Microbiotas from UC patients display altered metabolism and reduced ability of LAB to colonize mucus

Scientific Reports

Volumn 3, Issue , 2013, Pages

  Vigsnaes, Louise Kristine ^a   Van Den Abbeele, Pieter ^b   Sulek, Karolina ^a   Frandsen, Henrik Lauritz ^a   Steenholdt, Casper ^c   Brynskov, Jørn ^c   Vermeiren, Joan ^b   Van De Wiele, Tom ^b   Licht, Tine Rask ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b GHENT UNIVERSITY   (Belgium)

^c GENTOFTE UNIVERSITY HOSPITAL   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

LACTIC ACID; MUCIN;

ARTICLE; BACTERIUM; FECES; GASTROINTESTINAL TRACT; GENETICS; HUMAN; INTESTINE MUCOSA; METABOLISM; METABOLOME; METAGENOME; MICROBIOLOGY; MUCUS; PHYSIOLOGY; ULCERATIVE COLITIS;

BACTERIA; COLITIS, ULCERATIVE; FECES; GASTROINTESTINAL TRACT; HUMANS; INTESTINAL MUCOSA; LACTIC ACID; METABOLOME; METAGENOME; MUCINS; MUCUS;

EID: 84873126693     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep01110     Document Type: Article

References (66)

