Advertisement

Prebiotics: tools to manipulate the gut microbiome and metabolome

  • Fatima Enam
  • Thomas J. MansellEmail author
Food Biotechnology & Probiotics - Review

Abstract

The human gut is an ecosystem comprising trillions of microbes interacting with the host. The composition of the microbiota and their interactions play roles in different biological processes and in the development of human diseases. Close relationships between dietary modifications, microbiota composition and health status have been established. This review focuses on prebiotics, or compounds which selectively encourage the growth of beneficial bacteria, their mechanisms of action and benefits to human hosts. We also review advances in synthesis technology for human milk oligosaccharides, part of one of the most well-characterized prebiotic–probiotic relationships. Current and future research in this area points to greater use of prebiotics as tools to manipulate the microbial and metabolic diversity of the gut for the benefit of human health.

Keywords

Prebiotics Human milk oligosaccharides Gut microbiome 

Abbreviations

DP

Degree of polymerization

HMO

Human milk oligosaccharide

FOS

Fructooligosaccharide

GOS

Galactooligosaccharides

MOS

Mannan-oligosaccharides

SCFA

Short-chain fatty acid

XOS

Xylooligosaccharides

Notes

Acknowledgements

This work was supported by the Iowa State University Startup Funds. F.E. was supported in part by the Manley Hoppe Professorship and T.J.M. by the Karen and Denny Vaughn Faculty Fellowship.

