Utilisation of Mucin Glycans by the Human Gut Symbiont Ruminococcus gnavus Is Strain-Dependent

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Crost, Emmanuelle H ^a   Tailford, Louise E ^a   Le Gall, Gwenaelle ^a   Fons, Michel ^b   Henrissat, Bernard ^b,c   Juge, Nathalie ^a  

^a INSTITUTE OF FOOD RESEARCH   (United Kingdom)

^b AIX MARSEILLE UNIVERSITY   (France)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA LEVO FUCOSIDASE; CARBON; GLYCAN; GLYCOSIDASE; MONOSACCHARIDE; MUCIN; PROPANOL; PROPIONIC ACID; PROTEIN GH29; PROTEIN GH33; PROTEIN GH95; SIALIC ACID; SIALIDASE; UNCLASSIFIED DRUG;

ADAPTATION; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; CARBOHYDRATE METABOLISM; CARBON SOURCE; COMMENSAL; CONTROLLED STUDY; ENZYME SPECIFICITY; ENZYME SUBSTRATE; GENOMICS; HOST PATHOGEN INTERACTION; INTESTINE FLORA; MICROBIAL ACTIVITY; NONHUMAN; PROTEIN METABOLISM; RUMINOCOCCUS; RUMINOCOCCUS GNAVUS; SYMBIONT; TRANSCRIPTOMICS;

BASE SEQUENCE; CARBOHYDRATE METABOLISM; GASTROINTESTINAL TRACT; GENE ORDER; GENETIC LOCI; GENOME, BACTERIAL; HUMANS; METABOLOME; MOLECULAR SEQUENCE DATA; MUCINS; MULTIGENE FAMILY; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; POLYSACCHARIDES; RUMINOCOCCUS; SYMBIOSIS; TRANSCRIPTOME;

EID: 84886440497     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076341     Document Type: Article

References (69)

1. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, et al. (2005) Diversity of the human intestinal microbial flora. Science 308: 1635-1638.
2. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, et al. (2011) Enterotypes of the human gut microbiome. Nature 473: 174-180.
3. Human Microbiome Project Consortium (2012) Structure, function and diversity of the healthy human microbiome. Nature 486: 207-214.
4. Koropatkin NM, Cameron EA, Martens EC, (2012) How glycan metabolism shapes the human gut microbiota. Nat Rev Microbiol 10: 323-335.
5. Flint HJ, Scott KP, Louis P, Duncan SH, (2012) The role of the gut microbiota in nutrition and health. Nat Rev Gastroenterol Hepatol 9: 577-589.
6. Nyangale EP, Mottram DS, Gibson GR, (2012) Gut microbial activity, implications for health and disease: the potential role of metabolite analysis. J Proteome Res 11: 5573-5585.
7. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, et al. (2012) Human gut microbiome viewed across age and geography. Nature 486: 222-227.
8. Duboc H, Rajca S, Rainteau D, Benarous D, Maubert MA, et al. (2013) Connecting dysbiosis, bile-acid dysmetabolism and gut inflammation in inflammatory bowel diseases. Gut 62: 531-539.
9. Manichanh C, Borruel N, Casellas F, Guarner F, (2012) The gut microbiota in IBD. Nat Rev Gastroenterol Hepatol 9: 599-608.
10. Martinez C, Antolin M, Santos J, Torrejon A, Casellas F, et al. (2008) Unstable composition of the fecal microbiota in ulcerative colitis during clinical remission. Am J Gastroenterol 103: 643-648.
11. Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermúdez-Humarán LG, et al. (2008) Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci USA 105: 16731-16736.
12. Johansson ME, Ambort D, Pelaseyed T, Schütte A, Gustafsson JK, et al. (2011) Composition and functional role of the mucus layers in the intestine. Cell Mol Life Sci 68: 3635-3641.
13. Juge N, (2012) Microbial adhesins to gastrointestinal mucus. Trends Microbiol 20: 30-39.
14. Jensen PH, Kolarich D, Packer NH, (2010) Mucin-type O-glycosylation-putting the pieces together. FEBS J 277: 81-94.
15. Larsson JM, Karlsson H, Sjövall H, Hansson GC, (2009) A complex, but uniform O-glycosylation of the human MUC2 mucin from colonic biopsies analyzed by nanoLC/MSn. Glycobiology 19: 756-766.
16. Robbe C, Capon C, Coddeville B, Michalski JC, (2004) Structural diversity and specific distribution of O-glycans in normal human mucins along the intestinal tract. Biochem J 384: 307-316.
17. Zoetendal EG, von Wright A, Vilpponen-Salmela T, Ben-Amor K, Akkermans ADL, et al. (2002) Mucosa-associated bacteria in the human gastrointestinal tract are uniformly distributed along the colon and differ from the community recovered from feces. Appl Environ Microbiol 68: 3401-3407.
18. Nielsen DS, Møller PL, Rosenfeldt V, Paerregaard A, Michaelsen KF, et al. (2003) Case study of the distribution of mucosa-associated Bifidobacterium species, Lactobacillus species, and other lactic acid bacteria in the human colon. Appl Environ Microbiol 69: 7545-7548.
19. Lepage P, Seksik P, Sutren M, de la Cochetière MF, Jian R, et al. (2005) Biodiversity of the mucosa-associated microbiota is stable along the distal digestive tract in healthy individuals and patients with IBD. Inflamm Bowel Dis 11: 473-480.
20. Mackie RI, Sghir A, Gaskins HR, (1999) Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr 69: 1035S-1045S.
21. Lozupone CA, Hamady M, Cantarel BL, Coutinho PM, Henrissat B, et al. (2008) The convergence of carbohydrate active gene repertoires in human gut microbes. ProcNatl Acad Sci USA 10: 15076-15081.
22. Van den Abbeele P, Van de Wiele T, Verstraete W, Possemiers S, (2011) The host selects mucosal and luminal associations of coevolved gut microorganisms: a novel concept. FEMS Microbiol Rev 35: 681-704.
23. Ludwig W, Schleifer KH, Whitman WB (2009) Revised road map to the phylum Firmicutes. In: Bergey's Manual of Systematic Bacteriology, 2nd ed., vol. 3 (The Firmicutes) (P. De Vos, G. Garrity, D. Jones, N.R. Krieg, W. Ludwig, F.A. Rainey, K.-H. Schleifer, and W.B. Whitman, eds.), Springer-Verlag, New York. pp. 1-13.
24. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, et al. (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464: 59-65.
25. Favier CF, de Vos WM, Akkermans AD, (2003) Development of bacterial and bifidobacterial communities in feces of newborn babies. Anaerobe 9: 219-229.
