Molecular genetics of Yersinia and other fucosyltransferase genes, Transfus. Clin. Biol., 2, 235–242.PubMedCrossRefGoogle Scholar
  68. 68.
    Gagneux, P., and Varki, A. (1999) Evolutionary considerations in relating oligosaccharide diversity to biological function, Glycobiology, 9, 747–755.PubMedCrossRefGoogle Scholar
  69. 69.
    Marionneau, S., Cailleau-Thomas, A., Rocher, J., Le Moullac-Vaidye, B., Ruvoen, N., Clement, M., and Le Pendu, J. (2001) ABH and Lewis histo-blood group antigens, a model for the meaning of oligosaccharide diversity in the face of a changing world, Biochimie, 83, 565–573.PubMedCrossRefGoogle Scholar
  70. 70.
    Audfray, A., Varrot, A., and Imberty, A. (2013) Bacteria love our sugars: interaction between soluble lectins and human fucosylated glycans, structures, thermodynamics and design of competing glycocompounds, Comptes Rendus Chimie, 16, 482–490.CrossRefGoogle Scholar
  71. 71.
    McGovern, D. P., Jones, M. R., Taylor, K. D., Marciante, K., Yan, X., Dubinsky, M., Ippoliti, A., Vasiliauskas, E., Berel, D., Derkowski, C., Dutridge, D., Fleshner, P., Shih, D. Q., Melmed, G., Mengesha, E., King, L., Pressman, S., Haritunians, T., Guo, X., Targan, S. R., and Rotter, J. I.; International IBD Genetics Consortium (2010) Fucosyltransferase 2 (FUT2) non-secretor status is associated with Crohn’s disease, Hum. Mol. Genet., 19, 34683476.CrossRefGoogle Scholar
  72. 72.
    Smyth, D. J., Cooper, J. D., Howson, J. M., Clarke, P., Downes, K., Mistry, T., Stevens, H., Walker, N. M., and Todd, J. A. (2011) FUT2 nonsecretor status links type Yersinia diabetes susceptibility and resistance to infection, Diabetes, 60, 3081–3084.PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Parmar, A. S., Alakulppi, N., Paavola-Sakki, P., Kurppa, K., Halme, L., Farkkila, M., Turunen, U., Lappalainen, M., Kontula, K., Kaukinen, K., Maki, M., Lindfors, K., Partanen, J., Sistonen, P., Matto, J., Wacklin, P., Saavalainen, P., and Maki, M. (2012) Association study of FUT2 (rs601338) with celiac disease and inflammatory bowel disease in the Finnish population, Tissue Antigens, 80, 488–493.PubMedCrossRefGoogle Scholar
  74. 74.
    Eden, J., and Leffler, H. (1980) Glycosphingolipids of human urinary tract epithelial cells as possible receptors for adhering Escherichia coli bacteria, Scand. J. Infect. Dis. Suppl., 24, 144–149.PubMedGoogle Scholar
  75. 75.
    Stapleton, A., Nudelman, E., Clausen, H., Hakomori, S., and Stamm, W. E. (1992) Binding of uropathogenic Escherichia coli R45 to glycolipids extracted from vaginal epithelial cells is dependent on histo-blood group secretor status, J. Clin. Invest., 90, 965–972.PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Biondi, C., Cotorruelo, C., Balague, C., Toresani, I., Racca, L., Di Monaco, R. D., Fernandez, L., and Racca, A. (1999) Association of the “secretor state” with the presence and recurrence of urinary infections in pregnant women, Ann. Clin. Biochem., 36, 391–392.PubMedCrossRefGoogle Scholar
  77. 77.
    Anstee, D. J. (2010) The relationship between blood groups and disease, Blood, 115, 4635–4643.PubMedCrossRefGoogle Scholar
  78. 78.
    Ferrer-Admetlla, A., Sikora, M., Laayouni, H., Esteve, A., Roubinet, F., Blancher, A., Calafell, F., Bertranpetit, J., and Casals, F. (2009) A natural history of FUT2 polymorphism in humans, Mol. Biol. Evol., 26, 1993–2003.PubMedCrossRefGoogle Scholar
  79. 79.