References

  1. 1.
    Aachary AA, Prapulla SG (2011) Xylooligosaccharides (XOS) as an emerging prebiotic: microbial synthesis, utilization, structural characterization, bioactive properties, and applications. Compr Rev Food Sci Food Saf 10:2–16CrossRefGoogle Scholar
  2. 2.
    Akramiene D, Kondrotas A, Didziapetriene J, Kevelaitis E (2007) Effects of beta-glucans on the immune system. Medicina 43:597–606CrossRefPubMedGoogle Scholar
  3. 3.
    Andreas NJ, Kampmann B, Mehring Le-Doare K (2015) Human breast milk: a review on its composition and bioactivity. Early Hum Dev 91:629–635CrossRefPubMedGoogle Scholar
  4. 4.
    Arora T, Sharma R, Frost G (2011) Propionate. Anti-obesity and satiety enhancing factor? Appetite 56:511–515CrossRefPubMedGoogle Scholar
  5. 5.
    Bäckhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI (2005) Host-bacterial mutualism in the human intestine. Science 307:1915–1920CrossRefPubMedGoogle Scholar
  6. 6.
    Baumgärtner F, Seitz L, Sprenger GA, Albermann C (2013) Construction of Escherichia coli strains with chromosomally integrated expression cassettes for the synthesis of 2′-fucosyllactose. Microb Cell Fact 12:1–13CrossRefGoogle Scholar
  7. 7.
    Belenguer A, Duncan SH, Calder AG, Holtrop G, Louis P, Lobley GE, Flint HJ (2006) Two routes of metabolic cross-feeding between Bifidobacterium adolescentis and butyrate-producing anaerobes from the human gut. Appl Environ Microbiol 72:3593–3599CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Ben X-M, Zhou X-Y, Zhao W-H, Yu W-L, Pan W, Zhang W-L, Wu S-M, Van Beusekom CM, Schaafsma A (2004) Supplementation of milk formula with galacto-oligosaccharides improves intestinal micro-flora and fermentation in term infants. Chin Med J 117:927–931PubMedGoogle Scholar
  9. 9.
    Bindels LB, Delzenne NM, Cani PD, Walter J (2015) Towards a more comprehensive concept for prebiotics. Nat Rev Gastroenterol Hepatol 12:303–310CrossRefPubMedGoogle Scholar
  10. 10.
    Bindels LB, Dewulf EM, Delzenne NM (2013) GPR43/FFA2: physiopathological relevance and therapeutic prospects. Trends Pharmacol Sci 34:226–232CrossRefPubMedGoogle Scholar
  11. 11.
    Birt DF, Boylston T, Hendrich S, Jane J-L, Hollis J, Li L, McClelland J, Moore S, Phillips GJ, Rowling M, Schalinske K, Scott MP, Whitley EM (2013) Resistant starch: promise for improving human health. Adv Nutr 4:587–601CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Bode L (2012) Human milk oligosaccharides: every baby needs a sugar mama. Glycobiology 22:1147–1162CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Bode L, Contractor N, Barile D, Pohl N, Prudden AR, Boons G-J, Jin Y-S, Jennewein S (2016) Overcoming the limited availability of human milk oligosaccharides: challenges and opportunities for research and application. Nutr Rev 74:635–644CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Bokulich NA, Chung J, Battaglia T, Henderson N, Jay M, Li H, Lieber AD, Wu F, Perez-Perez GI, Chen Y, Schweizer W, Zheng X, Contreras M, Dominguez-Bello MG, Blaser MJ (2016) Antibiotics, birth mode, and diet shape microbiome maturation during early life. Sci Transl Med 8:343ra82CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM, Dinan TG, Bienenstock J, Cryan JF (2011) Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci USA 108:16050–16055CrossRefPubMedGoogle Scholar
  16. 16.
    Brown GD (2006) Dectin-1: a signalling non-TLR pattern-recognition receptor. Nat Rev Immunol 6:33–43CrossRefPubMedGoogle Scholar
  17. 17.
    Brown GD, Gordon S (2001) Immune recognition. A new receptor for beta-glucans. Nature 413:36–37CrossRefPubMedGoogle Scholar
  18. 18.
    Burokas A, Arboleya S, Moloney RD, Peterson VL, Murphy K, Clarke G, Stanton C, Dinan TG, Cryan JF (2017) Targeting the microbiota-gut-brain axis: prebiotics have anxiolytic and antidepressant-like effects and reverse the impact of chronic stress in mice. Biol Psychiatry 82:472–487CrossRefPubMedGoogle Scholar
  19. 19.
    Byndloss MX, Olsan EE, Rivera-Chávez F, Tiffany CR, Cevallos SA, Lokken KL, Torres TP, Byndloss AJ, Faber F, Gao Y, Litvak Y, Lopez CA, Xu G, Napoli E, Giulivi C, Tsolis RM, Revzin A, Lebrilla CB, Bäumler AJ (2017) Microbiota-activated PPAR-γ signaling inhibits dysbiotic Enterobacteriaceae expansion. Science 357:570–575CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Cani PD (2017) Gut cell metabolism shapes the microbiome. Science 357:548–549CrossRefPubMedGoogle Scholar
  21. 21.
    Cani PD (2018) Human gut microbiome: hopes, threats and promises. Gut 67:1716–1725CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Chang HN, Lee SY, Nielsen J, Stephanopoulos G (2018) Emerging areas in bioengineering. Wiley, ChichesterCrossRefGoogle Scholar
  23. 23.
    Charbonneau MR, Blanton LV, DiGiulio DB, Relman DA, Lebrilla CB, Mills DA, Gordon JI (2016) A microbial perspective of human developmental biology. Nature 535:48–55CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Chaturvedi P, Warren CD, Altaye M, Morrow AL, Ruiz-Palacios G, Pickering LK, Newburg DS (2001) Fucosylated human milk oligosaccharides vary between individuals and over the course of lactation. Glycobiology 11:365–372CrossRefPubMedGoogle Scholar
  25. 25.
    Chen C, Zhang Y, Xue M, Liu X-W, Li Y, Chen X, Wang PG, Wang F, Cao H (2015) Sequential one-pot multienzyme (OPME) synthesis of lacto-N-neotetraose and its sialyl and fucosyl derivatives. Chem Commun 51:7689–7692CrossRefGoogle Scholar
  26. 26.
    Chen R (2018) Enzyme and microbial technology for synthesis of bioactive oligosaccharides: an update. Appl Microbiol Biotechnol 102:3017–3026CrossRefPubMedGoogle Scholar
  27. 27.
