Glycan Utilisation and Function in the Microbiome of Weaning Infants
Abstract
:1. Introduction
2. Glycans: Sources, Structures, and Functions
2.1. Sources: Mammalian, Plant, Microbial
2.2. Structures and Functions
3. Dietary Glycans in the First 1000 Days
3.1. Human and Ruminant Milk Oligosaccharides
3.2. Plant-Derived Glycans
4. Microbiome
4.1. Neonatal Microbes and Dietary Glycans
4.2. Effect of Dietary Glycans at Weaning
4.3. Species Characteristics
4.4. Trophic Networks, Hierarchies, and Biogeography
5. Dietary Glycans Influence the Gut Mucosa
5.1. Mucin Production and Glycosylation
5.2. Composition of the Mucosa
6. Glycan Utilisation Systems by Infant Microbiota
7. Microbial Biosynthesis of Glycans
8. Dietary Glycans in Immunity
9. Summary
Author Contributions
Funding
Conflicts of Interest
References
- Varki, A. Biological roles of glycans. Glycobiology 2017, 27, 3–49. [Google Scholar] [CrossRef] [PubMed]
- Moran, A.P. Microbial Glycobiology: Structures, Relevance and Applications; Elsevier: Amsterdam, The Netherlands, 2009. [Google Scholar]
- Wandall, H.H.; Bagdonaite, I. Global aspects of viral glycosylation. Glycobiology 2018, 28, 443–467. [Google Scholar] [Green Version]
- Burton, R.A.; Gidley, M.J.; Fincher, G.B. Heterogeneity in the chemistry, structure and function of plant cell walls. Nat. Chem. Biol. 2010, 6, 724. [Google Scholar] [CrossRef] [PubMed]
- Dias, A.M.; Pereira, M.S.; Padrão, N.A.; Alves, I.; Marcos-Pinto, R.; Lago, P.; Pinho, S.S. Glycans as critical regulators of gut immunity in homeostasis and disease. Cell. Immunol. 2018, 333, 9–18. [Google Scholar] [CrossRef] [PubMed]
- Cummings, R.D.; Pierce, J.M. The challenge and promise of glycomics. Chem. Biol. 2014, 21, 1–15. [Google Scholar] [CrossRef] [PubMed]
- Martens, E.C.; Kelly, A.G.; Tauzin, A.S.; Brumer, H. The devil lies in the details: How variations in polysaccharide fine-structure impact the physiology and evolution of gut microbes. J. Mol. Biol. 2014, 426, 3851–3865. [Google Scholar] [CrossRef]
- Lyons, J.J.; Milner, J.D.; Rosenzweig, S.D. Glycans instructing immunity: The emerging role of altered glycosylation in clinical immunology. Front. Pediatrics 2015, 3, 54. [Google Scholar] [CrossRef]
- Jakobsdottir, G.; Nyman, M.; Fåk, F. Designing future prebiotic fiber to target metabolic syndrome. Nutrition 2014, 30, 497–502. [Google Scholar] [CrossRef]
- Kunz, C.; Meyer, C.; Collado, M.C.; Geiger, L.; García-Mantrana, I.; Bertua-Ríos, B.; Martínez-Costa, C.; Borsch, C.; Rudloff, S. Influence of Gestational Age, Secretor, and Lewis Blood Group Status on the Oligosaccharide Content of Human Milk. J. Pediatric Gastroenterol. Nutr. 2017, 64, 789–798. [Google Scholar] [CrossRef]
- Urashima, T.; Taufik, E.; Fukuda, K.; Asakuma, S. Recent advances in studies on milk oligosaccharides of cows and other domestic farm animals. Biosci. Biotechnol. Biochem. 2013, 77, 455–466. [Google Scholar] [CrossRef]
- Castanys-Muñoz, E.; Martin, M.J.; Vazquez, E. Building a Beneficial Microbiome from Birth. Adv. Nutr. 2016, 7, 323–330. [Google Scholar] [CrossRef] [PubMed]
- Holscher, H.D.; Faust, K.L.; Czerkies, L.A.; Litov, R.; Ziegler, E.E.; Lessin, H.; Hatch, T.; Sun, S.; Tappenden, K.A. Effects of Prebiotic-Containing Infant Formula on Gastrointestinal Tolerance and Fecal Microbiota in a Randomized Controlled Trial. J. Parenter. Enter. Nutr. 2012, 36, 95S–105S. [Google Scholar] [CrossRef] [PubMed]