    Lee, Y. K. (2013) Effects of diet on gut microbiota profile and the implications for health and disease, Biosci. Microbiota Food Health, 32, 1–12.PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Terrapon, N., and Henrissat, B. (2014) How do gut microbes break down dietary fiber? Trends Biochem. Sci., 39, 156–158.PubMedCrossRefGoogle Scholar
  81. 81.
    Gill, S. R., Pop, M., DeBoy, R. T., Eckburg, P. B., Turnbaugh, P. J., Samuel, B. S., Gordon, J. I., Relman, D. A., Fraser-Liggett, C. M., and Nelson, K. E. (2006) Metagenomic analysis of the human distal gut microbiome, Science, 312, 1355–1359.PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Koropatkin, N. M., Cameron, E. A., and Martens, E. C. (2012) How glycan metabolism shapes the human gut microbiota, Nat. Rev. Microbiol., 10, 323–335.PubMedPubMedCentralGoogle Scholar
  83. 83.
    Xu, J., Bjursell, M. K., Himrod, J., Deng, S., Carmichael, L. K., Chiang, H. C., Hooper, L. V., and Gordon, J. I. (2003) A genomic view of the human–Bacteroides thetaiotaomicron symbiosis, Science, 299, 2074–2076.PubMedCrossRefGoogle Scholar
  84. 84.
    Turroni, F., Ribbera, A., Foroni, E., Van Sinderen, D., and Ventura, M. (2008) Human gut microbiota and bifidobacteria: from composition to functionality, Antonie Van Leeuwenhoek, 94, 35–50.PubMedCrossRefGoogle Scholar
  85. 85.
    Turroni, F., Duranti, S., Bottacini, F., Guglielmetti, S., Van Sinderen, D., and Ventura, M. (2014) Bifidobacterium bifidum as an example of a specialized human gut commensal, Front. Microbiol., 5, 437.PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Ventura, M., Turroni, F., Motherway, M. O. C., MacSharry, J., and Van Sinderen, D. (2012) Host–microbe interactions that facilitate gut colonization by commensal bifidobacteria, Trends Microbiol., 20, 467–476.PubMedCrossRefGoogle Scholar
  87. 87.
    Ventura, M., Canchaya, C., Tauch, A., Chandra, G., Fitzgerald, G. F., Chater, K. F., and Van Sinderen, D. (2007) Genomics of Actinobacteria: tracing the evolutionary history of an ancient phylum, Microbiol. Mol. Biol. Rev., 71, 495–548.PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Crost, E. H., Tailford, L. E., Le Gall, G., Fons, M., Henrissat, B., and Juge, N. (2013) Utilization of mucin glycans by the human gut symbiont Ruminococcus gnavus is strain-dependent, PLoS One, 8, e76341.PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Turroni, F., Foroni, E., Serafini, F., Viappiani, A., Montanini, B., Bottacini, F., Ferrarini, A., Bacchini, P. L., Rota, C., Delledonne, M., Ottonello, S., Van Sinderen, D., and Ventura, M. (2011) The ability of Bifidobacterium breve to grow on different milk types: exploring milk metabolism through genome analysis, Appl. Environ. Microbiol., 77, 7408–7417.PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Newburg, D. S. (2013) Glycobiology of human milk, Biochemistry (Moscow), 78, 771–785.CrossRefGoogle Scholar
  91. 91.
    Coppa, G. V., Pierani, P., Zampini, L., Carloni, I., Carlucci, A., and Gabrielli, O. (1999) Oligosaccharides in human milk during different phases of lactation, Acta Pediatr. Suppl., 88, 89–94.CrossRefGoogle Scholar
  92. 92.
    Tao, N., Wu, S., Kim, J., An, H. J., Hinde, K., Power, M. L., Gagneux, P., German, J. B., and Lebrilla, C. B. (2011) Evolutionary glycomics: characterization of milk oligosaccharides in primates, J. Proteome Res., 10, 1548–1557.PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Albrecht, S., Lane, J. A., Marino, K., Al Busadah, K. A., Carrington, S. D., Hickey, R. M., and Rudd, P. M. (2014) A comparative study of free oligosaccharides in the milk of domestic animals, Br. J. Nutr., 111, 1313–1328.PubMedCrossRefGoogle Scholar
  94. 94.