    Chichlowski M, De Lartigue G, German JB, Raybould HE, Mills DA (2012) Bifidobacteria isolated from infants and cultured on human milk oligosaccharides affect intestinal epithelial function. J Pediatr Gastroenterol Nutr 55:321–327CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Chunchai T, Thunapong W, Yasom S, Wanchai K, Eaimworawuthikul S, Metzler G, Lungkaphin A, Pongchaidecha A, Sirilun S, Chaiyasut C, Pratchayasakul W, Thiennimitr P, Chattipakorn N, Chattipakorn SC (2018) Decreased microglial activation through gut-brain axis by prebiotics, probiotics, or synbiotics effectively restored cognitive function in obese-insulin resistant rats. J Neuroinflamm 15:11CrossRefGoogle Scholar
  29. 29.
    Chung WSF, Walker AW, Louis P, Parkhill J, Vermeiren J, Bosscher D, Duncan SH, Flint HJ (2016) Modulation of the human gut microbiota by dietary fibres occurs at the species level. BMC Biol 14:3CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Collins MD, Gibson GR (1999) Probiotics, prebiotics, and synbiotics: approaches for modulating the microbial ecology of the gut. Am J Clin Nutr 69:1052S–1057SCrossRefPubMedGoogle Scholar
  31. 31.
    Comstock SS, Li M, Wang M, Monaco MH, Kuhlenschmidt TB, Kuhlenschmidt MS, Donovan SM (2017) Dietary human milk oligosaccharides but not prebiotic oligosaccharides increase circulating natural killer cell and mesenteric lymph node memory t cell populations in noninfected and rotavirus-infected neonatal piglets. J Nutr 147:1041–1047CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Comstock SS, Wang M, Hester SN, Li M, Donovan SM (2014) Select human milk oligosaccharides directly modulate peripheral blood mononuclear cells isolated from 10-d-old pigs. Br J Nutr 111:819–828CrossRefPubMedGoogle Scholar
  33. 33.
    Costabile A, Kolida S, Klinder A, Gietl E, Bäuerlein M, Frohberg C, Landschütze V, Gibson GR (2010) A double-blind, placebo-controlled, cross-over study to establish the bifidogenic effect of a very-long-chain inulin extracted from globe artichoke (Cynara scolymus) in healthy human subjects. Br J Nutr 104:1007–1017CrossRefPubMedGoogle Scholar
  34. 34.
    Crout DH, Vic G (1998) Glycosidases and glycosyl transferases in glycoside and oligosaccharide synthesis. Curr Opin Chem Biol 2:98–111CrossRefPubMedGoogle Scholar
  35. 35.
    David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, Biddinger SB, Dutton RJ, Turnbaugh PJ (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nature 505:559–563CrossRefPubMedGoogle Scholar
  36. 36.
    Dewulf EM, Cani PD, Claus SP, Fuentes S, Puylaert PGB, Neyrinck AM, Bindels LB, de Vos WM, Gibson GR, Thissen J-P, Delzenne NM (2013) Insight into the prebiotic concept: lessons from an exploratory, double blind intervention study with inulin-type fructans in obese women. Gut 62:1112–1121CrossRefPubMedGoogle Scholar
  37. 37.
    Drouillard S, Driguez H, Samain E (2006) Large-scale synthesis of H-antigen oligosaccharides by expressing Helicobacter pylori α1,2-fucosyltransferase in metabolically engineered Escherichia coli cells. Angew Chem Int Ed 45:1778–1780CrossRefGoogle Scholar
  38. 38.
    Durrer KE, Allen MS, Hunt von Herbing I (2017) Genetically engineered probiotic for the treatment of phenylketonuria (PKU); assessment of a novel treatment in vitro and in the PAHenu2 mouse model of PKU. PLoS One 12:e0176286CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    El Kaoutari A, Armougom F, Gordon JI, Raoult D, Henrissat B (2013) The abundance and variety of carbohydrate-active enzymes in the human gut microbiota. Nat Rev Microbiol 11:497–504CrossRefPubMedGoogle Scholar
  40. 40.
    Endo T, Koizumi S, Tabata K, Ozaki A (2000) Large-scale production of CMP-NeuAc and sialylated oligosaccharides through bacterial coupling. Appl Microbiol Biotechnol 53:257–261CrossRefPubMedGoogle Scholar
  41. 41.
    Fair RJ, Hahm HS, Seeberger PH (2015) Combination of automated solid-phase and enzymatic oligosaccharide synthesis provides access to α(2,3)-sialylated glycans. Chem Commun 51:6183–6185CrossRefGoogle Scholar
  42. 42.
    Fanaro S, Marten B, Bagna R, Vigi V, Fabris C, Peña-Quintana L, Argüelles F, Scholz-Ahrens KE, Sawatzki G, Zelenka R, Schrezenmeir J, de Vrese M, Bertino E (2009) Galacto-oligosaccharides are bifidogenic and safe at weaning: a double-blind randomized multicenter study. J Pediatr Gastroenterol Nutr 48:82–88CrossRefPubMedGoogle Scholar
  43. 43.
    Ferenczi S, Szegi K, Winkler Z, Barna T, Kovács KJ (2016) Oligomannan prebiotic attenuates immunological, clinical and behavioral symptoms in mouse model of inflammatory bowel disease. Sci Rep 6:34132CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Fernandes R, do Rosario VA, Mocellin MC, Kuntz MGF, Trindade EBSM (2017) Effects of inulin-type fructans, galacto-oligosaccharides and related synbiotics on inflammatory markers in adult patients with overweight or obesity: a systematic review. Clin Nutr 36:1197–1206CrossRefPubMedGoogle Scholar
  45. 45.
    Ferreira RM, Pereira-Marques J, Pinto-Ribeiro I, Costa JL, Carneiro F, Machado JC, Figueiredo C (2018) Gastric microbial community profiling reveals a dysbiotic cancer-associated microbiota. Gut 67:226–236CrossRefPubMedGoogle Scholar
  46. 46.
    Floch MH (2010) Fecal bacteriotherapy, fecal transplant, and the microbiome. J Clin Gastroenterol 44:529–530CrossRefPubMedGoogle Scholar
  47. 47.
    Foster JA, McVey Neufeld K-A (2013) Gut-brain axis: how the microbiome influences anxiety and depression. Trends Neurosci 36:305–312CrossRefPubMedGoogle Scholar
  48. 48.
    Freeman LR, Haley-Zitlin V, Rosenberger DS, Granholm A-C (2014) Damaging effects of a high-fat diet to the brain and cognition: a review of proposed mechanisms. Nutr Neurosci 17:241–251CrossRefPubMedGoogle Scholar
  49. 49.
    Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, Nakanishi Y, Uetake C, Kato K, Kato T, Takahashi M, Fukuda NN, Murakami S, Miyauchi E, Hino S, Atarashi K, Onawa S, Fujimura Y, Lockett T, Clarke JM, Topping DL, Tomita M, Hori S, Ohara O, Morita T, Koseki H, Kikuchi J, Honda K, Hase K, Ohno H (2013) Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504:446–450CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, Scott K, Stanton C, Swanson KS, Cani PD, Verbeke K, Reid G (2017) Expert consensus document: the International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol 14:491–502CrossRefPubMedGoogle Scholar