- Vandenplas, Y.; Greef, E.D.; Veereman, G. Prebiotics in infant formula. Gut Microbes 2014, 5, 681–687. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Borewicz, K.; Suarez-Diez, M.; Hechler, C.; Beijers, R.; de Weerth, C.; Arts, I.; Penders, J.; Thijs, C.; Nauta, A.; Lindner, C.; et al. The effect of prebiotic fortified infant formulas on microbiota composition and dynamics in early life. Sci. Rep. 2019, 9, 2434. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Doherty, A.M.; Lodge, C.J.; Dharmage, S.C.; Dai, X.; Bode, L.; Lowe, A.J. Human Milk Oligosaccharides and Associations With Immune-Mediated Disease and Infection in Childhood: A Systematic Review. Front. Pediatrics 2018, 6, 91. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Coppa, G.; Pierani, P.; Zampini, L.; Carloni, I.; Carlucci, A.; Gabrielli, O. Oligosaccharides in human milk during different phases of lactation. Acta Paediatr. 1999, 88, 89–94. [Google Scholar] [CrossRef]
- Veh, R.W.; Michalski, J.-C.; Corfield, A.P.; Sander-Wewer, M.; Gies, D.; Schauer, R. New chromatographic system for the rapid analysis and preparation of colostrum sialyloligosaccharides. J. Chromatogr. A 1981, 212, 313–322. [Google Scholar] [CrossRef]
- Aldredge, D.L.; Geronimo, M.R.; Hua, S.; Nwosu, C.C.; Lebrilla, C.B.; Barile, D. Annotation and structural elucidation of bovine milk oligosaccharides and determination of novel fucosylated structures. Glycobiology 2013, 23, 664–676. [Google Scholar] [CrossRef]
- Ninonuevo, M.R.; Park, Y.; Yin, H.; Zhang, J.; Ward, R.E.; Clowers, B.H.; German, J.B.; Freeman, S.L.; Killeen, K.; Grimm, R. A strategy for annotating the human milk glycome. J. Agric. Food Chem. 2006, 54, 7471–7480. [Google Scholar] [CrossRef]
- Tao, N.; DePeters, E.; German, J.; Grimm, R.; Lebrilla, C. Variations in bovine milk oligosaccharides during early and middle lactation stages analyzed by high-performance liquid chromatography-chip/mass spectrometry. J. Dairy Sci. 2009, 92, 2991–3001. [Google Scholar] [CrossRef]
- Barile, D.; Marotta, M.; Chu, C.; Mehra, R.; Grimm, R.; Lebrilla, C.B.; German, J. Neutral and acidic oligosaccharides in Holstein-Friesian colostrum during the first 3 days of lactation measured by high performance liquid chromatography on a microfluidic chip and time-of-flight mass spectrometry. J. Dairy Sci. 2010, 93, 3940–3949. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Martin, C.; Ling, P.-R.; Blackburn, G. Review of infant feeding: Key features of breast milk and infant formula. Nutrients 2016, 8, 279. [Google Scholar] [CrossRef] [PubMed]
- Wylie, A.D.; Zandberg, W.F. Quantitation of Sialic Acids in Infant Formulas by Liquid Chromatography–Mass Spectrometry: An Assessment of Different Protein Sources and Discovery of New Analogues. J. Agric. Food Chem. 2018, 66, 8114–8123. [Google Scholar] [CrossRef] [PubMed]
- Samraj, A.N.; Pearce, O.M.T.; Läubli, H.; Crittenden, A.N.; Bergfeld, A.K.; Banda, K.; Gregg, C.J.; Bingman, A.E.; Secrest, P.; Diaz, S.L.; et al. A red meat-derived glycan promotes inflammation and cancer progression. Proc. Natl. Acad. Sci. USA 2015, 112, 542. [Google Scholar] [CrossRef] [PubMed]
- Urashima, T.; Kitaoka, M.; Asakuma, S.; Messer, M. Milk Oligosaccharides. In Advanced Dairy Chemistry: Volume 3: Lactose, Water, Salts and Minor Constituents; McSweeney, P., Fox, P.F., Eds.; Springer: New York, NY, USA, 2009; pp. 295–349. [Google Scholar] [CrossRef]
- Martinez-Ferez, A.; Rudloff, S.; Guadix, A.; Henkel, C.A.; Pohlentz, G.; Boza, J.J.; Guadix, E.M.; Kunz, C. Goats’ milk as a natural source of lactose-derived oligosaccharides: Isolation by membrane technology. Int. Dairy J. 2006, 16, 173–181. [Google Scholar] [CrossRef]
- Morrow, A.L.; Warren, C.D.; Newburg, D.S.; Ruiz-Palacios, G.; Pickering, L.K.; Altaye, M.; Chaturvedi, P. Fucosylated human milk oligosaccharides vary between individuals and over the course of lactation. Glycobiology 2001, 11, 365–372. [Google Scholar]
- Korpela, K.; Salonen, A.; Hickman, B.; Kunz, C.; Sprenger, N.; Kukkonen, K.; Savilahti, E.; Kuitunen, M.; de Vos, W.M. Fucosylated oligosaccharides in mother’s milk alleviate the effects of caesarean birth on infant gut microbiota. Sci. Rep. 2018, 8, 13757. [Google Scholar] [CrossRef]
- Wismar, R.; Brix, S.; Frøkiær, H.; Lærke, H.N. Dietary fibers as immunoregulatory compounds in health and disease. Ann. N. Y. Acad. Sci. 2010, 1190, 70–85. [Google Scholar] [CrossRef]