    Wiederschain, G. Y., and Newburg, D. S. (1996) Compartmentalization of fucosyltransferase and α-Lfucosidase in human milk, Biochem. Mol. Med., 58, 211–220.PubMedCrossRefGoogle Scholar
  95. 95.
    Thurl, S., Henker, J., Siegel, M., Tovar, K., and Sawatzki, G. (1997) Detection of four human milk groups with respect to Lewis blood group dependent oligosaccharides, Glycoconj. J., 14, 795–799.PubMedCrossRefGoogle Scholar
  96. 96.
    Newburg, D. S., Ruiz-Palacios, G. M., Altaye, M., Chaturvedi, P., Meinzen-Derr, J., De Lourdes Guerrero, M., and Morrow, A. L. (2004) Innate protection conferred by fucosylated oligosaccharides of human milk against diarrhea in breastfed infants, Glycobiology, 14, 253–263.PubMedCrossRefGoogle Scholar
  97. 97.
    German, J., Freeman, S., Lebrilla, C., and Mills, D. (2008) in Personalized Nutrition for the Diverse Needs of Infants and Children. Nestle Nutr. Workshop Ser. Pediatr. Program (Bier, D. M., German, J. B., and Lonnerdal, B., eds.) Vol. 62, Karger Publishers, Basel, pp. 205–222.CrossRefGoogle Scholar
  98. 98.
    Chaturvedi, P., Warren, C. D., Altaye, M., Morrow, A. L., Ruiz-Palacios, G., Pickering, L. K., and Newburg, D. S. (2001) Fucosylated human milk oligosaccharides vary between individuals and over the course of lactation, Glycobiology, 11, 365–372.PubMedCrossRefGoogle Scholar
  99. 99.
    Biol-N’garagba, M. C., and Louisot, P. (2003) Regulation of the intestinal glycoprotein glycosylation during postnatal development: role of hormonal and nutritional factors, Biochimie, 85, 331–352.PubMedCrossRefGoogle Scholar
  100. 100.
    Newburg, D. S., and Morelli, L. (2015) Human milk and infant intestinal mucosal glycans guide succession of the neonatal intestinal microbiota, Pediatr. Res., 77, 115–120.PubMedCrossRefGoogle Scholar
  101. 101.
    Thurl, S., Munzert, M., Henker, J., Boehm, G., MullerWerner, B., Jelinek, J., and Stahl, B. (2010) Variation of human milk oligosaccharides in relation to milk groups and lactational periods, Br. J. Nutr., 104, 1261–1271.PubMedCrossRefGoogle Scholar
  102. 102.
    Garrido, D., Barile, D., and Mills, D. A. (2012) A molecular basis for bifidobacterial enrichment in the infant gastrointestinal tract, Adv. Nutr., 3, 415S–421S.PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Yu, Z. T., Chen, C., and Newburg, D. S. (2013) Utilization of major fucosylated and sialylated human milk oligosaccharides by isolated human gut microbes, Glycobiology, 23, 1281–1292.PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Lewis, Z. T., Totten, S. M., Smilowitz, J. T., Popovic, M., Parker, E., Lemay, D. G., Van Tassell, M. L., Miller, M. J., Jin, Y. S., German, J. B., Lebrilla, C. B., and Mills, D. A. (2015) Maternal fucosyltransferase 2 status affects the gut bifidobacterial communities of breastfed infants, Microbiome, 3, 13.PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Marcobal, A., Barboza, M., Froehlich, J. W., Block, D. E., German, J. B., Lebrilla, C. B., and Mills, D. A. (2010) Consumption of human milk oligosaccharides by gutrelated microbes, J. Agric. Food Chem., 58, 5334–5340.PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Marcobal, A., Barboza, M., Sonnenburg, E. D., Pudlo, N., Martens, E. C., Desai, P., Lebrilla, C. B., Weimer, B. C., Mills, D. A., German, J. B., and Sonnenburg, J. L. (2011) Bacteroides in the infant gut consume milk oligosaccharides via mucus-utilization pathways, Cell Host Microbe, 10, 507–514.PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Newburg, D. S., Ruiz-Palacios, G. M., and Morrow, A. L. (2005) Human milk glycans protect infants against enteric pathogens, Annu. Rev. Nutr., 25, 37–58.PubMedCrossRefGoogle Scholar
  108. 108.