  51. 51.
    Gibson GR, Probert HM, Loo JV, Rastall RA, Roberfroid MB (2004) Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutr Res Rev 17:259–275CrossRefPubMedGoogle Scholar
  52. 52.
    Gibson GR, Rastall RA (2006) Prebiotics: development & application. Wiley, ChichesterCrossRefGoogle Scholar
  53. 53.
    Gibson GR, Roberfroid MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125:1401–1412CrossRefPubMedGoogle Scholar
  54. 54.
    Gill SR, Pop M, Deboy RT, Eckburg PB, Turnbaugh PJ, Samuel BS, Gordon JI, Relman DA, Fraser-Liggett CM, Nelson KE (2006) Metagenomic analysis of the human distal gut microbiome. Science 312:1355–1359CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Grulee CG, Sanford HN, Herron PH (1934) Breast and artificial feeding: influence on morbidity and mortality of twenty thousand infants. JAMA 103:735–739CrossRefGoogle Scholar
  56. 56.
    Guo L, Chen X, Xu L, Xiao M, Lu L (2018) Enzymatic synthesis of 6′-sialyllactose, a dominant sialylated human milk oligosaccharide, by a novel exo-α-sialidase from Bacteroides fragilis NCTC9343. Appl Environ Microbiol.  https://doi.org/10.1128/aem.00071-18 CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Gyorgy P, Norris RF, Rose CS (1954) Bifidus factor. I. A variant of Lactobacillus bifidus requiring a special growth factor. Arch Biochem Biophys 48:193–201CrossRefPubMedGoogle Scholar
  58. 58.
    Haberman Y, Tickle TL, Dexheimer PJ, Kim M-O, Tang D, Karns R, Baldassano RN, Noe JD, Rosh J, Markowitz J, Heyman MB, Griffiths AM, Crandall WV, Mack DR, Baker SS, Huttenhower C, Keljo DJ, Hyams JS, Kugathasan S, Walters TD, Aronow B, Xavier RJ, Gevers D, Denson LA (2014) Pediatric Crohn disease patients exhibit specific ileal transcriptome and microbiome signature. J Clin Invest 124:3617–3633CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Hansen CHF, Frøkiær H, Christensen AG, Bergström A, Licht TR, Hansen AK, Metzdorff SB (2013) Dietary xylooligosaccharide downregulates IFN-γ and the low-grade inflammatory cytokine IL-1β systemically in mice. J Nutr 143:533–540CrossRefPubMedGoogle Scholar
  60. 60.
    Hardy H, Harris J, Lyon E, Beal J, Foey AD (2013) Probiotics, prebiotics and immunomodulation of gut mucosal defences: homeostasis and immunopathology. Nutrients 5:1869–1912CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Herrmann GF, Elling L, Krezdorn CH, Kleene R, Berger EG, Wandrey C (1995) Use of transformed whole yeast cells expressing β-1,4-galactosyltransferase for the synthesis of N-acetyllactosamine. Bioorg Med Chem Lett 5:673–676CrossRefGoogle Scholar
  62. 62.
    Herrmann GF, Wang P, Shen G-J, Wong C-H (1994) Recombinant whole cells as catalysts for the enzymatic synthesis of oligosaccharides and glycopeptides. Angew Chem Int Ed Engl 33:1241–1242CrossRefGoogle Scholar
  63. 63.
    Hoentjen F, Welling GW, Harmsen HJM, Zhang X, Snart J, Tannock GW, Lien K, Churchill TA, Lupicki M, Dieleman LA (2005) Reduction of colitis by prebiotics in HLA-B27 transgenic rats is associated with microflora changes and immunomodulation. Inflamm Bowel Dis 11:977–985CrossRefPubMedGoogle Scholar
  64. 64.
    Hosono A, Ozawa A, Kato R, Ohnishi Y, Nakanishi Y, Kimura T, Nakamura R (2003) Dietary fructooligosaccharides induce immunoregulation of intestinal IgA secretion by murine Peyer’s patch cells. Biosci Biotechnol Biochem 67:758–764CrossRefPubMedGoogle Scholar
  65. 65.
    Howard MD, Gordon DT, Garleb KA, Kerley MS (1995) Dietary fructooligosaccharide, xylooligosaccharide and gum arabic have variable effects on cecal and colonic microbiota and epithelial cell proliferation in mice and rats. J Nutr 125:2604–2609PubMedGoogle Scholar
  66. 66.
    Hsu C-K, Liao J-W, Chung Y-C, Hsieh C-P, Chan Y-C (2004) Xylooligosaccharides and fructooligosaccharides affect the intestinal microbiota and precancerous colonic lesion development in rats. J Nutr 134:1523–1528CrossRefPubMedGoogle Scholar
  67. 67.
    Isabella VM, Ha BN, Castillo MJ, Lubkowicz DJ, Rowe SE, Millet YA, Anderson CL, Li N, Fisher AB, West KA, Reeder PJ, Momin MM, Bergeron CG, Guilmain SE, Miller PF, Kurtz CB, Falb D (2018) Development of a synthetic live bacterial therapeutic for the human metabolic disease phenylketonuria. Nat Biotechnol 36:857–864CrossRefPubMedGoogle Scholar
  68. 68.
    Kassam Z, Hundal R, Marshall JK, Lee CH (2012) Fecal transplant via retention enema for refractory or recurrent Clostridium difficile infection. Arch Intern Med 172:191–193CrossRefPubMedGoogle Scholar
  69. 69.
    Bych K, Miks MH, Johanson T, Hederos MJ, Vigsnaes LK, Becker P (2018) Production of HMOs using microbial hosts—from cell engineering to large scale production. Curr Opin Biotechnol 56:130–137CrossRefPubMedGoogle Scholar
  70. 70.
    Kearney SM, Gibbons SM, Erdman SE, Alm EJ (2018) Orthogonal dietary niche enables reversible engraftment of a gut bacterial commensal. Cell Rep 24:1842–1851CrossRefPubMedGoogle Scholar
  71. 71.
    Kim G-B, Seo YM, Kim CH, Paik IK (2011) Effect of dietary prebiotic supplementation on the performance, intestinal microflora, and immune response of broilers. Poult Sci 90:75–82CrossRefPubMedGoogle Scholar
  72. 72.
    King A (2012) Prevention. Cost-effectiveness of cardiovascular disease prevention and management in the developing world. Nat Rev Cardiol 9:258CrossRefPubMedGoogle Scholar
  73. 73.
    Klinder A, Forster A, Caderni G, Femia AP, Pool-Zobel BL (2004) Fecal water genotoxicity is predictive of tumor-preventive activities by inulin-like oligofructoses, probiotics (Lactobacillus rhamnosus and Bifidobacterium lactis), and their synbiotic combination. Nutr Cancer 49:144–155CrossRefPubMedGoogle Scholar
  74. 74.
    Kobayashi T, Okazaki M, Fujikawa S, Koga K (1991) Effect of xylooligosaccharides on feces of men. J Jpn Soc Biosci Biotech Agrochem 65:1651–1653Google Scholar
  75. 75.