- Warren, F.J.; Fukuma, N.M.; Mikkelsen, D.; Flanagan, B.M.; Williams, B.A.; Lisle, A.T.; Cuív, P.Ó.; Morrison, M.; Gidley, M.J. Food Starch Structure Impacts Gut Microbiome Composition. mSphere 2018, 3, e00086-18. [Google Scholar] [CrossRef] [Green Version]
- Gamage, H.K.A.H.; Tetu, S.G.; Chong, R.W.W.; Ashton, J.; Packer, N.H.; Paulsen, I.T. Cereal products derived from wheat, sorghum, rice and oats alter the infant gut microbiota in vitro. Sci. Rep. 2017, 7, 14312. [Google Scholar] [CrossRef]
- Bernal, M.J.; Periago, M.J.; Martínez, R.; Ortuño, I.; Sánchez-Solís, M.; Ros, G.; Romero, F.; Abellán, P. Effects of infant cereals with different carbohydrate profiles on colonic function—Randomised and double-blind clinical trial in infants aged between 6 and 12 months—Pilot study. Eur. J. Pediatric 2013, 172, 1535–1542. [Google Scholar] [CrossRef] [PubMed]
- Tuncil, Y.E.; Nakatsu, C.H.; Kazem, A.E.; Arioglu-Tuncil, S.; Reuhs, B.; Martens, E.C.; Hamaker, B.R. Delayed utilization of some fast-fermenting soluble dietary fibers by human gut microbiota when presented in a mixture. J. Funct. Foods 2017, 32, 347–357. [Google Scholar] [CrossRef]
- Louis, P.; Young, P.; Holtrop, G.; Flint, H.J. Diversity of human colonic butyrate-producing bacteria revealed by analysis of the butyryl-CoA: Acetate CoA-transferase gene. Environ. Microbiol. 2010, 12, 304–314. [Google Scholar] [CrossRef] [PubMed]
- Rios-Covian, D.; Gueimonde, M.; Duncan, S.H.; Flint, H.J.; de Los Reyes-Gavilan, C.G. Enhanced butyrate formation by cross-feeding between Faecalibacterium prausnitzii and Bifidobacterium adolescentis. Fems Microbiol. Lett. 2015, 362. [Google Scholar] [CrossRef] [PubMed]
- Walker, A.W.; Flint, H.J.; Sheridan, P.O.; Chung, W.S.F.; Duncan, S.H.; Bosscher, D.; Vermeiren, J.; Garcia-Campayo, V.; Parkhill, J. Impact of carbohydrate substrate complexity on the diversity of the human colonic microbiota. Fems Microbiol. Ecol. 2018, 95. [Google Scholar] [CrossRef] [Green Version]
- Aagaard, K.; Ma, J.; Antony, K.M.; Ganu, R.; Petrosino, J.; Versalovic, J. The placenta harbors a unique microbiome. Sci. Transl. Med. 2014, 6, 237ra265. [Google Scholar] [CrossRef]
- Schlinzig, T.; Johansson, S.; Stephansson, O.; Hammarstrom, L.; Zetterstrom, R.H.; von Dobeln, U.; Cnattingius, S.; Norman, M. Surge of immune cell formation at birth differs by mode of delivery and infant characteristics-A population-based cohort study. PLoS ONE 2017, 12, e0184748. [Google Scholar] [CrossRef]
- Negele, K.; Heinrich, J.; Borte, M.; von Berg, A.; Schaaf, B.; Lehmann, I.; Wichmann, H.E.; Bolte, G.; Group, L.S. Mode of delivery and development of atopic disease during the first 2 years of life. Pediatric Allergy Immunol. 2004, 15, 48–54. [Google Scholar] [CrossRef]
- Li, H.t.; Zhou, Y.b.; Liu, J.m. The impact of cesarean section on offspring overweight and obesity: A systematic review and meta-analysis. Int. J. Obes. 2012, 37, 893. [Google Scholar] [CrossRef]
- Tamburini, S.; Shen, N.; Wu, H.C.; Clemente, J.C. The microbiome in early life: Implications for health outcomes. Nat. Med. 2016, 22, 713. [Google Scholar] [CrossRef]
- Tannock, G.W.; Lawley, B.; Munro, K.; Gowri Pathmanathan, S.; Zhou, S.J.; Makrides, M.; Gibson, R.A.; Sullivan, T.; Prosser, C.G.; Lowry, D.; et al. Comparison of the Compositions of the Stool Microbiotas of Infants Fed Goat Milk Formula, Cow Milk-Based Formula, or Breast Milk. Appl. Environ. Microbiol. 2013, 79, 3040. [Google Scholar] [CrossRef] [PubMed]
- Goonatilleke, E.; Xu, G.; Davis, J.C.; Lebrilla, C.B.; German, J.B.; Smilowitz, J.T. Absolute Quantitation of Human Milk Oligosaccharides Reveals Phenotypic Variations during Lactation. J. Nutr. 2016, 147, 117–124. [Google Scholar] [Green Version]