    Pieters, R. J. (2011) Carbohydrate mediated bacterial adhesion, Adv. Exp. Med. Biol., 715, 227–240.PubMedCrossRefGoogle Scholar
  109. 109.
    Bienenstock, J., Buck, R. H., Linke, H., Forsythe, P., Stanisz, A. M., and Kunze, W. A. (2013) Fucosylated but not sialylated milk oligosaccharides diminish colon motor contractions, PLoS One, 8, e76236.PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Johansson, M. E., Sjovall, H., and Hansson, G. C. (2013) The gastrointestinal mucus system in health and disease, Nat. Rev. Gastroenterol. Hepatol., 10, 352–361.PubMedPubMedCentralCrossRefGoogle Scholar
  111. 111.
    Johansson, M. E. (2014) Mucus layers in inflammatory bowel disease, Inflamm. Bowel Dis., 20, 2124–2131.PubMedCrossRefGoogle Scholar
  112. 112.
    Bergstrom, K. S. B., and Xia, L. (2013) Mucin-type O-glycans and their roles in intestinal homeostasis, Glycobiology, 23, 1026–1037.PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Robbe, C., Capon, C., Coddeville, B., and Michalski, J. C. (2004) Structural diversity and specific distribution of O-glycans in normal human mucins along the intestinal tract, Biochem. J., 384, 307–316.PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Robbe, C., Capon, C., Maes, E., Rousset, M., Zweibaum, A., Zanetta, J. P., and Michalski, J. C. (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.PubMedCrossRefGoogle Scholar
  115. 115.
    Larsson, J. M., Karlsson, H., Sjovall, H., and Hansson, G. C. (2009) A complex, but uniform O-glycosylation of the human MUC2 mucin from colonic biopsies analyzed by nanoLC/MSn, Glycobiology, 19, 756–766.PubMedCrossRefGoogle Scholar
  116. 116.
    Robbe-Masselot, C., Maes, E., Rousset, M., Michalski, J. C., and Capon, C. (2009) Glycosylation of human fetal mucins: a similar repertoire of O-glycans along the intestinal tract, Glycoconj. J., 26, 397–413.PubMedCrossRefGoogle Scholar
  117. 117.
    Bry, L., Falk, P. G., Midtvedt, T., and Gordon, J. I. (1996) A model of host–microbial interactions in an open mammalian ecosystem, Science, 273, 1380–1383.PubMedCrossRefGoogle Scholar
  118. 118.
    Turck, D., Feste, A. S., and Lifschitz, C. H. (1993) Age and diet affect the composition of porcine colonic mucins, Pediatr. Res., 33, 564–567.PubMedCrossRefGoogle Scholar
  119. 119.
    Meng, D., Newburg, D. S., Young, C., Baker, A., Tonkonogy, S. L., Sartor, R. B., Walker, W. A., and Nanthakumar, N. N. (2007) Bacterial symbionts induce a FUT2-dependent fucosylated niche on colonic epithelium via ERK and JNK signaling, Am. J. Physiol. Gastrointest. Liver Physiol., 293, 780–787.CrossRefGoogle Scholar
  120. 120.
    Goto, Y., Obata, T., Kunisawa, J., Sato, S., Ivanov, I. I., Lamichhane, A., Takeyama, N., Kamioka, M., Sakamoto, M., Matsuki, T., Setoyama, H., Imaoka, A., Uematsu, S., Akira, S., Domino, S. E., Kulig, P., Becher, B., Renauld, J. C., Sasakawa, C., Umesaki, Y., Benno, Y., and Kiyono, H. (2014) Innate lymphoid cells regulate intestinal epithelial cell glycosylation, Science, 345, 1254009.PubMedPubMedCentralCrossRefGoogle Scholar
  121. 121.