    Koeth RA, Wang Z, Levison BS, Buffa JA, Org E, Sheehy BT, Britt EB, Fu X, Wu Y, Li L, Smith JD, DiDonato JA, Chen J, Li H, Wu GD, Lewis JD, Warrier M, Brown JM, Krauss RM, Tang WHW, Bushman FD, Lusis AJ, Hazen SL (2013) Intestinal microbiota metabolism of l-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat Med 19:576–585CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Kontula P, von Wright A, Mattila-Sandholm T (1998) Oat bran β-gluco- and xylo-oligosaccharides as fermentative substrates for lactic acid bacteria. Int J Food Microbiol 45:163–169CrossRefPubMedGoogle Scholar
  77. 77.
    Kostic AD, Xavier RJ, Gevers D (2014) The microbiome in inflammatory bowel disease: current status and the future ahead. Gastroenterology 146:1489–1499CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Kunz C, Rudloff S, Baier W, Klein N, Strobel S (2000) Oligosaccharides in human milk: structural, functional, and metabolic aspects. Annu Rev Nutr 20:699–722CrossRefPubMedGoogle Scholar
  79. 79.
    Kurtz CB, Millet YA, Puurunen MK, Perreault M, Charbonneau MR, Isabella VM, Kotula JW, Antipov E, Dagon Y, Denney WS, Wagner DA, West KA, Degar AJ, Brennan AM, Miller PF (2019) An engineered E. coli Nissle improves hyperammonemia and survival in mice and shows dose-dependent exposure in healthy humans. Sci Transl Med.  https://doi.org/10.1126/scitranslmed.aau7975 CrossRefPubMedGoogle Scholar
  80. 80.
    Kurtz C, Denney WS, Blankstein L, Guilmain SE, Machinani S, Kotula J, Saha S, Miller P, Brennan AM (2018) Translational development of microbiome-based therapeutics: kinetics of E. coli Nissle and engineered strains in humans and nonhuman primates. Clin Transl Sci 11:200–207CrossRefPubMedGoogle Scholar
  81. 81.
    Lee W-H, Pathanibul P, Quarterman J, Jo J-H, Han NS, Miller MJ, Jin Y-S, Seo J-H (2012) Whole cell biosynthesis of a functional oligosaccharide, 2′-fucosyllactose, using engineered Escherichia coli. Microb Cell Fact 11:1–9CrossRefGoogle Scholar
  82. 82.
    Lewandowska U, Szewczyk K, Hrabec E, Janecka A, Gorlach S (2013) Overview of metabolism and bioavailability enhancement of polyphenols. J Agric Food Chem 61:12183–12199CrossRefPubMedGoogle Scholar
  83. 83.
    Lewis S, Burmeister S, Brazier J (2005) Effect of the Prebiotic oligofructose on relapse of Clostridium difficile-associated diarrhea: a randomized, controlled study. Clin Gastroenterol Hepatol 3:442–448CrossRefPubMedGoogle Scholar
  84. 84.
    Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI (2005) Obesity alters gut microbial ecology. Proc Natl Acad Sci USA 102:11070–11075CrossRefPubMedGoogle Scholar
  85. 85.
    Liu RH (2004) Potential synergy of phytochemicals in cancer prevention: mechanism of action. J Nutr 134:3479S–3485SCrossRefPubMedGoogle Scholar
  86. 86.
    Makki K, Deehan EC, Walter J, Bäckhed F (2018) The impact of dietary fiber on gut microbiota in host health and disease. Cell Host Microbe 23:705–715CrossRefPubMedGoogle Scholar
  87. 87.
    Manthey CF, Autran CA, Eckmann L, Bode L (2014) Human milk oligosaccharides protect against enteropathogenic Escherichia coli attachment in vitro and EPEC colonization in suckling mice. J Pediatr Gastroenterol Nutr 58:165–168CrossRefPubMedGoogle Scholar
  88. 88.
    Marcobal A, Barboza M, Sonnenburg ED, Pudlo N, Martens EC, Desai P, Lebrilla CB, Weimer BC, Mills DA, German JB, Sonnenburg JL (2011) Bacteroides in the infant gut consume milk oligosaccharides via mucus-utilization pathways. Cell Host Microbe 10:507–514CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Mariño E, Richards JL, McLeod KH, Stanley D, Yap YA, Knight J, McKenzie C, Kranich J, Oliveira AC, Rossello FJ, Krishnamurthy B, Nefzger CM, Macia L, Thorburn A, Baxter AG, Morahan G, Wong LH, Polo JM, Moore RJ, Lockett TJ, Clarke JM, Topping DL, Harrison LC, Mackay CR (2017) Gut microbial metabolites limit the frequency of autoimmune T cells and protect against type 1 diabetes. Nat Immunol 18:552–562CrossRefPubMedGoogle Scholar
  90. 90.
    Martens EC, Koropatkin NM, Smith TJ, Gordon JI (2009) Complex glycan catabolism by the human gut microbiota: the Bacteroidetes Sus-like paradigm. J Biol Chem 284:24673–24677CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    McNulty NP, Wu M, Erickson AR, Pan C, Erickson BK, Martens EC, Pudlo NA, Muegge BD, Henrissat B, Hettich RL, Gordon JI (2013) 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:e1001637CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Miene C, Weise A, Glei M (2011) Impact of polyphenol metabolites produced by colonic microbiota on expression of COX-2 and GSTT2 in human colon cells (LT97). Nutr Cancer 63:653–662CrossRefPubMedGoogle Scholar
  93. 93.
    Miller TL, Wolin MJ (1996) Pathways of acetate, propionate, and butyrate formation by the human fecal microbial flora. Appl Environ Microbiol 62:1589–1592PubMedPubMedCentralGoogle Scholar
  94. 94.
    Momeni-Moghaddam P, Keyvanshokooh S, Ziaei-Nejad S, Parviz Salati A, Pasha-Zanoosi H (2015) Effects of mannan oligosaccharide supplementation on growth, some immune responses and gut lactic acid bacteria of common carp (Cyprinus Carpio) fingerlings. Vet Res Forum 6:239–244PubMedPubMedCentralGoogle Scholar
  95. 95.
    Moro G, Arslanoglu S, Stahl B, Jelinek J, Wahn U, Boehm G (2006) A mixture of prebiotic oligosaccharides reduces the incidence of atopic dermatitis during the first six months of age. Arch Dis Child 91:814–819CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Muegge BD, Kuczynski J, Knights D, Clemente JC, González A, Fontana L, Henrissat B, Knight R, Gordon JI (2011) Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332:970–974CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    Musso G, Gambino R, Cassader M (2010) Gut microbiota as a regulator of energy homeostasis and ectopic fat deposition: mechanisms and implications for metabolic disorders. Curr Opin Lipidol 21:76–83CrossRefPubMedGoogle Scholar
  98. 98.