26. Hattori M, Taylor TD, (2009) The human intestinal microbiome: a new frontier of human biology. DNA Res 16: 1-12.
27. Willing BP, Dicksved J, Halfvarson J, Andersson AF, Lucio M, et al. (2010) A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology 139: 1844-1854.
28. Joossens M, Huys G, Cnockaert M, De Preter V, Verbeke K, et al. (2011) Dysbiosis of the faecal microbiota in patients with Crohn's disease and their unaffected relatives. Gut 60: 631-637.
29. Prindiville T, Cantrell M, Wilson KH, (2004) Ribosomal DNA sequence analysis of mucosa-associated bacteria in Crohn's disease. Inflamm Bowel Dis 10: 824-833.
30. Png CW, Lindén SK, Gilshenan KS, Zoetendal EG, McSweeney CS, et al. (2010) Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria. Am J Gastroenterol 105: 2420-2428.
31. Nishikawa J, Kudo T, Sakata S, Benno Y, Sugiyama T, (2009) Diversity of mucosa-associated microbiota in active and inactive ulcerative colitis. Scand J Gastroenterol 44: 180-186.
32. Gunning AP, Kirby AR, Fuell C, Pin C, Tailford LE, et al. (2013) Mining the "glycocode"-exploring the spatial distribution of glycans in gastrointestinal mucin using force spectroscopy. FASEB J 27: 2342-2354.
33. Ramare F, Nicoli J, Dabard J, Corring T, Ladire M, et al. (1993) Trypsin-dependent production of an antibacterial substance by a human Peptostreptococcus strain in gnotobiotic rats and in vitro. Appl Environ Microbiol 59: 2876-2883.
34. Dabard J, Bridonneau C, Phillipe C, Anglade P, Molle D, et al. (2001) Ruminococcin A, a new lantibiotic produced by a Ruminococcus gnavus strain isolated from human feces. Appl Environ Microbiol 67: 4111-4118.
35. Moore WE, Holdeman LV, (1974) Special problems associated with the isolation and identification of intestinal bacteria in fecal flora studies. Am J Clin Nutr 27: 1450-1455.
36. Duncan SH, Hold GL, Harmsen HJ, Stewart CS, Flint HJ, (2002) Growth requirements and fermentation products of Fusobacterium prausnitzii, and a proposal to reclassify it as Faecalibacterium prausnitzii gen. nov., comb. nov. Int J Syst Evol Microbiol 52: 2141-2146.
37. Lopez-Siles M, Khan TM, Duncan SH, Harmsen HJ, Garcia-Gil LJ, et al. (2012) Cultured representatives of two major phylogroups of human colonic Faecalibacterium prausnitzii can utilize pectin, uronic acids, and host-derived substrates for growth. Appl Environ Microbiol 78: 420-428.
38. Baranyi J, Roberts TA (2000) Principles and Application of Predictive Modeling of the Effects of Preservative Factors on Microorganisms. In: Lund BM, Baird-Parker TC, Gould GW, editors. The Microbiological Safety and Quality of Food. Aspen Publishers, Inc. pp. 342-358.
39. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, et al. (2009) The carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 37: D233-D238.
40. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
41. Eddy SR, (1998) Profile hidden Markov models. Bioinformatics 14: 755-763.
42. Cervera-Tison M, Tailford LE, Fuell C, Bruel L, Sulzenbacher G, et al. (2012) Functional analysis of family GH36 α-galactosidases from Ruminococcus gnavus E1: insights into the metabolism of a plant oligosaccharide by a human gut symbiont. Appl Environ Microbiol 78: 7720-7732.
43. Ficko-Blean E, Boraston AB, (2012) Insights into the recognition of the human glycome by microbial carbohydrate-binding modules. Curr Opin Struct Biol 22: 570-577.
44. Nishimoto M, Kitaoka M, (2007) Identification of N-acetylhexosamine 1-kinase in the complete lacto-N-biose I/galacto-N-biose metabolic pathway in Bifidobacterium longum. Appl Environ Microbiol 73: 6444-6449.
45. Henrissat B, Davies G, (1997) Structural and sequence-based classification of glycoside hydrolases. Curr OpinStruct Biol 7: 637-644.
46. Miwa M, Horimoto T, Kiyohara M, Katayama T, Kitaoka M, et al. (2010) Cooperation of β-galactosidase and β-N-acetylhexosaminidase from bifidobacteria in assimilation of human milk oligosaccharides with type 2 structure. Glycobiology 20: 1402-1409.
47. Wada J, Ando T, Kiyohara M, Ashida H, Kitaoka M, et al. (2008) Bifidobacterium bifidum lacto-N-biosidase, a critical enzyme for the degradation of human milk oligosaccharides with a type 1 structure. Appl Environ Microbiol 74: 3996-4004.