- Bai, Y.; Tao, J.; Zhou, J.; Fan, Q.; Liu, M.; Hu, Y.; Xu, Y.; Zhang, L.; Yuan, J.; Li, W. Fucosylated Human Milk Oligosaccharides and N-Glycans in the Milk of Chinese Mothers Regulate the Gut Microbiome of Their Breast-Fed Infants during Different Lactation Stages. MSystems 2018, 3, e00206–e00218. [Google Scholar] [CrossRef] [PubMed]
- De Filippo, C.; Cavalieri, D.; Di Paola, M.; Ramazzotti, M.; Poullet, J.B.; Massart, S.; Collini, S.; Pieraccini, G.; Lionetti, P. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl. Acad. Sci. USA 2010, 107, 14691. [Google Scholar] [CrossRef] [PubMed]
- Backhed, F.; Roswall, J.; Peng, Y.; Feng, Q.; Jia, H.; Kovatcheva-Datchary, P.; Li, Y.; Xia, Y.; Xie, H.; Zhong, H.; et al. Dynamics and Stabilization of the Human Gut Microbiome during the First Year of Life. Cell Host Microbe 2015, 17, 852. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Subramanian, S.; Huq, S.; Yatsunenko, T.; Haque, R.; Mahfuz, M.; Alam, M.A.; Benezra, A.; DeStefano, J.; Meier, M.F.; Muegge, B.D. Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature 2014, 510, 417. [Google Scholar] [CrossRef] [PubMed]
- Lim, E.S.; Zhou, Y.; Zhao, G.; Bauer, I.K.; Droit, L.; Ndao, I.M.; Warner, B.B.; Tarr, P.I.; Wang, D.; Holtz, L.R. Early life dynamics of the human gut virome and bacterial microbiome in infants. Nat. Med. 2015, 21, 1228. [Google Scholar] [CrossRef]
- Bäckhed, F.; Ley, R.E.; Sonnenburg, J.L.; Peterson, D.A.; Gordon, J.I. Host-bacterial mutualism in the human intestine. Science 2005, 307, 1915–1920. [Google Scholar]
- Leitch, E.C.M.; Walker, A.W.; Duncan, S.H.; Holtrop, G.; Flint, H.J. Selective colonization of insoluble substrates by human faecal bacteria. Environ. Microbiol. 2007, 9, 667–679. [Google Scholar] [CrossRef]
- Scheiwiller, J.; Arrigoni, E.; Brouns, F.; Amado, R. Human faecal microbiota develops the ability to degrade type 3 resistant starch during weaning. J. Pediatric Gastroenterol. Nutr. 2006, 43, 584–591. [Google Scholar] [CrossRef]
- Tailford, L.E.; Crost, E.H.; Kavanaugh, D.; Juge, N. Mucin glycan foraging in the human gut microbiome. Front. Genet. 2015, 6, 81. [Google Scholar] [CrossRef] [PubMed]
- Macfarlane, G.; Gibson, G.; Cummings, J. Comparison of fermentation reactions in different regions of the human colon. J. Appl. Bacteriol. 1992, 72, 57–64. [Google Scholar] [PubMed]
- Albenberg, L.; Esipova, T.V.; Judge, C.P.; Bittinger, K.; Chen, J.; Laughlin, A.; Grunberg, S.; Baldassano, R.N.; Lewis, J.D.; Li, H.; et al. Correlation Between Intraluminal Oxygen Gradient and Radial Partitioning of Intestinal Microbiota. Gastroenterology 2014, 147, 1055–1063.e8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lind Due, V.; Bonde, J.; Kann, T.; Perner, A. Extremely low oxygen tension in the rectal lumen of human subjects. Acta Anaesthesiol. Scand. 2003, 47, 372. [Google Scholar] [CrossRef] [PubMed]
- Macfarlane, S.; Macfarlane, G.T. Regulation of short-chain fatty acid production. Proc. Nutr. Soc. 2003, 62, 67–72. [Google Scholar] [CrossRef] [PubMed]
- Eckburg, P.B.; Bik, E.M.; Bernstein, C.N.; Purdom, E.; Dethlefsen, L.; Sargent, M.; Gill, S.R.; Nelson, K.E.; Relman, D.A. Diversity of the human intestinal microbial flora. Science 2005, 308, 1635–1638. [Google Scholar] [CrossRef] [PubMed]
- Donaldson, G.P.; Lee, S.M.; Mazmanian, S.K. Gut biogeography of the bacterial microbiota. Nat. Rev. Microbiol. 2016, 14, 20. [Google Scholar] [CrossRef]
- Fanaro, S.; Chierici, R.; Guerrini, P.; Vigi, V. Intestinal microflora in early infancy: composition and development. Acta Paediatr. 2003, 92, 48–55. [Google Scholar] [CrossRef]
- Palmer, C.; Bik, E.M.; DiGiulio, D.B.; Relman, D.A.; Brown, P.O. Development of the human infant intestinal microbiota. PLoS Biol. 2007, 5, e177. [Google Scholar] [CrossRef]
- Zmora, N.; Zilberman-Schapira, G.; Suez, J.; Mor, U.; Dori-Bachash, M.; Bashiardes, S.; Kotler, E.; Zur, M.; Regev-Lehavi, D.; Brik, R.B.-Z. Personalized gut mucosal colonization resistance to empiric probiotics is associated with unique host and microbiome features. Cell 2018, 174, 1388–1405. [Google Scholar] [CrossRef]