    Nagura T, Hachimura S, Hashiguchi M, Ueda Y, Kanno T, Kikuchi H, Sayama K, Kaminogawa S (2002) Suppressive effect of dietary raffinose on T-helper 2 cell-mediated immunity. Br J Nutr 88:421–426CrossRefPubMedGoogle Scholar
  99. 99.
    Newburg DS, Walker WA (2007) Protection of the neonate by the innate immune system of developing gut and of human milk. Pediatr Res 61:2–8CrossRefPubMedGoogle Scholar
  100. 100.
    Niness KR (1999) Inulin and oligofructose: what are they? J Nutr 129:1402S–1406SCrossRefPubMedGoogle Scholar
  101. 101.
    Obermeier S, Rudloff S, Pohlentz G, Lentze MJ, Kunz C (1999) Secretion of 13C-labelled oligosaccharides into human milk and infant’s urine after an oral [13C]galactose load. Isotopes Environ Health Stud 35:119–125CrossRefPubMedGoogle Scholar
  102. 102.
    Ofek I, Beachey EH (1978) Mannose binding and epithelial cell adherence of Escherichia coli. Infect Immunity 22:247–254Google Scholar
  103. 103.
    Okazaki M, Fujikawa S, Matsumoto N (1990) Effect of xylooligosaccharide on the growth of bifidobacteria. Bifidobact Microflora 9:77–86CrossRefGoogle Scholar
  104. 104.
    Osman N, Adawi D, Molin G, Ahrne S, Berggren A, Jeppsson B (2006) Bifidobacterium infantis strains with and without a combination of oligofructose and inulin (OFI) attenuate inflammation in DSS-induced colitis in rats. BMC Gastroenterol 6:31CrossRefPubMedPubMedCentralGoogle Scholar
  105. 105.
    Paineau D, Payen F, Panserieu S, Coulombier G, Sobaszek A, Lartigau I, Brabet M, Galmiche J-P, Tripodi D, Sacher-Huvelin S, Chapalain V, Zourabichvili O, Respondek F, Wagner A, Bornet FRJ (2008) The effects of regular consumption of short-chain fructo-oligosaccharides on digestive comfort of subjects with minor functional bowel disorders. Br J Nutr 99:311–318CrossRefPubMedGoogle Scholar
  106. 106.
    Pant K, Yadav AK, Gupta P, Islam R, Saraya A, Venugopal SK (2017) Butyrate induces ROS-mediated apoptosis by modulating miR-22/SIRT-1 pathway in hepatic cancer cells. Redox Biol 12:340–349CrossRefPubMedPubMedCentralGoogle Scholar
  107. 107.
    Parnell JA, Reimer RA (2010) Effect of prebiotic fibre supplementation on hepatic gene expression and serum lipids: a dose-response study in JCR:LA-cp rats. Br J Nutr 103:1577–1584CrossRefPubMedGoogle Scholar
  108. 108.
    Pereira FC, Berry D (2017) Microbial nutrient niches in the gut. Environ Microbiol 19:1366–1378CrossRefPubMedPubMedCentralGoogle Scholar
  109. 109.
    Perugino G, Trincone A, Rossi M, Moracci M (2004) Oligosaccharide synthesis by glycosynthases. Trends Biotechnol 22:31–37CrossRefPubMedGoogle Scholar
  110. 110.
    Phelps CF (1965) The physical properties of inulin solutions. Biochem J 95:41–47CrossRefPubMedPubMedCentralGoogle Scholar
  111. 111.
    Plante OJ, Palmacci ER, Seeberger PH (2001) Automated solid-phase synthesis of oligosaccharides. Science 291:1523–1527CrossRefPubMedGoogle Scholar
  112. 112.
    Pourghassem Gargari B, Dehghan P, Aliasgharzadeh A, Asghari Jafar-Abadi M (2013) Effects of high performance inulin supplementation on glycemic control and antioxidant status in women with type 2 diabetes. Diabetes Metab J 37:140–148CrossRefPubMedPubMedCentralGoogle Scholar
  113. 113.
    Priem B, Gilbert M, Wakarchuk WW, Heyraud A, Samain E (2002) A new fermentation process allows large-scale production of human milk oligosaccharides by metabolically engineered bacteria. Glycobiology 12:235–240CrossRefPubMedGoogle Scholar
  114. 114.
    Propst EL, Flickinger EA, Bauer LL, Merchen NR, Fahey GC Jr (2003) A dose-response experiment evaluating the effects of oligofructose and inulin on nutrient digestibility, stool quality, and fecal protein catabolites in healthy adult dogs. J Anim Sci 81:3057–3066CrossRefPubMedGoogle Scholar
  115. 115.
    Prudden AR, Chinoy ZS, Wolfert MA, Boons G-J (2014) A multifunctional anomeric linker for the chemoenzymatic synthesis of complex oligosaccharides. Chem Commun 50:7132–7135CrossRefGoogle Scholar
  116. 116.
    Quintero M, Maldonado M, Perez-Munoz M, Jimenez R, Fangman T, Rupnow J, Wittke A, Russell M, Hutkins R (2011) Adherence inhibition of Cronobacter sakazakii to intestinal epithelial cells by prebiotic oligosaccharides. Curr Microbiol 62:1448–1454CrossRefPubMedGoogle Scholar
  117. 117.
    Rastall RA, Gibson GR (2015) Recent developments in prebiotics to selectively impact beneficial microbes and promote intestinal health. Curr Opin Biotechnol 32:42–46CrossRefPubMedGoogle Scholar
  118. 118.
    dos Reis SA, da Conceição LL, Rosa DD, Dias MMDS, Peluzio MDCG (2014) Mechanisms used by inulin-type fructans to improve the lipid profile. Nutr Hosp 31:528–534PubMedGoogle Scholar
  119. 119.
    Roberfroid MB (2005) Introducing inulin-type fructans. Br J Nutr 93:S13–S25CrossRefPubMedGoogle Scholar
  120. 120.
    Rogler G, Andus T (1998) Cytokines in inflammatory bowel disease. World J Surg 22:382–389CrossRefPubMedGoogle Scholar
  121. 121.
    Roller M, Rechkemmer G, Watzl B (2004) Prebiotic inulin enriched with oligofructose in combination with the probiotics Lactobacillus rhamnosus and Bifidobacterium lactis modulates intestinal immune functions in rats. J Nutr 134:153–156CrossRefPubMedGoogle Scholar
  122. 122.
    Ross GD, Větvička V (2008) CR122 (CD11b, CD18): a phagocyte and NK cell membrane receptor with multiple ligand specificities and functions. Clin Exp Immunol 92:181–184CrossRefGoogle Scholar
  123. 123.
    Rowland IR, Rumney CJ, Coutts JT, Lievense LC (1998) Effect of Bifidobacterium longum and inulin on gut bacterial metabolism and carcinogen-induced aberrant crypt foci in rats. Carcinogenesis 19:281–285CrossRefPubMedGoogle Scholar
  124. 124.
    Ruffing A, Mao Z, Ruizhen Chen R (2006) Metabolic engineering of Agrobacterium sp. for UDP-galactose regeneration and oligosaccharide synthesis. Metab Eng 8:465–473CrossRefPubMedGoogle Scholar
  125. 125.
    Ruiz-Palacios GM, Cervantes LE, Ramos P, Chavez-Munguia B, Newburg DS (2003) Campylobacter jejuni binds intestinal H(O) antigen (Fucα1, 2Galβ1, 4GlcNAc), and fucosyloligosaccharides of human milk inhibit its binding and infection. J Biol Chem 278:14112–14120CrossRefPubMedGoogle Scholar