1. Eckburg, P. B. et al. Diversity of the human intestinal microbial flora. Science 308, 1635-1638 (2005). (Pubitemid 40807514)
2. Zoetendal, E. G. et al. 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 (2002). (Pubitemid 34734038)
3. Johansson, M. E. V. et al. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc. Natl. Acad. Sci. U. S. A. 105, 15064-15069 (2008).
4. Killer, J. & Marounek, M. Fermentation of mucin by bifidobacteria from rectal samples of humans and rectal and intestinal samples of animals. Folia Microbiol. (Praha). 56, 85-89 (2011).
5. Kline, K. A., Falker, S., Dahlberg, S., Normark, S. & Henriques-Normark, B. Bacterial Adhesins inHost-Microbe Interactions. Cell Host&Microbe 5, 580-592 (2009).
6. Pretzer, G. et al. Biodiversity-based identification and functional characterization of the mannose-specific adhesin of Lactobacillus plantarum. J. Bacteriol. 187, 6128-6136 (2005). (Pubitemid 41262809)
7. Kornbluth, A. & Sachar, D. B. Ulcerative Colitis Practice Guidelines in Adults: American College of Gastroenterology, Practice Parameters Committee. Am. J. Gastroenterol. 105, 501-523 (2010).
8. Loftus, E. V. Clinical epidemiology of inflammatory bowel disease: Incidence, prevalence, and environmental influences. Gastroenterol 126, 1504-1517 (2004).
9. Sartor, R. B. Mechanisms of disease: pathogenesis of Crohn's disease and ulcerative colitis. Nat. Clin. Pract. Gastroenterol. Hepatol 3, 390-407 (2006). (Pubitemid 44018812)
10. Brown, S. J. & Mayer, L. The immune response in inflammatory bowel disease. Am. J. Gastroenterol. 102, 2058-2069 (2007). (Pubitemid 47301524)
11. Hanauer, S. B. Inflammatory bowel disease: epidemiology, pathogenesis, and therapeutic opportunities. Inflamm. Bowel. Dis. 12 Suppl 1, S3-S9 (2006). (Pubitemid 43068428)
12. Larsson, J. M. et al. Altered O-glycosylation profile of MUC2 mucin occurs in active ulcerative colitis and is associated with increased inflammation. Inflamm. Bowel Dis. 17, 2299-30 (2011).
13. Pullan, R. D. et al. Thickness of Adherent Mucus Gel on Colonic Mucosa in Humans and Its Relevance to Colitis. Gut 35, 353-359 (1994). (Pubitemid 24092905)
14. Frank, D. N. et al. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl. Acad. Sci. U. S. A. 104, 13780-13785 (2007). (Pubitemid 350003397)
15. Michail, S. et al. Alterations in the gut microbiome of children with severe ulcerative colitis. Inflamm. Bowel. Dis. 18, 1799-1808 (2012).
16. Qin,J. J. et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464, 59-70 (2010).
17. Sokol, H. et al. Low Counts of Faecalibacterium prausnitzii in Colitis Microbiota. Inflamm. Bowel Dis. 15, 1183-1189 (2009).
18. Takaishi, H. et al. Imbalance in intestinal microflora constitution could be involved in the pathogenesis of inflammatory bowel disease. Int. J. Med. Microbiol. 298, 463-472 (2008). (Pubitemid 351734793)
19. Ouwehand, A. C., Suomalainen, T., Tolkko, S. & Salminen, S. In vitro adhesion of propionic acid bacteria to human intestinal mucus. Lait 82, 123-130 (2002).
20. Van den Abbeele, P. et al. In vitro model to study the modulation of the mucinadhered bacterial community. Applied Microbiology and Biotechnology 83, 349-359 (2009).
21. Ouwehand, A. C. et al. Resected human colonic tissue: New model for characterizing adhesion of lactic acid bacteria. Clinical and Diagnostic Laboratory Immunology 9, 184-186 (2002). (Pubitemid 34084298)
22. Laparra, J.&Sanz, Y. Comparison of in vitro models to study bacterial adhesion to the intestinal epithelium. Letters in Applied Microbiology 49, 695-701 (2009).
23. Van den Abbeele, P. et al. Incorporating a mucosal environment in a dynamic gutmodel results in a more representative colonization by lactobacilli. Microbial Biotechnology 5, 106-115 (2011).
24. Van den Abbeele, P. et al.Microbial Community Development in a Dynamic Gut Model Is Reproducible, Colon Region Specific, and Selective for Bacteroidetes and Clostridium Cluster IX. Applied and Environmental Microbiology 76, 5237-5246 (2010).
25. Hong, P. Y., Croix, J. A., Greenberg, E., Gaskins, H. R. & Mackie, R. I. Pyrosequencing-Based Analysis of the Mucosal Microbiota in Healthy Individuals Reveals Ubiquitous Bacterial Groups and Micro-Heterogeneity. Plos One 6, e25042 (2011).