- Corfield, A.P. Mucins: A biologically relevant glycan barrier in mucosal protection. Biochim. Et Biophys. Acta (Bba) - Gen. Subj. 2015, 1850, 236–252. [Google Scholar] [CrossRef] [PubMed]
- Bergstrom, K.S.; Xia, L. Mucin-type O-glycans and their roles in intestinal homeostasis. Glycobiology 2013, 23, 1026–1037. [Google Scholar] [CrossRef] [PubMed]
- Arike, L.; Holmén-Larsson, J.; Hansson, G.C. Intestinal Muc2 mucin O-glycosylation is affected by microbiota and regulated by differential expression of glycosyltranferases. Glycobiology 2017, 27, 318–328. [Google Scholar] [CrossRef] [PubMed]
- Montagne, L.; Piel, C.; Lalles, J. Effect of diet on mucin kinetics and composition: Nutrition and health implications. Nutr. Rev. 2004, 62, 105–114. [Google Scholar] [CrossRef] [PubMed]
- Schmidt-Wittig, U.; Enss, M.-L.; Coenen, M.; Gärtner, K.; Hedrich, H. Response of rat colonic mucosa to a high fiber diet. Ann. Nutr. Metab. 1996, 40, 343–350. [Google Scholar] [CrossRef] [PubMed]
- Barcelo, A.; Claustre, J.; Moro, F.; Chayvialle, J.; Cuber, J.; Plaisancié, P. Mucin secretion is modulated by luminal factors in the isolated vascularly perfused rat colon. Gut 2000, 46, 218–224. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bakshani, C.R.; Morales-Garcia, A.L.; Althaus, M.; Wilcox, M.D.; Pearson, J.P.; Bythell, J.C.; Burgess, J.G. Evolutionary conservation of the antimicrobial function of mucus: A first defence against infection. NPJ Biofilms Microbiomes 2018, 4, 14. [Google Scholar] [CrossRef]
- Ndeh, D.; Gilbert, H.J. Biochemistry of complex glycan depolymerisation by the human gut microbiota. Fems Microbiol. Rev. 2018, 42, 146–164. [Google Scholar] [CrossRef] [Green Version]
- Koropatkin, N.M.; Cameron, E.A.; Martens, E.C. How glycan metabolism shapes the human gut microbiota. Nat. Rev. Microbiol. 2012, 10, 323. [Google Scholar] [CrossRef]
- Garrido, D.; Ruiz-Moyano, S.; Lemay, D.G.; Sela, D.A.; German, J.B.; Mills, D.A. Comparative transcriptomics reveals key differences in the response to milk oligosaccharides of infant gut-associated bifidobacteria. Sci. Rep. 2015, 5, 13517. [Google Scholar] [CrossRef]
- Pokusaeva, K.; Fitzgerald, G.F.; van Sinderen, D. Carbohydrate metabolism in Bifidobacteria. Genes Nutr. 2011, 6, 285–306. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Milani, C.; Turroni, F.; Duranti, S.; Lugli, G.A.; Mancabelli, L.; Ferrario, C.; van Sinderen, D.; Ventura, M. Genomics of the genus Bifidobacterium reveals species-specific adaptation to the glycan-rich gut environment. Appl. Environ. Microbiol. 2016, 82, 980–991. [Google Scholar] [CrossRef] [PubMed]
- Lugli, G.A.; Mancino, W.; Milani, C.; Duranti, S.; Turroni, F.; van Sinderen, D.; Ventura, M. Reconstruction of the Bifidobacterial Pan-Secretome Reveals the Network of Extracellular Interactions between Bifidobacteria and the Infant Gut. Appl. Environ. Microbiol. 2018, 84, e00796-18. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kitaoka, M. Bifidobacterial enzymes involved in the metabolism of human milk oligosaccharides. Adv. Nutr. 2012, 3, 422S–429S. [Google Scholar] [CrossRef] [PubMed]
- Katoh, T.; Maeshibu, T.; Kikkawa, K.-i.; Gotoh, A.; Tomabechi, Y.; Nakamura, M.; Liao, W.-H.; Yamaguchi, M.; Ashida, H.; Yamamoto, K. Identification and characterization of a sulfoglycosidase from Bifidobacterium bifidum implicated in mucin glycan utilization. Biosci. Biotechnol. Biochem. 2017, 81, 2018–2027. [Google Scholar] [CrossRef]
- Turroni, F.; Milani, C.; van Sinderen, D.; Ventura, M. Genetic strategies for mucin metabolism in Bifidobacterium bifidum PRL2010: An example of possible human-microbe co-evolution. Gut Microbes 2011, 2, 183–189. [Google Scholar] [CrossRef]