  126. 126.
    Salyers AA, Vercellotti JR, West SE, Wilkins TD (1977) Fermentation of mucin and plant polysaccharides by strains of Bacteroides from the human colon. Appl Environ Microbiol 33:319–322PubMedPubMedCentralGoogle Scholar
  127. 127.
    Salyers AA, West SE, Vercellotti JR, Wilkins TD (1977) Fermentation of mucins and plant polysaccharides by anaerobic bacteria from the human colon. Appl Environ Microbiol 34:529–533PubMedPubMedCentralGoogle Scholar
  128. 128.
    Saville BA, Saville S (2018) Xylooligosaccharides and arabinoxylanoligosaccharides and their application as prebiotics. Appl Food Biotechnol 5:121–130Google Scholar
  129. 129.
    Scholz-Ahrens KE, Schaafsma G, van den Heuvel EG, Schrezenmeir J (2001) Effects of prebiotics on mineral metabolism. Am J Clin Nutr 73:459S–464SCrossRefPubMedGoogle Scholar
  130. 130.
    Schuster M, Wang P, Paulson JC, Wong C-H (1994) Solid-Phase Chemical-Enzymic Synthesis of Glycopeptides and Oligosaccharides. J Am Chem Soc 116:1135–1136CrossRefGoogle Scholar
  131. 131.
    Sears P, Wong CH (2001) Toward automated synthesis of oligosaccharides and glycoproteins. Science 291:2344–2350CrossRefPubMedGoogle Scholar
  132. 132.
    Sender R, Fuchs S, Milo R (2016) Revised estimates for the number of human and bacteria cells in the body. PLoS Biol 14:e1002533CrossRefPubMedPubMedCentralGoogle Scholar
  133. 133.
    Sender R, Fuchs S, Milo R (2016) Are we really vastly outnumbered? Revisiting the ratio of bacterial to host cells in humans. Cell 164:337–340CrossRefPubMedGoogle Scholar
  134. 134.
    Shepherd ES, DeLoache WC, Pruss KM, Whitaker WR, Sonnenburg JL (2018) An exclusive metabolic niche enables strain engraftment in the gut microbiota. Nature 557:434–438CrossRefPubMedPubMedCentralGoogle Scholar
  135. 135.
    Sierra C, Bernal M-J, Blasco J, Martínez R, Dalmau J, Ortuño I, Espín B, Vasallo M-I, Gil D, Vidal M-L, Infante D, Leis R, Maldonado J, Moreno J-M, Román E (2015) Prebiotic effect during the first year of life in healthy infants fed formula containing GOS as the only prebiotic: a multicentre, randomised, double-blind and placebo-controlled trial. Eur J Nutr 54:89–99CrossRefPubMedGoogle Scholar
  136. 136.
    Silk DBA, Davis A, Vulevic J, Tzortzis G, Gibson GR (2009) Clinical trial: the effects of a trans-galactooligosaccharide prebiotic on faecal microbiota and symptoms in irritable bowel syndrome. Aliment Pharmacol Ther 29:508–518CrossRefPubMedGoogle Scholar
  137. 137.
    Smiricky-Tjardes MR, Flickinger EA, Grieshop CM, Bauer LL, Murphy MR, Fahey GC Jr (2003) In vitro fermentation characteristics of selected oligosaccharides by swine fecal microflora. J Anim Sci 81:2505–2514CrossRefPubMedGoogle Scholar
  138. 138.
    Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly-Y M, Glickman JN, Garrett WS (2013) The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341:569–573CrossRefGoogle Scholar
  139. 139.
    Stewart ML, Timm DA, Slavin JL (2008) Fructooligosaccharides exhibit more rapid fermentation than long-chain inulin in an in vitro fermentation system. Nutr Res 28:329–334CrossRefPubMedGoogle Scholar
  140. 140.
    Tang WHW, Wang Z, Levison BS, Koeth RA, Britt EB, Fu X, Wu Y, Hazen SL (2013) Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk. N Engl J Med 368:1575–1584CrossRefPubMedPubMedCentralGoogle Scholar
  141. 141.
    Tan J, McKenzie C, Vuillermin PJ, Goverse G, Vinuesa CG, Mebius RE, Macia L, Mackay CR (2016) Dietary fiber and bacterial SCFA enhance oral tolerance and protect against food allergy through diverse cellular pathways. Cell Rep 15:2809–2824CrossRefPubMedGoogle Scholar
  142. 142.
    Thilakarathna WW, Langille MGI, Rupasinghe HPV (2018) Polyphenol-based prebiotics and synbiotics: potential for cancer chemoprevention. Curr Opin Food Sci 20:51–57CrossRefGoogle Scholar
  143. 143.
    Thompson WG, Longstreth GF, Drossman DA, Heaton KW, Irvine EJ, Müller-Lissner SA (1999) Functional bowel disorders and functional abdominal pain. Gut 45:II43–II47PubMedPubMedCentralGoogle Scholar
  144. 144.
    Thongaram T, Hoeflinger JL, Chow J, Miller MJ (2017) Prebiotic galactooligosaccharide metabolism by probiotic lactobacilli and bifidobacteria. J Agric Food Chem 65:4184–4192CrossRefPubMedGoogle Scholar
  145. 145.
    Tilg H, Adolph TE, Gerner RR, Moschen AR (2018) The intestinal microbiota in colorectal cancer. Cancer Cell 33:954–964CrossRefPubMedGoogle Scholar
  146. 146.
    Tomás-Barberán FA, Selma MV, Espín JC (2016) Interactions of gut microbiota with dietary polyphenols and consequences to human health. Curr Opin Clin Nutr Metab Care 19:471–476CrossRefPubMedGoogle Scholar
  147. 147.
    Trautwein EA, Rieckhoff D, Erbersdobler HF (1998) Dietary inulin lowers plasma cholesterol and triacylglycerol and alters biliary bile acid profile in hamsters. J Nutr 128:1937–1943CrossRefPubMedGoogle Scholar
  148. 148.
    Treves DS, Manning S, Adams J (1998) Repeated evolution of an acetate-crossfeeding polymorphism in long-term populations of Escherichia coli. Mol Biol Evol 15:789–797CrossRefPubMedGoogle Scholar
  149. 149.
    Tuohy KM, Probert HM, Smejkal CW, Gibson GR (2003) Using probiotics and prebiotics to improve gut health. Drug Discov Today 8:692–700CrossRefPubMedGoogle Scholar
  150. 150.
    Turnbaugh PJ, Bäckhed F, Fulton L, Gordon JI (2008) Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 3:213–223CrossRefPubMedPubMedCentralGoogle Scholar
  151. 151.
    Turroni F, Milani C, Duranti S, Mahony J, van Sinderen D, Ventura M (2018) Glycan utilization and cross-feeding activities by bifidobacteria. Trends Microbiol 26:339–350CrossRefPubMedGoogle Scholar
  152. 152.
    Tzortzis G, Vulevic J (2009) Galacto-oligosaccharide prebiotics. In: Charalampopoulos D, Rastall RA (eds) Prebiotics and probiotics science and technology. Springer, New York, pp 207–244CrossRefGoogle Scholar
  153. 153.
