Genetic strategies for mucin metabolism in Bifidobacterium bifidum PRL2010: An example of possible human-microbe co-evolution

Gut Microbes

Volumn 2, Issue 3, 2011, Pages 183-189

  Turroni, Francesca ^a   Milani, Christian ^a   van Sinderen, Douwe ^b   Ventura, Marco ^a  

^a UNIVERSITY OF PARMA   (Italy)

^b UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

Bifidobacteria; Bifidobacterium; Co evolution; Genomics; Host glycans metabolism

Indexed keywords

GLYCOSIDASE; MONOSACCHARIDE; MUCIN;

ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; BIFIDOBACTERIUM BIFIDUM; GENETIC CONSERVATION; GENETIC VARIABILITY; GENOMICS; HYDROLYSIS; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN METABOLISM; PROTEIN STRUCTURE;

BACTERIAL PROTEINS; BIFIDOBACTERIUM; BIOLOGICAL EVOLUTION; GASTROINTESTINAL TRACT; GENOME, BACTERIAL; HUMANS; MUCINS; PHYLOGENY; POLYSACCHARIDES;

BIFIDOBACTERIUM; BIFIDOBACTERIUM BIFIDUM;

EID: 80051707062     PISSN: 19490976     EISSN: 19490984     Source Type: Journal    
DOI: 10.4161/gmic.2.3.16105     Document Type: Article

References (41)