- Turroni, F.; Bottacini, F.; Foroni, E.; Mulder, I.; Kim, J.-H.; Zomer, A.; Sánchez, B.; Bidossi, A.; Ferrarini, A.; Giubellini, V. Genome analysis of Bifidobacterium bifidum PRL2010 reveals metabolic pathways for host-derived glycan foraging. Proc. Natl. Acad. Sci. USA 2010, 107, 19514–19519. [Google Scholar] [CrossRef]
- Ruas-Madiedo, P.; Gueimonde, M.; Fernández-García, M.; Clara, G.; Margolles, A. Mucin degradation by Bifidobacterium strains isolated from the human intestinal microbiota. Appl. Environ. Microbiol. 2008, 74, 1936–1940. [Google Scholar] [CrossRef]
- Mills, D.A.; Garrido, D.; Barile, D. A Molecular Basis for Bifidobacterial Enrichment in the Infant Gastrointestinal Tract. Adv. Nutr. 2012, 3, 415S–421S. [Google Scholar]
- Garrido, D.; Dallas, D.C.; Mills, D.A. Consumption of human milk glycoconjugates by infant-associated bifidobacteria: Mechanisms and implications. Microbiology 2013, 159, 649–664. [Google Scholar] [CrossRef]
- Pacheco, A.R.; Barile, D.; Underwood, M.A.; Mills, D.A. The impact of the milk glycobiome on the neonate gut microbiota. Annu. Rev. Anim. Biosci. 2015, 3, 419–445. [Google Scholar] [CrossRef] [PubMed]
- Marcobal, A.; Barboza, M.; Froehlich, J.W.; Block, D.E.; German, J.B.; Lebrilla, C.B.; Mills, D.A. Consumption of human milk oligosaccharides by gut-related microbes. J. Agric. Food Chem. 2010, 58, 5334–5340. [Google Scholar] [CrossRef] [PubMed]
- Rogowski, A.; Briggs, J.A.; Mortimer, J.C.; Tryfona, T.; Terrapon, N.; Lowe, E.C.; Baslé, A.; Morland, C.; Day, A.M.; Zheng, H.; et al. Glycan complexity dictates microbial resource allocation in the large intestine. Nat. Commun. 2015, 6, 7481. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sela, D.A. Bifidobacterial utilization of human milk oligosaccharides. Int. J. Food Microbiol. 2011, 149, 58–64. [Google Scholar] [CrossRef] [PubMed]
- Sheridan, P.O.; Martin, J.C.; Lawley, T.D.; Browne, H.P.; Harris, H.M.; Bernalier-Donadille, A.; Duncan, S.H.; O’Toole, P.W.; Scott, K.P.; Flint, H.J. Polysaccharide utilization loci and nutritional specialization in a dominant group of butyrate-producing human colonic Firmicutes. Microb. Genom. 2016, 2. [Google Scholar] [CrossRef]
- Grondin, J.M.; Tamura, K.; Déjean, G.; Abbott, D.W.; Brumer, H. Polysaccharide utilization loci: Fueling microbial communities. J. Bacteriol. 2017, 199, e00860-16. [Google Scholar] [CrossRef] [PubMed]
- Sonnenburg, E.D.; Zheng, H.; Joglekar, P.; Higginbottom, S.K.; Firbank, S.J.; Bolam, D.N.; Sonnenburg, J.L. Specificity of polysaccharide use in intestinal bacteroides species determines diet-induced microbiota alterations. Cell 2010, 141, 1241–1252. [Google Scholar] [CrossRef]
- Schwalm, N.D.; Townsend, G.E.; Groisman, E.A. Multiple signals govern utilization of a polysaccharide in the gut bacterium Bacteroides thetaiotaomicron. mBio 2016, 7, e01342-16. [Google Scholar] [CrossRef]
- Tuncil, Y.E.; Xiao, Y.; Porter, N.T.; Reuhs, B.L.; Martens, E.C.; Hamaker, B.R. Reciprocal Prioritization to Dietary Glycans by Gut Bacteria in a Competitive Environment Promotes Stable Coexistence. mBio 2017, 8, e01068-17. [Google Scholar] [CrossRef]
- Porter, N.T.; Martens, E.C. The Critical Roles of Polysaccharides in Gut Microbial Ecology and Physiology. Annu. Rev. Microbiol. 2017, 71, 349–369. [Google Scholar] [CrossRef]
- Cockburn, D.W.; Suh, C.; Medina, K.P.; Duvall, R.M.; Wawrzak, Z.; Henrissat, B.; Koropatkin, N.M. Novel carbohydrate binding modules in the surface anchored alpha-amylase of Eubacterium rectale provide a molecular rationale for the range of starches used by this organism in the human gut. Mol. Microbiol. 2018, 107, 249–264. [Google Scholar] [CrossRef] [PubMed]
- Cockburn, D.W.; Orlovsky, N.I.; Foley, M.H.; Kwiatkowski, K.J.; Bahr, C.M.; Maynard, M.; Demeler, B.; Koropatkin, N.M. Molecular details of a starch utilization pathway in the human gut symbiont Eubacterium rectale. Mol. Microbiol. 2015, 95, 209–230. [Google Scholar] [CrossRef] [PubMed]
