Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism

Nature

Volumn 517, Issue 7533, 2015, Pages 165-169

  Cuskin, Fiona ^a,b   Lowe, Elisabeth C ^a   Temple, Max J ^a   Zhu, Yanping ^a,b   Cameron, Elizabeth A ^c   Pudlo, Nicholas A ^c   Porter, Nathan T ^c   Urs, Karthik ^c   Thompson, Andrew J ^d   Cartmell, Alan ^e   Rogowski, Artur ^a   Hamilton, Brian S ^f   Chen, Rui ^f   Tolbert, Thomas J ^g   Piens, Kathleen ^h   Bracke, Debby ^h   Vervecken, Wouter ^h   Hakki, Zalihe ^e   Speciale, Gaetano ^e   Munoz Munoz, Jose L ^a   Day, Andrew ^a   Peña, Maria J ^b   McLean, Richard ⁱ   Suits, Michael D ^j   Boraston, Alisdair B ^j   Atherly, Todd ^k   Ziemer, Cherie J ^k   Williams, Spencer J ^e   Davies, Gideon J ^d   Abbott, Wade D ⁱ   Martens, Eric C ^c   Gilbert, Harry J ^a,b   more..

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF GEORGIA   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF YORK   (United Kingdom)

^e UNIVERSITY OF MELBOURNE   (Australia)

^f INDIANA UNIVERSITY   (United States)

^g UNIVERSITY OF KANSAS   (United States)

^h Oxyrane Belgium NV   (Belgium)

ⁱ LETHBRIDGE RESEARCH CENTRE   (Canada)

^j UNIVERSITY OF VICTORIA   (Canada)

^k AGRICULTURAL RESEARCH SERVICE   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA MANNAN; ENZYME; GLYCAN; MANNAN; MANNOSE; OLIGOSACCHARIDE; POLYSACCHARIDE; UNCLASSIFIED DRUG; GLYCOPROTEIN;

BACTERIUM; BIOCHEMISTRY; DIET; GENE EXPRESSION; MICROBIOLOGY; POLYSACCHARIDE; SUGAR; YEAST;

ARTICLE; BACTERIAL STRAIN; BACTERIAL STRUCTURES; BACTEROIDES THETAIOTAOMICRON; CARBON SOURCE; CATABOLISM; CELL CULTURE; CELL SURFACE; CHEMICAL ANALYSIS; COCULTURE; CONTROLLED STUDY; CYTOPLASM; DEPOLYMERIZATION; DIET; ENZYMATIC DEGRADATION; GENE DISRUPTION; GRAM NEGATIVE BACTERIUM; INTESTINE FLORA; METABOLISM; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; YEAST; ANIMAL; BACTEROIDETES; BIOLOGICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; CYTOLOGY; ENZYMOLOGY; EVOLUTION; FEMALE; GASTROINTESTINAL TRACT; GENE LOCUS; GENETICS; GERMFREE ANIMAL; HUMAN; MALE; MICROBIOLOGY; MOUSE; PERIPLASM;

BACTEROIDES THETAIOTAOMICRON; BACTEROIDETES; EUKARYOTA; NEGIBACTERIA;

ANIMALS; BACTEROIDETES; BIOLOGICAL EVOLUTION; CARBOHYDRATE CONFORMATION; DIET; ENZYMES; FEMALE; GASTROINTESTINAL TRACT; GENETIC LOCI; GERM-FREE LIFE; GLYCOPROTEINS; HUMANS; MALE; MANNANS; MANNOSE; MICE; MODELS, BIOLOGICAL; MODELS, MOLECULAR; OLIGOSACCHARIDES; PERIPLASM; YEASTS;

EID: 84922629682     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature13995     Document Type: Article

References (24)