26. Nava, G. M., Friedrichsen, H. J. & Stappenbeck, T. S. Spatial organization of intestinal microbiota in the mouse ascending colon. Isme Journal 5, 627-638 (2011).
27. Vermeiren, J. et al. Decreased colonization of fecal Clostridium coccoides/Eubacterium rectale species from ulcerative colitis patients in an in vitro dynamic gut model with mucin environment. FEMS. Microbiol. Ecol 79, 685-696 (2012).
28. Van den Abbeele, P. et al. Butyrate-producing Clostridium cluster XIVa species specifically colonize mucus in an in vitro gut model. ISME J, in press(2012).
29. Derrien, M. et al. Modulation of Mucosal Immune Response, Tolerance, and Proliferation in Mice Colonized by the Mucin-Degrader Akkermansia muciniphila. Front Microbiol. 2, 1-14 (2011).
30. Van den Abbeele, P., Van de Wiele, T., Verstraete, W. & Possemiers, S. The host selects mucosal and luminal associations of coevolved gut microorganisms: a novel concept. FEMS Microbiol. Rev. 35, 681-704 (2011).
31. Gilad, O., Svensson, B., Viborg, A. H., Stuer-Lauridsen, B. & Jacobsen, S. The extracellular proteome of Bifidobacterium animalis subsp lactis BB-12 reveals proteins with putative roles in probiotic effects. Proteomics 11, 2503-2514 (2011).
32. Kankainen, M. et al. Comparative genomic analysis of Lactobacillus rhamnosus GG reveals pili containing a human-mucus binding protein. Proc. Natl. Acad. Sci. U. S. A. 106, 17193-17198 (2009).
33. Pridmore, R. D. et al. The genome sequence of the probiotic intestinal bacterium Lactobacillus johnsonii NCC 533. Proc. Natl. Acad. Sci. U. S. A. 101, 2512-2517 (2004). (Pubitemid 38269342)
34. Kleerebezem, M. et al. The extracellular biology of the lactobacilli. FEMS Microbiol. Rev. 34, 199-230 (2010).
35. Van Tassell, M. L. & Miller, M. J. Lactobacillus Adhesion to Mucus. Nutrients 3, 613-636 (2011).
36. Fooks, L. J. & Gibson, G. R. In vitro investigations of the effect of probiotics and prebiotics on selected human intestinal pathogens. FEMS. Microbiol. Ecol 39, 67-75 (2002). (Pubitemid 34214794)
37. Lee, J. H., Li, X. L. & O'Sullivan, D. J. Transcription Analysis of a Lantibiotic Gene Cluster from Bifidobacterium longum DJO10A. Applied and Environmental Microbiology 77, 5879-5887 (2011).
38. Saulnier, D. M. et al. Exploring Metabolic Pathway Reconstruction and Genome-Wide Expression Profiling in Lactobacillus reuteri to Define Functional Probiotic Features. Plos One 6, 1-14 (2011).
39. Chenoll, E. et al. Novel Probiotic Bifidobacterium bifidum CECT 7366 Strain Active against the Pathogenic Bacterium Helicobacter pylori. Applied and Environmental Microbiology 77, 1335-1343 (2011).
40. Collado, M. C., Meriluoto, J. & Salminen, S. In vitro analysis of probiotic strain combinations to inhibit pathogen adhesion to human intestinal mucus. Food. Res. Int. 40, 629-636 (2007). (Pubitemid 46575270)
41. Lee, Y. K., Puong, K. Y.,Ouwehand,A. C.&Salminen, S.Displacement of bacterial pathogens from mucus and Caco-2 cell surface by lactobacilli. Journal of Medical Microbiology 52, 925-930 (2003). (Pubitemid 37297325)
42. Hoarau, C., Lagaraine, C., Martin, L., Velge-Roussel, F. & Lebranchu, Y. Supernatant of Bifidobacterium breve induces dendritic cell maturation, activation, and survival through a Toll-like receptor 2 pathway. Journal of Allergy and Clinical Immunology 117, 696-702 (2006). (Pubitemid 43340238)
43. Zeuthen, L. H. et al. Lactobacillus acidophilus induces a slow but more sustained chemokine and cytokine response in naive foetal enterocytes compared to commensal Escherichia coli. BMC Immunol 11, 1-10 (2010).
44. Mylonaki, M., Rayment, N. B., Rampton, D. S., Hudspith, B. N. & Brostoff, J. Molecular characterization of rectal mucosa-associated bacterial flora in inflammatory bowel disease. Inflamm. Bowel Dis. 11, 481-487 (2005). (Pubitemid 40704083)
45. Vigsnaes, L. K., Brynskov, J., Steenholdt, C., Wilcks, A. & Licht, T. R. Gramnegative bacteria account for main differences between faecal microbiota from patients with ulcerative colitis and healthy controls. Benef. Microbes. 3, 287-97 (2012).
46. Macfarlane, S., Furrie, E., Cummings, J. H. &Macfarlane, G. T. Chemotaxonomic analysis of bacterial populations colonizing the rectal mucosa in patients with ulcerative colitis. Clin. Infect. Dis. 38, 1690-1699 (2004). (Pubitemid 38781660)