1. Ventura M, O'Flaherty S, Claesson MJ, Turroni F, Klaenhammer TR, van Sinderen D, et al. Genomescale analyses of health-promoting bacteria: probiogenomics. Nat Rev Microbiol 2009; 7:61-71.
2. Guarner F, Malagelada JR. Gut flora in health and disease Lancet 2003; 361:512-9.
3. Backhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA 2004; 101:15718-23.
4. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006; 444:1027-31.
5. Frank DN, St. Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci USA 2007; 104:13780-5.
6. Kassinen A, Krogius-Kurikka L, Makivuokko H, Rinttila T, Paulin L, Corander J, et al. The fecal microbiota of irritable bowel syndrome patients differs significantly from that of healthy subjects. Gastroenterology 2007; 133:24-33.
7. Manichanh C, Rigottier-Gois L, Bonnaud E, Gloux K, Pelletier E, Frangeul L, et al. Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach. Gut 2006; 55:205-11.
8. Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. Host-bacterial mutualism in the human intestine. Science 2005; 307:1915-20.
9. Cerf-Bensussan N, Gaboriau-Routhiau V. The immune system and the gut microbiota: friends or foes? Nat Rev Immunol 2010; 10:735-44.
10. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, et al. Diversity of the human intestinal microbial flora. Science 2005; 308:1635-8.
11. Derrien M, van Passel MW, van de Bovenkamp JH, Schipper RG, de Vos WM, Dekker J. Mucin-bacterial interactions in the human oral cavity and digestive tract. Gut Microbes 2010; 1:254-68.
12. Podolsky DK. Oligosaccharide structures of human colonic mucin. J Biol Chem 1985; 260:8262-71.
13. Forstner OM, Sylvester FA. Production, structure and biologic relevance of gastrointestinal mucins. New York: Raven Press 1995.
14. Johansson ME, Phillipson M, Petersson J, Velcich A, Holm L, Hansson GC. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc Natl Acad Sci USA 2008; 105:15064-9.
15. Rabiu BA, Gibson GR. Carbohydrates: a limit on bacterial diversity within the colon. Biol Rev Camb Philos Soc 2002; 77:443-53.
16. Attene-Ramos MS, Nava GM, Muellner MG, Wagner ED, Plewa MJ, Gaskins HR. DNA damage and toxicogenomic analyses of hydrogen sulfide in human intestinal epithelial FHs 74 Int cells. Environ Mol Mutagen 2010; 51:304-14.
17. Midtvedt AC, Carlstedt-Duke B, Midtvedt T. Establishment of a mucin-degrading intestinal microflora during the first two years of human life. J Pediatr Gastroenterol Nutr 1994; 18:321-6.
18. Derrien M, Vaughan EE, Plugge CM, de Vos WM. Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol 2004; 54:1469-76.
19. Derrien M, Collado MC, Ben-Amor K, Salminen S, de Vos WM. The Mucin degrader Akkermansia muciniphila is an abundant resident of the human intestinal tract. Appl Environ Microbiol 2008; 74:1646-8.
20. Collado MC, Derrien M, Isolauri E, de Vos WM, Salminen S. Intestinal integrity and Akkermansia muciniphila, a mucin-degrading member of the intestinal microbiota present in infants, adults and the elderly. Appl Environ Microbiol 2007; 73:7767-70.
21. Turroni F, Bottacini F, Foroni E, Mulder I, Kim JH, Zomer A, et al. Genome analysis of Bifidobacterium bifidum PRL2010 reveals metabolic pathways for host-derived glycan foraging. Proc Natl Acad Sci USA 2010; 107:19514-9.
22. Caballero-Franco C, Keller K, De Simone C, Chadee K. The VSL#3 probiotic formula induces mucin gene expression and secretion in colonic epithelial cells. Am J Physiol Gastrointest Liver Physiol 2007; 292:315-22.
23. Dharmani P, Srivastava V, Kissoon-Singh V, Chadee K. Role of intestinal mucins in innate host defense mechanisms against pathogens. J Innate Immun 2009; 1:123-35.
24. Loesche WJ. Effect of bacterial contamination on cecal size and cecal contents of gnotobiotic rodents. J Bacteriol 1969; 99:520-6.
25. Kankainen M, Paulin L, Tynkkynen S, von Ossowski I, Reunanen J, Partanen P, et al. Comparative genomic analysis of Lactobacillus rhamnosus GG reveals pili containing a human-mucus binding protein. Proc Natl Acad Sci USA 2009; 106:17193-8.
26. Fujita K, Oura F, Nagamine N, Katayama T, Hiratake J, Sakata K, et al. Identification and molecular clonng of a novel glycoside hydrolase family of core 1 type O-glycan-specific endo-alpha-N-acetylgalactosaminidase from Bifidobacterium longum. J Biol Chem 2005; 280:37415-22.
27. Katayama T, Fujita K, Yamamoto K. Novel bifidobacterial glycosidases acting on sugar chains of mucin glycoproteins. J Biosci Bioeng 2005; 99:457-65.
28. Wada J, Ando T, Kiyohara M, Ashida H, Kitaoka M, Yamaguchi M, et al. Bifidobacterium bifidum lacto-N-biosidase, a critical enzyme for the degradation of human milk oligosaccharides with a type 1 structure. Appl Environ Microbiol 2008; 74:3996-4004.
29. Nishimoto M, Kitaoka M. Identification of N-acetylhexosamine 1-kinase in the complete lacto-N-biose I/galacto-N-biose metabolic pathway in Bifidobacterium longum. Appl Environ Microbiol 2007; 73:6444-9.
30. Turroni F, Foroni E, Pizzetti P, Giubellini V, Ribbera A, Merusi P, et al. Exploring the diversity of the bifidobacterial population in the human intestinal tract. Appl Environ Microbiol 2009; 75:1534-45.
31. Ventura M, Canchaya C, Tauch A, Chandra G, Fitzgerald GF, Chater KF, et al. Genomics of Actinobacteria: tracing the evolutionary history of an ancient phylum. Microbiol Mol Biol Rev 2007; 71:495-548.
32. Ruas-Madiedo P, Gueimonde M, Fernandez-Garcia M, de los Reyes-Gavilan CG, Margolles A. Mucin degradation by Bifidobacterium strains isolated from the human intestinal microbiota. Appl Environ Microbiol 2008; 74:1936-40.
33. Ruiz L, Gueimonde M, Coute Y, Salminen S, Sanchez JC, de los Reyes-Gavilan CG, et al. Evaluation of the ability of Bifidobacterium longum to metabolize human intestinal mucus. FEMS Microbiol Lett 2011; 314:125-30.
34. Salyers AA, West SE, Vercellotti JR, Wilkins TD. Fermentation of mucins and plant polysaccharides by anaerobic bacteria from the human colon. Appl Environ Microbiol 1977; 34:529-33.
35. Coutinho PM, Henrissat B. Life with no sugars? J Mol Microbiol Biotechnol 1999; 1:307-8.
36. Draper P, Kent PW. Biosynthesis of intestinal mucins. 4. Utilization of [1-C]glucose by sheep colonic mucosa in vitro. Biochem J 1963; 86:248-54.
37. Dean KJ, Sweeley CC. Studies on human liver alpha-galactosidases. I. Purification of alpha-galactosidase A and its enzymatic properties with glycolipid and oligosaccharide substrates. J Biol Chem 1979; 254:9994-10000.
38. Zhurina D, Zomer A, Gleinser M, Brancaccio VF, Auchter M, Waidmann MS, et al. Complete genome sequence of Bifidobacterium bifidum S17. J Bacteriol 2011; 193:301-2.
39. Turroni F, van Sinderen D, Ventura M. Genomics and ecological overview of the genus Bifidobacterium. Int J Food Microbiol 2010.
40. Ruas-Madiedo P, Medrano M, Salazar N, De Los Reyes-Gavilan CG, Perez PF, Abraham AG. Exopolysaccharides produced by Lactobacillus and Bifidobacterium strains abrogate in vitro the cytotoxic effect of bacterial toxins on eukaryotic cells. J Appl Microbiol 2010; 109:2079-86.
41. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 2009; 37:233-8.