- Crost, E.H.; Tailford, L.E.; Le Gall, G.; Fons, M.; Henrissat, B.; Juge, N. Utilisation of Mucin Glycans by the Human Gut Symbiont Ruminococcus gnavus Is Strain-Dependent. PLoS ONE 2013, 8, e76341. [Google Scholar] [CrossRef] [PubMed]
- Porter, N.T.; Canales, P.; Peterson, D.A.; Martens, E.C. A Subset of Polysaccharide Capsules in the Human Symbiont Bacteroides thetaiotaomicron Promote Increased Competitive Fitness in the Mouse Gut. Cell Host Microbe 2017, 22, 494–506.e8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Scholl, D.; Adhya, S.; Merril, C. Escherichia coli K1’s capsule is a barrier to bacteriophage T7. Appl. Environ. Microbiol. 2005, 71, 4872–4874. [Google Scholar] [CrossRef] [PubMed]
- Whitfield, C. Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu. Rev. Biochem. 2006, 75, 39–68. [Google Scholar] [CrossRef]
- Tzianabos, A.O.; Onderdonk, A.B.; Rosner, B.; Cisneros, R.L.; Kasper, D.L. Structural features of polysaccharides that induce intra-abdominal abscesses. Science 1993, 262, 416–419. [Google Scholar] [CrossRef]
- Rios-Covian, D.; Cuesta, I.; Alvarez-Buylla, J.R.; Ruas-Madiedo, P.; Gueimonde, M.; Clara, G. Bacteroides fragilis metabolises exopolysaccharides produced by bifidobacteria. BMC Microbiol. 2016, 16, 150. [Google Scholar]
- Wang, Y.; Gänzle, M.G.; Schwab, C. Exopolysaccharide synthesized by Lactobacillus reuteri decreases the ability of enterotoxigenic Escherichia coli to bind to porcine erythrocytes. Appl. Environ. Microbiol. 2010, 76, 4863–4866. [Google Scholar] [CrossRef]
- Lammerts van Bueren, A.; Saraf, A.; Martens, E.C.; Dijkhuizen, L. Differential Metabolism of Exopolysaccharides from Probiotic Lactobacilli by the Human Gut Symbiont Bacteroides thetaiotaomicron. Appl. Environ. Microbiol. 2015, 81, 3973. [Google Scholar] [CrossRef]
- Yother, J. Capsules of Streptococcus pneumoniae and other bacteria: Paradigms for polysaccharide biosynthesis and regulation. Annu. Rev. Microbiol. 2011, 65, 563–581. [Google Scholar] [CrossRef] [PubMed]
- van Hijum, S.A.; Kralj, S.; Ozimek, L.K.; Dijkhuizen, L.; van Geel-Schutten, I.G. Structure-function relationships of glucansucrase and fructansucrase enzymes from lactic acid bacteria. Microbiol. Mol. Biol. Rev. 2006, 70, 157–176. [Google Scholar] [CrossRef] [PubMed]
- Coyne, M.J.; Chatzidaki-Livanis, M.; Paoletti, L.C.; Comstock, L.E. Role of glycan synthesis in colonization of the mammalian gut by the bacterial symbiont Bacteroides fragilis. Proc. Natl. Acad. Sci. USA 2008, 105, 13099–13104. [Google Scholar] [CrossRef] [PubMed]
- Martens, E.C.; Roth, R.; Heuser, J.E.; Gordon, J.I. Coordinate regulation of glycan degradation and polysaccharide capsule biosynthesis by a prominent human gut symbiont. J. Biol. Chem. 2009, 284, 18445–18457. [Google Scholar] [CrossRef] [PubMed]
- Vos, A.P.; M’Rabet, L.; Stahl, B.; Boehm, G.; Garssen, J. Immune-modulatory effects and potential working mechanisms of orally applied nondigestible carbohydrates. Crit. Rev. Immunol. 2007, 27, 97–140. [Google Scholar] [CrossRef] [PubMed]
- Macfarlane, G.T.; Steed, H.; Macfarlane, S. Bacterial metabolism and health-related effects of galacto-oligosaccharides and other prebiotics. J. Appl. Microbiol. 2008, 104, 305–344. [Google Scholar] [CrossRef] [PubMed]
- Leung, M.Y.K.; Liu, C.; Koon, J.C.M.; Fung, K.P. Polysaccharide biological response modifiers. Immunol. Lett. 2006, 105, 101–114. [Google Scholar] [CrossRef]
- Maverakis, E.; Kim, K.; Shimoda, M.; Gershwin, M.E.; Patel, F.; Wilken, R.; Raychaudhuri, S.; Ruhaak, L.R.; Lebrilla, C.B. Glycans in the immune system and The Altered Glycan Theory of Autoimmunity: A critical review. J. Autoimmun. 2015, 57, 1–13. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- van Kooyk, Y.; Rabinovich, G.A. Protein-glycan interactions in the control of innate and adaptive immune responses. Nat. Immunol. 2008, 9, 593. [Google Scholar] [CrossRef]