    Kumar, H., Wacklin, P., Nakphaichit, M., Loyttyniemi, E., Chowdhury, S., Shouche, Y., Matto, J., Isolauri, E., and Salminen, S. (2015) Secretor status is strongly associated with microbial alterations observed during pregnancy, PLoS One, 10, e0134623.PubMedPubMedCentralCrossRefGoogle Scholar
  122. 122.
    Wacklin, P., Makivuokko, H., Alakulppi, N., Nikkila, J., Tenkanen, H., Rabina, J., Partanen, J., Aranko, K., and Matto, J. (2011) Secretor genotype (FUT2 gene) is strongly associated with the composition of Bifidobacteria in the human intestine, PLoS One, 6, e20113.PubMedPubMedCentralCrossRefGoogle Scholar
  123. 123.
    Wacklin, P., Tuimala, J., Nikkila, J., Tims, S., Makivuokko, H., Alakulppi, N., Laine, P., RajilicStojanovic, M., Paulin, L., De Vos, W. M., and Matto, J. (2014) Faecal microbiota composition in adults is associated with the FUT2 gene determining the secretor status, PLoS One, 9, e94863.PubMedPubMedCentralCrossRefGoogle Scholar
  124. 124.
    Romero, R., Hassan, S. S., Gajer, P., Tarca, A. L., Fadrosh, D. W., Nikita, L., Galuppi, M., Lamont, R. F., Chaemsaithong, P., Miranda, J., Chaiworapongsa, T., and Ravel, J. (2014) The composition and stability of the vaginal microbiota of normal pregnant women is different from that of non-pregnant women, Microbiome, 2, 4.PubMedPubMedCentralCrossRefGoogle Scholar
  125. 125.
    Aagaard, K., Riehle, K., Ma, J., Segata, N., Mistretta, T. A., Coarfa, C., Raza, S., Rosenbaum, S., Van den Veyver, I., Milosavljevic, A., Gevers, D., Huttenhower, C., Petrosino, J., and Versalovic, J. (2012) A metagenomic approach to characterization of the vaginal microbiome signature in pregnancy, PLoS One, 7, e36466.PubMedPubMedCentralCrossRefGoogle Scholar
  126. 126.
    Mendz, G. L., Lord, S. J., Kaakoush, N. O., HaikalMukhtar, H., and Quinlivan, J. A. (2015) The vaginal microbiome of gravidae in the third trimester: vaginotypes and preterm birth, https://www.researchgate.net/publication/283353077.Google Scholar
  127. 127.
    Milani, C., Mancabelli, L., Lugli, G. A., Duranti, S., Turroni, F., Ferrario, C., Mangifesta, M., Viappiani, A., Ferretti, P., Gorfer, V., Tett, A., Segata, N., Van Sinderen, D., and Ventura, M. (2015) Exploring vertical transmission of bifidobacteria from mother to child, Appl. Environ. Microbiol., 81, 7078–7087.PubMedPubMedCentralCrossRefGoogle Scholar
  128. 128.
    Dominguez-Bello, M. G., Costello, E. K., Contreras, M., Magris, M., Hidalgo, G., Fierer, N., and Knight, R. (2010) Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns, Proc. Natl. Acad. Sci. USA, 107, 11971–11975.PubMedPubMedCentralCrossRefGoogle Scholar
  129. 129.
    Ravel, J., Gajer, P., Abdo, Z., Schneider, G. M., Koenig, S. S., McCulle, S. L., Karlebach, S., Gorle, R., Russell, J., Tacket, C. O., Brotman, R. M., Davis, C. C., Ault, K., Peralta, L., and Forney, L. J. (2011) Vaginal microbiome of reproductive-age women, Proc. Natl. Acad. Sci. USA, 108, 4680–4687.PubMedCrossRefGoogle Scholar
  130. 130.