1. Arumugam, M. et al. Enterotypes of the human gut microbiome. Nature 473, 174-180 (2011).
2. Bäckhed, F., Ley, R. E., Sonnenburg, J. L., Peterson, D. A. & Gordon, J. I. Host-bacterial mutualism in the human intestine. Science 307, 1915-1920 (2005).
3. Arpaia, N. et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 504, 451-455 (2013).
4. Flint, H. J., Bayer, E. A., Rincon, M. T., Lamed, R. & White, B. A. Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nature Rev. Microbiol. 6, 121-131 (2008).
5. Kau, A. L., Ahern, P. P., Griffin, N. W., Goodman, A. L.&Gordon, J. I. Human nutrition, the gut microbiome and the immune system. Nature 474, 327-336 (2011).
6. Round, J. L. & Mazmanian, S. K. The gut microbiota shapes intestinal immune responses during health and disease. Nature Rev. Immunol. 9, 313-323 (2009).
7. Martens, E. C., Koropatkin, N. M., Smith, T. J. & Gordon, J. I. Complex glycan catabolism by the human gut microbiota: the Bacteroidetes Sus-like paradigm. J. Biol. Chem. 284, 24673-24677 (2009).
8. El Kaoutari, A., Armougom, F., Gordon, J. I., Raoult, D. & Henrissat, B. The abundance and variety of carbohydrate-active enzymes in the human gut microbiota. Nature Rev. Microbiol. 11, 497-504 (2013).
9. Lombard, V., Golaconda Ramulu, H., Drula, E., Coutinho, P. M. & Henrissat, B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42, D490-D495 (2014).
10. Konrad, A. et al. Immune sensitization to yeast antigens in ASCA-positive patients with Crohn's disease. Inflamm. Bowel Dis. 10, 97-105 (2004).
11. Mpofu, C. M. et al. Microbial mannan inhibits bacterial killing by macrophages: a possible pathogenic mechanism for Crohn's disease. Gastroenterology 133, 1487-1498 (2007).
12. Xu, J. et al. A genomic view of the human-Bacteroides thetaiotaomicron symbiosis. Science 299, 2074-2076 (2003).
13. Martens, E. C., Chiang, H. C. & Gordon, J. I. Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host Microbe 4, 447-457 (2008).
14. Ballou, C. E., Ballou, L. & Ball, G. Schizosaccharomyces pombe glycosylationmutant withalteredcell surfaceproperties.Proc.NatlAcad. Sci.USA91,9327-9331(1994).
15. Raschke, W. C., Kern, K. A.,Antalis, C.&Ballou, C. E. Genetic control of yeastmannan structure. Isolation and characterization of mannan mutants. J. Biol. Chem. 248, 4660-4666 (1973).
16. Gregg, K. J. et al. Analysis of a new family of widely distributed metal-independent alpha-mannosidases provides unique insight into the processing of N-linked glycans. J. Biol. Chem. 286, 15586-15596 (2011).
17. Zhu, Y. et al.Mechanistic insights into a Ca21-dependent family of a-mannosidases in a human gut symbiont. Nature Chem. Biol. 6, 125-132 (2010).
18. Rakoff-Nahoum, S., Coyne, M. J. & Comstock, L. E. An ecological network of polysaccharide utilization among human intestinal symbionts. Curr. Biol. 24, 40-49 (2014).
19. Ze, X., Duncan, S. H., Louis, P. & Flint, H. J. Ruminococcus bromii is a keystone species for the degradation of resistant starch in the human colon. ISME J. 6, 1535-1543 (2012).
20. Hehemann, J. H. et al. Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota. Nature 464, 908-912 (2010).
21. Larsbrink, J. et al. A discrete genetic locus confers xyloglucan metabolism in select human gut Bacteroidetes. Nature 506, 498-502 (2014).
22. 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. 426, 3851-3865 (2014).
23. Martens, E. C. et al. Recognition and degradation of plant cell wall polysaccharides by two human gut symbionts. PLoS Biol. 9, e1001221 (2011).
24. Everard, A., Matamoros, S., Geurts, L., Delzenne, N. M. & Cani, P. D. Saccharomyces boulardii administration changes gut microbiota and reduces hepatic steatosis, low-grade inflammation, and fat mass in obese and type 2 diabetic db/db mice. MBio. 5, e01011-e01014 (2014).