- García-Lora, A.; Martinez, M.; Pedrinaci, S.; Garrido, F. Different regulation of PKC isoenzymes and MAPK by PSK and IL-2 in the proliferative and cytotoxic activities of the NKL human natural killer cell line. Cancer Immunol. Immunother. 2003, 52, 59–64. [Google Scholar]
- Iliev, I.D.; Mileti, E.; Matteoli, G.; Chieppa, M.; Rescigno, M. Intestinal epithelial cells promote colitis-protective regulatory T-cell differentiation through dendritic cell conditioning. Mucosal Immunol. 2009, 2, 340. [Google Scholar] [CrossRef] [PubMed]
- Iliev, I.D.; Spadoni, I.; Mileti, E.; Matteoli, G.; Sonzogni, A.; Sampietro, G.M.; Foschi, D.; Caprioli, F.; Viale, G.; Rescigno, M. Human intestinal epithelial cells promote the differentiation of tolerogenic dendritic cells. Gut 2009, 58, 1481–1489. [Google Scholar] [CrossRef] [PubMed]
- Rios, D.; Wood, M.; Li, J.; Chassaing, B.; Gewirtz, A.; Williams, I. Antigen sampling by intestinal M cells is the principal pathway initiating mucosal IgA production to commensal enteric bacteria. Mucosal Immunol. 2016, 9, 907. [Google Scholar] [CrossRef] [PubMed]
- Terahara, K.; Nochi, T.; Yoshida, M.; Takahashi, Y.; Goto, Y.; Hatai, H.; Kurokawa, S.; Jang, M.H.; Kweon, M.-N.; Domino, S.E. Distinct fucosylation of M cells and epithelial cells by Fut1 and Fut2, respectively, in response to intestinal environmental stress. Biochem. Biophys. Res. Commun. 2011, 404, 822–828. [Google Scholar] [CrossRef] [PubMed]
- Johansson, M.E.V.; Hansson, G.C. Immunological aspects of intestinal mucus and mucins. Nat. Rev. Immunol. 2016, 16, 639. [Google Scholar] [CrossRef] [PubMed]
- Perdijk, O.; van Neerven, R.J.J.; van den Brink, E.; Savelkoul, H.F.J.; Brugman, S. The oligosaccharides 6′-sialyllactose, 2′-fucosyllactose or galactooligosaccharides do not directly modulate human dendritic cell differentiation or maturation. PLoS ONE 2018, 13, e200356. [Google Scholar] [CrossRef]
- Wang, Q.; McLoughlin, R.M.; Cobb, B.A.; Charrel-Dennis, M.; Zaleski, K.J.; Golenbock, D.; Tzianabos, A.O.; Kasper, D.L. A bacterial carbohydrate links innate and adaptive responses through Toll-like receptor 2. J. Exp. Med. 2006, 203, 2853. [Google Scholar] [CrossRef]
- Hickey, C.A.; Kuhn, K.A.; Donermeyer, D.L.; Porter, N.T.; Jin, C.; Cameron, E.A.; Jung, H.; Kaiko, G.E.; Wegorzewska, M.; Malvin, N.P. Colitogenic Bacteroides thetaiotaomicron antigens access host immune cells in a sulfatase-dependent manner via outer membrane vesicles. Cell Host Microbe 2015, 17, 672–680. [Google Scholar] [CrossRef]
- Chang, C.-J.; Lin, C.-S.; Martel, J.; Ojcius, D.M.; Lai, W.-F.; Lu, C.-C.; Ko, Y.-F.; Young, J.D.; Lai, H.-C. Modulation of host immune response by Bacteroides fragilis polysaccharides: A review of recent observations. J. Biomed. Lab. Sci. 2016, 28, 1. [Google Scholar]
- Wegorzewska, M.M.; Glowacki, R.W.P.; Hsieh, S.A.; Donermeyer, D.L.; Hickey, C.A.; Horvath, S.C.; Martens, E.C.; Stappenbeck, T.S.; Allen, P.M. Diet modulates colonic T cell responses by regulating the expression of Bacteroides thetaiotaomicron antigen. Sci. Immunol. 2019, 4, 9079. [Google Scholar] [CrossRef]
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
McKeen, S.; Young, W.; Fraser, K.; Roy, N.C.; McNabb, W.C. Glycan Utilisation and Function in the Microbiome of Weaning Infants. Microorganisms 2019, 7, 190. https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms7070190
McKeen S, Young W, Fraser K, Roy NC, McNabb WC. Glycan Utilisation and Function in the Microbiome of Weaning Infants. Microorganisms. 2019; 7(7):190. https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms7070190
Chicago/Turabian StyleMcKeen, Starin, Wayne Young, Karl Fraser, Nicole C. Roy, and Warren C. McNabb. 2019. "Glycan Utilisation and Function in the Microbiome of Weaning Infants" Microorganisms 7, no. 7: 190. https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms7070190