47. Flint, H. J., Duncan, S. H., Scott, K. P. & Louis, P. Interactions and competition within the microbial community of the human colon: links between diet and health. Environmental Microbiology 9, 1101-1111 (2007). (Pubitemid 46697267)
48. Jones, B. V., Begley, M., Hill, C., Gahan, C. G.M. & Marchesi, J. R. Functional and comparative metagenomic analysis of bile salt hydrolase activity in the human gut microbiome. Proc. Natl. Acad. Sci. U. S. A. 105, 13580-13585 (2008).
49. Ridlon, J.M., Kang, D. J. & Hylemon, P. B. Bile salt biotransformations by human intestinal bacteria. J. Lipid Res. 47, 241-259 (2006). (Pubitemid 43276911)
50. Doerner, K. C., Takamine, F., Lavoie, C. P., Mallonee, D. H. & Hylemon, P. B. Assessment of fecal bacteria with bile acid 7 alpha-dehydroxylating activity for the presence of bai-like genes. Appl. Environ. Microbiol. 63, 1185-1188 (1997). (Pubitemid 27098519)
51. Mcgarr, S. E., Ridlon, J. M.&Hylemon, P. B. Diet, anaerobic bacterial metabolism, and colon cancer-A review of the literature. J. Clin. Gastroenterol. 39, 98-109 (2005). (Pubitemid 40130020)
52. Smith, E.A.&Macfarlane, G. T. Formation of phenolic and indolic compounds by anaerobic bacteria in the human large intestine. Microb. Ecol. 33, 180-188 (1997). (Pubitemid 27191286)
53. Elsden, S. R., Hilton, M. G. & Waller,J.M. End Products of Metabolism of Aromatic Amino-Acids by Clostridia. Arch. Microbiol. 107, 283-288 (1976).
54. Smith, E. A. & Macfarlane, G. T. Enumeration of human colonic bacteria producing phenolic and indolic compounds: Effects of pH, carbohydrate availability and retention time on dissimilatory aromatic amino acid metabolism. J. Appl. Bacteriol. 81, 288-302 (1996).
55. Hengstermann, S. et al. Altered status of antioxidant vitamins and fatty acids in patients with inactive inflammatory bowel disease. Clin. Nutr. 27, 571-578 (2008).
56. Zocco, M. A. et al. Efficacy of Lactobacillus GG in maintaining remission of ulcerative colitis. Aliment. Pharmacol. Ther 23, 1567-1574 (2006). (Pubitemid 43727463)
57. Langholz, E., Munkholm, P., Davidsen, M. & Binder, V. Course of Ulcerative-Colitis-Analysis of Changes in Disease-Activity Over Years. Gastroenterol 107, 3-11 (1994). (Pubitemid 24195339)
58. Binder, V. A Comparison Between Clinical State, Macroscopic and Microscopic Appearances of Rectal Mucosa, and Cytologic Picture of Mucosal Exudate in Ulcerative Colitis. Scand. J. Gastroenterol. 5, 627-632 (1970).
59. Ott, S. J. et al. In vitro alterations of intestinal bacterial microbiota in fecal samples during storage. Diagn. Microbiol. Infect. Dis. 50, 237-245 (2004). (Pubitemid 39593146)
60. De Weirdt, R. et al. Human faecal microbiota display variable patterns of glycerol metabolism. FEMS. Microbiol. Ecol 74, 601-611 (2010).
61. Leser, T. D., Lindecrona, R. H., Jensen, T. K., Jensen, B. B. &Moller, K. Changes in bacterial community structure in the colon of pigs fed different experimental diets and after infection with Brachyspira hyodysenteriae. Appl. Environ.Microbiol. 66, 3290-3296 (2000). (Pubitemid 30624570)
62. Walter, J. et al. Detection and identification of gastrointestinal Lactobacillus species by using denaturing gradient gel electrophoresis and species-specific PCR primers. Appl. Environ. Microbiol. 66, 297-303 (2000). (Pubitemid 30030531)
63. Petersen, A. et al. Analysis of the intestinal microbiota of oligosaccharide fed mice exhibiting reduced resistance to Salmonella infection. Beneficial Microbes 3, 271-281 (2010).
64. Bernbom, N. et al. Comparison of methods and animal models commonly used for investigation of fecal microbiota: Effects of time, host and gender. J. Microbiol. Methods 66, 87-95 (2006). (Pubitemid 43786435)
65. Vigsnaes, L. K., Holck, J., Meyer, A. S. & Licht, T. R. In vitro fermentation of sugar beet arabino-oligosaccharides by fecal microbiota obtained from patients with ulcerative colitis to selectively stimulate the growth of Bifidobacterium spp. and Lactobacillus spp. Appl. Environ. Microbiol. 77, 8336-8344 (2011).
66. Bergstrom, A. et al. Introducing GUt Low-Density Array (GULDA)-a validated approach for qPCR-based intestinal microbial community analysis. FEMS Microbiol. Lett. 337, 38-47 (2012).