    Voreades, N., Kozil, A., and Weir, T. L. (2014) Diet and the development of the human intestinal microbiome, Front. Microbiol., 5, 494.PubMedPubMedCentralCrossRefGoogle Scholar
  131. 131.
    Dai, D., and Walker, W. A. (1999) Protective nutrients and bacterial colonization in the immature human gut, Adv. Pediatr., 46, 353–382.PubMedGoogle Scholar
  132. 132.
    Mackie, R. I., Sghir, A., and Gaskins, H. R. (1999) Developmental microbial ecology of the neonatal gastrointestinal tract, Am. J. Clin. Nutr., 69, 1035S–1045S.PubMedGoogle Scholar
  133. 133.
    Turroni, F., Peano, C., Pass, D. A., Foroni, E., Severgnini, M., Claesson, M. J., Kerr, C., Hourihane, J., Murray, D., Fuligni, F., Gueimonde, M., Margolles, A., De Bellis, G., O’Toole, P. W., Van Sinderen, D., Marchesi, J. R., and Ventura, M. (2012) Diversity of bifidobacteria within the infant gut microbiota, PLoS One, 7, e36957.PubMedPubMedCentralCrossRefGoogle Scholar
  134. 134.
    Salyers, A. A., Vercellotti, J. R., West, S. E., and Wilkins, T. D. (1977) Fermentation of mucin and plant polysaccharides by strains of Bacteroides from the human colon, Appl. Environ. Microbiol., 33, 319–322.PubMedPubMedCentralGoogle Scholar
  135. 135.
    Salyers, A. A., West, S. E., Vercellotti, J. R., and Wilkins, T. D. (1977) Fermentation of mucins and plant polysaccharides by anaerobic bacteria from the human colon, Appl. Environ. Microbiol., 34, 529–533.PubMedPubMedCentralGoogle Scholar
  136. 136.
    Turroni, F., Milani, C., Van Sinderen, D., and 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.PubMedCrossRefGoogle Scholar
  137. 137.
    Turroni, F., Serafini, F., Foroni, E., Duranti, S., Motherway, M. O. C., Taverniti, V., Mangifesta, M., Milani, C., Viappiani, A., Roversi, T., Sanchez, B., Santoni, A., Gioiosa, L., Ferrarini, A., Delledonne, M., Margolles, A., Piazza, L., Palanza, P., Bolchi, A., Guglielmetti, S., Van Sinderen, D., and Ventura, M. (2013) Role of sortase-dependent pili of Bifidobacterium bifidum PRL2010 in modulating bacterium–host interactions, Proc. Natl. Acad. Sci. USA, 110, 11151–11156.PubMedPubMedCentralCrossRefGoogle Scholar
  138. 138.
    Mukai, T., Kaneko, S., Matsumoto, M., and Ohori, H. (2004) Binding of Bifidobacterium bifidum and Lactobacillus reuteri to the carbohydrate moieties of intestinal glycolipids recognized by peanut agglutinin, Int. J. Food Microbiol., 90, 357–362.PubMedCrossRefGoogle Scholar
  139. 139.
    Etzold, S., and Juge, N. (2014) Structural insights into bacterial recognition of intestinal mucins, Curr. Opin. Struct. Biol., 28, 23–31.PubMedCrossRefGoogle Scholar
  140. 140.
    Etzold, S., Kober, O. I., MacKenzie, D. A., Tailford, L. E., Gunning, A. P., Walshaw, J., Hemmings, A. M., and Juge, N. (2014) Structural basis for adaptation of lactobacilli to gastrointestinal mucus, Environ. Microbiol., 16, 888–903.PubMedCrossRefGoogle Scholar
  141. 141.
    Coyne, M. J., Reinap, B., Lee, M. M., and Comstock, L. E. (2005) Human symbionts use a host-like pathway for surface fucosylation, Science, 307, 1778–1781.PubMedCrossRefGoogle Scholar
  142. 142.
    Duncan, S. H., Louis, P., and Flint, H. J. (2004) Lactateutilizing bacteria, isolated from human feces, that produce butyrate as a major fermentation product, Appl. Environ. Microbiol., 70, 5810–5817.PubMedPubMedCentralCrossRefGoogle Scholar
  143. 143.