48. Kiyohara M, Nakatomi T, Kurihara S, Fushinobu S, Suzuki H, et al. (2012) α-N-acetylgalactosaminidase from infant-associated bifidobacteria belonging to novel glycoside hydrolase family 129 is implicated in alternative mucin degradation pathway. J Biol Chem 287: 693-700.
49. Yoshida E, Sakurama H, Kiyohara M, Nakajima M, Kitaoka M, et al. (2012) Bifidobacterium longum subsp. infantis uses two different β-galactosidases for selectively degrading type-1 and type-2 human milk oligosaccharides. Glycobiology 22: 361-368.
50. Dethlefsen L, Eckburg PB, Bik EM, Relman DA, (2006) Assembly of the human intestinal microbiota. Trends Ecol Evol 21: 517-523.
51. Hoskins LC, Agustines M, McKee WB, Boulding ET, Kriaris M, et al. (1985) Mucin degradation in human colon ecosystems. Isolation and properties of fecal strains that degrade ABH blood group antigens and oligosaccharides from mucin glycoproteins. J Clin Invest 75: 944-953.
52. Corfield AP, Wagner SA, Clamp JR, Kriaris MS, Hoskins LC, (1992) Mucin degradation in the human colon: production of sialidase, sialate O-acetylesterase, N-acetylneuraminate lyase, arylesterase, and glycosulfatase activities by strains of fecal bacteria. Infect Immun 60: 3971-3978.
53. Scott KP, Martin JC, Campbell G, Mayer CD, Flint HJ, (2006) Whole-genome transcription profiling reveals genes up-regulated by growth on fucose in the human gut bacterium "Roseburia inulinivorans". J Bacteriol 188: 4340-4349.
54. Almagro-Moreno S, Boyd EF, (2009) Insights into the evolution of sialic acid catabolism among bacteria. BMC Evol Biol 9: 118.
55. Li YT, Nakagawa H, Ross SA, Hansson GC, Li SC, (1990) A novel sialidase which releases 2,7-anhydro-alpha-N-acetylneuraminic acid from sialoglycoconjugates. J Biol Chem 265: 21629-21633.
56. Furuhata K, Takeda K, Ofura H, (1991) Studies on sialic acids XXIV. Synthesis of 2,7-nahydro-N-acetylneuraminic acid. Chem Pharm Bull 39: 817-819.
57. Derrien M, van Passel MW, van de Bovenkamp JH, Schipper RG, de Vos WM, et al. (2010) Mucin-bacterial interactions in the human oral cavity and digestive tract. Gut Microbes 1: 254-268.
58. Martens EC, Chiang HC, Gordon JI, (2008) Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host Microbe 4: 447-457.
59. Martens EC, Lowe EC, Chiang H, Pudlo NA, Wu M, et al. (2011) Recognition and degradation of plant cell wall polysaccharides by two human gut symbionts. PLoS Biol 9: e1001221.
60. Marcobal A, Barboza M, Sonnenburg ED, Pudlo N, Martens EC, et al. (2011) Bacteroides in the infant gut consume milk oligosaccharides via mucus-utilization pathways. Cell Host Microbe 10: 507-514.
61. Turroni F, Bottacini F, Foroni E, Mulder I, Kim JH, et al. (2010) Genome analysis of Bifidobacterium bifidum PRL2010 reveals metabolic pathways for host-derived glycan foraging. Proc Natl Acad Sci U S A 107: 19514-19519.
62. van Passel MW, Kant R, Zoetendal EG, Plugge CM, Derrien M, et al. (2011) The genome of Akkermansia muciniphila, a dedicated intestinal mucin degrader, and its use in exploring intestinal metagenomes. PLoS One 6: e16876.
63. Katayama T, Sakuma A, Kimura T, Makimura Y, Hiratake J, et al. (2004) Molecular cloning and characterization of Bifidobacterium bifidum 1,2-alpha-L-fucosidase (AfcA), a novel inverting glycosidase (glycoside hydrolase family 95). J Bacteriol 186: 4885-4893.
64. Ashida H, Miyake A, Kiyohara M, Wada J, Yoshida E, et al. (2009) Two distinct alpha-L-fucosidases from Bifidobacterium bifidum are essential for the utilization of fucosylated milk oligosaccharides and glycoconjugates. Glycobiology 19: 1010-1017.
65. Vimr ER, Kalivoda KA, Deszo EL, Steenbergen SM, (2004) Diversity of microbial sialic acid metabolism. Microbiol Mol Biol Rev 68: 132-153.
66. Lewis AL, Lewis WG, (2012) Host sialoglycans and bacterial sialidases: a mucosal perspective. Cell Microbiol 14: 1174-1182.
67. Chou MY, Li SC, Li YT, (1996) Cloning and expression of sialidase L, a NeuAcalpha2→3Gal-specific sialidase from the leech, Macrobdella decora. J Biol Chem 271: 19219-192224.
68. Gut H, King SJ, Walsh MA, (2008) Structural and functional studies of Streptococcus pneumoniae neuraminidase B: An intramolecular trans-sialidase. FEBS Lett 582: 3348-3352.
69. Tannock GW, Lawley B, Munro K, Gowri Pathmanathan S, Zhou SJ, et al. (2013) Comparison of the compositions of the stool microbiotas of infants fed goat milk formula, cow milk-based formula, or breast milk. Appl Environ Microbiol 79: 3040-3048.