    Underwood MA, Gaerlan S, De Leoz MLA, Dimapasoc L, Kalanetra KM, Lemay DG, German JB, Mills DA, Lebrilla CB (2015) Human milk oligosaccharides in premature infants: absorption, excretion, and influence on the intestinal microbiota. Pediatr Res 78:670–677CrossRefPubMedPubMedCentralGoogle Scholar
  154. 154.
    Underwood MA, German JB, Lebrilla CB, Mills DA (2015) Bifidobacterium longum subspecies infantis: champion colonizer of the infant gut. Pediatr Res 77:229–235CrossRefPubMedGoogle Scholar
  155. 155.
    Vandeputte D, Falony G, Vieira-Silva S, Wang J, Sailer M, Theis S, Verbeke K, Raes J (2017) Prebiotic inulin-type fructans induce specific changes in the human gut microbiota. Gut 66:1968–1974CrossRefPubMedPubMedCentralGoogle Scholar
  156. 156.
    Vatanen T, Franzosa EA, Schwager R, Tripathi S, Arthur TD, Vehik K, Lernmark Å, Hagopian WA, Rewers MJ, She J-X, Toppari J, Ziegler A-G, Akolkar B, Krischer JP, Stewart CJ, Ajami NJ, Petrosino JF, Gevers D, Lähdesmäki H, Vlamakis H, Huttenhower C, Xavier RJ (2018) The human gut microbiome in early-onset type 1 diabetes from the TEDDY study. Nature 562:589–594CrossRefPubMedPubMedCentralGoogle Scholar
  157. 157.
    Vinolo MAR, Rodrigues HG, Nachbar RT, Curi R (2011) Regulation of inflammation by short chain fatty acids. Nutrients 3:858–876CrossRefPubMedPubMedCentralGoogle Scholar
  158. 158.
    Vogt L, Meyer D, Pullens G, Faas M, Smelt M, Venema K, Ramasamy U, Schols HA, De Vos P (2015) Immunological properties of inulin-type fructans. Crit Rev Food Sci Nutr 55:414–436CrossRefPubMedGoogle Scholar
  159. 159.
    Vohra Y, Vasan M, Venot A, Boons G-J (2008) One-pot synthesis of oligosaccharides by combining reductive openings of benzylidene acetals and glycosylations. Org Lett 10:3247–3250CrossRefPubMedPubMedCentralGoogle Scholar
  160. 160.
    Vulevic J, Drakoularakou A, Yaqoob P, Tzortzis G, Gibson GR (2008) Modulation of the fecal microflora profile and immune function by a novel trans-galactooligosaccharide mixture (B-GOS) in healthy elderly volunteers. Am J Clin Nutr 88:1438–1446PubMedGoogle Scholar
  161. 161.
    Waldecker M, Kautenburger T, Daumann H, Busch C, Schrenk D (2008) Inhibition of histone-deacetylase activity by short-chain fatty acids and some polyphenol metabolites formed in the colon. J Nutr Biochem 19:587–593CrossRefPubMedGoogle Scholar
  162. 162.
    Wang C-C, Lee J-C, Luo S-Y, Kulkarni SS, Huang Y-W, Lee C-C, Chang K-L, Hung S-C (2007) Regioselective one-pot protection of carbohydrates. Nature 446:896–899CrossRefPubMedGoogle Scholar
  163. 163.
    Weng M, Ganguli K, Zhu W, Shi HN, Walker WA (2014) Conditioned medium from Bifidobacterium infantis protects against Cronobacter sakazakii-induced intestinal inflammation in newborn mice. Am J Physiol Gastrointest Liver Physiol 306:G779–G787CrossRefPubMedPubMedCentralGoogle Scholar
  164. 164.
    Whistler RL, Bushway AA, Singh PP, Nakahara W, Tokuzen R (1976) Noncytotoxic, antitumor polysaccharides. In: Tipson RS (ed) Advances in carbohydrate chemistry and biochemistry. Academic Press, Cambridge, pp 235–275Google Scholar
  165. 165.
    White BA, Lamed R, Bayer EA, Flint HJ (2014) Biomass utilization by gut microbiomes. Annu Rev Microbiol 68:279–296CrossRefPubMedGoogle Scholar
  166. 166.
    Xiao L, Van’t Land B, Engen PA, Naqib A, Green SJ, Nato A, Leusink-Muis T, Garssen J, Keshavarzian A, Stahl B, Folkerts G (2018) Human milk oligosaccharides protect against the development of autoimmune diabetes in NOD-mice. Sci Rep 8:3829CrossRefPubMedPubMedCentralGoogle Scholar
  167. 167.
    Yamashita K, Kawai K, Itakura M (1984) Effects of fructo-oligosaccharides on blood glucose and serum lipids in diabetic subjects. Nutr Res 4:961–966CrossRefGoogle Scholar
  168. 168.
    Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP, Heath AC, Warner B, Reeder J, Kuczynski J, Caporaso JG, Lozupone CA, Lauber C, Clemente JC, Knights D, Knight R, Gordon JI (2012) Human gut microbiome viewed across age and geography. Nature 486:222–227CrossRefPubMedPubMedCentralGoogle Scholar
  169. 169.
    Yu J, Shin J, Park M, Seydametova E, Jung S-M, Seo J-H, Kweon D-H (2018) Engineering of α-1,3-fucosyltransferases for production of 3-fucosyllactose in Escherichia coli. Metab Eng 48:269–278CrossRefPubMedGoogle Scholar
  170. 170.
    Yu S, Liu J-J, Yun EJ, Kwak S, Kim KH, Jin Y-S (2018) Production of a human milk oligosaccharide 2′-fucosyllactose by metabolically engineered Saccharomyces cerevisiae. Microb Cell Fact 17:101CrossRefPubMedPubMedCentralGoogle Scholar
  171. 171.
    Yu Y, Lasanajak Y, Song X, Hu L, Ramani S, Mickum ML, Ashline DJ, Prasad BVV, Estes MK, Reinhold VN, Cummings RD, Smith DF (2014) Human milk contains novel glycans that are potential decoy receptors for neonatal rotaviruses. Mol Cell Proteom 13:2944–2960CrossRefGoogle Scholar
  172. 172.
    Zenhom M, Hyder A, de Vrese M, Heller KJ, Roeder T, Schrezenmeir J (2011) Prebiotic oligosaccharides reduce proinflammatory cytokines in intestinal Caco-2 cells via activation of PPARγ and peptidoglycan recognition protein 3. J Nutr 141:971–977CrossRefPubMedGoogle Scholar
  173. 173.
    Zeuner B, Vuillemin M, Holck J, Muschiol J, Meyer AS (2018) Loop engineering of an α-1,3/4-l-fucosidase for improved synthesis of human milk oligosaccharides. Enzyme Microb Technol 115:37–44CrossRefPubMedGoogle Scholar
  174. 174.
    Zhang Z, Ollmann IR, Ye X-S, Wischnat R, Baasov T, Wong C-H (1999) Programmable one-pot oligosaccharide synthesis. J Am Chem Soc 121:734–753CrossRefGoogle Scholar
  175. 175.
    Zivkovic AM, German JB, Lebrilla CB, Mills DA (2011) Human milk glycobiome and its impact on the infant gastrointestinal microbiota. Proc Natl Acad Sci USA 108(Suppl 1):4653–4658CrossRefPubMedGoogle Scholar

Copyright information

© Society for Industrial Microbiology and Biotechnology 2019

Authors and Affiliations

  1. 1.Department of Chemical and Biological EngineeringIowa State UniversityAmesUSA

Personalised recommendations