    Turroni, F., Ventura, M., Butto, L. F., Duranti, S., O’Toole, P. W., Motherway, M. O., and Van Sinderen, D. (2014) Molecular dialogue between the human gut microbiota and the host: a Lactobacillus and Bifidobacterium perspective, Cell Mol. Life Sci., 71, 183–203.PubMedCrossRefGoogle Scholar
  144. 144.
    Sonnenburg, J. L., Chen, C. T., and Gordon, J. I. (2006) Genomic and metabolic studies of the impact of probiotics on a model gut symbiont and host, PLoS Biol., 4, e413.PubMedPubMedCentralCrossRefGoogle Scholar
  145. 145.
    Tong, M., McHardy, I., Ruegger, P., Goudarzi, M., Kashyap, P. C., Haritunians, T., Li, X., Graeber, T. G., Schwager, E., Huttenhower, C., Fornace, A. J., Jr., Sonnenburg, J. L., McGovern, D. P., Borneman, J., and Braun, J. (2014) Reprograming of gut microbiome energy metabolism by the FUT2 Crohn’s disease risk polymorphism, ISME J., 8, 2193–2206.PubMedPubMedCentralCrossRefGoogle Scholar
  146. 146.
    Biagi, E., Candela, M., Fairweather-Tait, S., Franceschi, C., and Brigidi, P. (2012) Ageing of the human metaorganism: the microbial counterpart, Age, 34, 247–267.PubMedCrossRefGoogle Scholar
  147. 147.
    Sonnenburg, E. D., and Sonnenburg, J. L. (2014) Starving our microbial self: the deleterious consequences of a diet deficient in microbiota-accessible carbohydrates, Cell Metab., 20, 779–786.PubMedPubMedCentralCrossRefGoogle Scholar
  148. 148.
    Kashyap, P. C., Marcobal, A., Ursell, L. K., Smits, S. A., Sonnenburg, E. D., Costello, E. K., Higginbottom, S. K., Domino, S. E., Holmes, S. P., Relman, D. A., Knight, R., Gordon, J. I., and Sonnenburg, J. L. (2013) Genetically dictated change in host mucus carbohydrate landscape exerts a diet-dependent effect on the gut microbiota, Proc. Natl. Acad. Sci. USA, 110, 17059–17064.PubMedPubMedCentralCrossRefGoogle Scholar
  149. 149.
    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., and Lewis, J. D. (2011) Linking long-term dietary patterns with gut microbial enterotypes, Science, 334, 105–108.PubMedPubMedCentralCrossRefGoogle Scholar
  150. 150.
    Yatsunenko, T., Rey, F. E., Manary, M. J., Trehan, I., Dominguez-Bello, M. G., Contreras, M., Magris, M., Hidalgo, G., Baldassano, R. N., Anokhin, A. P., Heath, A. C., Warner, B., Reeder, J., Kuczynski, J., Caporaso, J. G., Lozupone, C. A., Lauber, C., Clemente, J. C., Knights, D., Knight, R., and Gordon, J. I. (2012) Human gut microbiome viewed across age and geography, Nature, 486, 222–227.PubMedPubMedCentralGoogle Scholar
  151. 151.
    Lynch, J. B., and Sonnenburg, J. L. (2012) Prioritization of a plant polysaccharide over a mucus carbohydrate is enforced by a Bacteroides hybrid two-component system, Mol. Microbiol., 85, 478–491.PubMedPubMedCentralCrossRefGoogle Scholar
  152. 152.
    Sonnenburg, E. D., Zheng, H., Joglekar, P., Higginbottom, S. K., Firbank, S. J., Bolam, D. N., and Sonnenburg, J. L. (2010) Specificity of polysaccharide use in intestinal Bacteroides species determines diet-induced microbiota alterations, Cell, 141, 1241–1252.PubMedPubMedCentralCrossRefGoogle Scholar

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© Pleiades Publishing, Ltd. 2017

Authors and Affiliations

  1. 1.Institute of Protein ResearchRussian Academy of SciencesPushchino, Moscow RegionRussia

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