Bifidobacterium breve UCC2003 surface exopolysaccharide production is a beneficial trait mediating commensal-host interaction through immune modulation and pathogen protection

Gut Microbes

Volumn 3, Issue 5, 2012, Pages 420-425

  Fanning, Saranna ^a,b,c   Hall, Lindsay J ^a,d   van Sinderen, Douwe ^a,b  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

^c CARNEGIE MELLON UNIVERSITY   (United States)

^d UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

B cells; Capsule; EPS; Genetics; Host bacteria interactions; Immunology; Microbiology; Molecular microbiology; Persistence; Phase variation; Probiotic

Indexed keywords

ACID; EXOPOLYSACCHARIDE; PROBIOTIC AGENT; BACTERIAL POLYSACCHARIDE; IMMUNOLOGIC FACTOR;

ADAPTIVE IMMUNITY; ARTICLE; B LYMPHOCYTE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BIFIDOBACTERIUM BREVE; BILE; BIOSYNTHESIS; CITROBACTER RODENTIUM; COMMENSAL; GENE CLUSTER; HOST PATHOGEN INTERACTION; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOSTIMULATION; INTESTINE FLORA; NONHUMAN; PHENOTYPE; PROMOTER REGION; TRANSCRIPTION REGULATION; WILD TYPE; ANIMAL; ANTIBIOSIS; BIFIDOBACTERIUM; GASTROINTESTINAL TRACT; GENE EXPRESSION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; IMMUNE EVASION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MULTIGENE FAMILY; PATHOGENICITY; REVIEW;

BIFIDOBACTERIUM BREVE; CITROBACTER RODENTIUM;

ANIMALS; ANTIBIOSIS; BIFIDOBACTERIUM; CITROBACTER RODENTIUM; GASTROINTESTINAL TRACT; GENE EXPRESSION; HUMANS; IMMUNE EVASION; IMMUNOLOGIC FACTORS; MULTIGENE FAMILY; POLYSACCHARIDES, BACTERIAL; PROMOTER REGIONS, GENETIC;

EID: 85046982764     PISSN: 19490976     EISSN: 19490984     Source Type: Journal    
DOI: 10.4161/gmic.20630     Document Type: Article

References (57)

1. Stainier DY. No organ left behind: tales of gut development and evolution. Science 2005; 307:1902-4. PMID:15790841; http://dx.doi.org/10.1126/science. 1108709.
2. Garrett WS, Gordon JI, Glimcher LH. Homeostasis and inf lammation in the intestine. Cell 2010; 140:859-70. PMID:20303876; http://dx.doi.org/10.1016/j.cell.2010.01.023.
3. Gill SR, Pop M, Deboy RT, Eckburg PB, Turnbaugh PJ, Samuel BS, et al. Metagenomic analysis of the human distal gut microbiome. Science 2006; 312:1355-9. PMID:16741115; http://dx.doi. org/10.1126/science.1124234.
4. Claesson MJ, Cusack S, O'Sullivan O, Greene-Diniz R, de Weerd H, Flannery E, et al. Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proc Natl Acad Sci USA 2011; 108:4586-91. PMID:20571116; http://dx.doi. org/10.1073/pnas.1000097107.
5. Turnbaugh PJ, Quince C, Faith JJ, McHardy AC, Yatsunenko T, Niazi F, et al. Organismal, genetic, and transcriptional variation in the deeply sequenced gut microbiomes of identical twins. Proc Natl Acad Sci USA 2010; 107:7503-8. PMID:20363958; http:// dx.doi.org/10.1073/pnas.1002355107.
6. Hooper LV. Bacterial contributions to mammalian gut development. Trends Microbiol 2004; 12:129-34. PMID:15001189; http://dx.doi.org/10.1016/j. tim.2004.01.001.
7. Gilmore MS, Ferretti JJ. Microbiology. The thin line between gut commensal and pathogen. Science 2003; 299:1999-2002. PMID:12663906; http://dx.doi.org/10.1126/science.1083534.
8. Fanaro S, Chierici R, Guerrini P, Vigi V. Intestinal microflora in early infancy: composition and development. Acta Paediatr Suppl 2003; 91:48-55. PMID:14599042.
9. Turroni F, van Sinderen D, Ventura M. Bifidobacteria: from ecology to genomics. Front Biosci 2009; 14:4673-84. PMID:19273381; http:// dx.doi.org/10.2741/3559.
10. Zwielehner J, Liszt K, Handschur M, Lassl C, Lapin A, Haslberger AG. Combined PCR-DGGE fingerprinting and quantitative-PCR indicates shifts in fecal population sizes and diversity of Bacteroides, bifidobacteria and Clostridium cluster IV in institutionalized elderly. Exp Gerontol 2009; 44:440-6. PMID:19376217; http://dx.doi.org/10.1016/j. exger.2009.04.002.
11. Biagi E, Nylund L, Candela M, Ostan R, Bucci L, Pini E, et al. Through ageing, and beyond: gut microbiota and inflammatory status in seniors and centenarians. PLoS One 2010; 5:10667. PMID:20498852; http://dx.doi.org/10.1371/journal.pone.0010667.
12. Nicholson JK, Holmes E, Wilson ID. Gut microorganisms, mammalian metabolism and personalized health care. Nat Rev Microbiol 2005; 3:431-8. PMID:15821725; http://dx.doi.org/10.1038/nrmicro1152.
13. Vijay-Kumar M, Aitken JD, Carvalho FA, Cullender TC, Mwangi S, Srinivasan S, et al. Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5. Science 2010; 328:228-31. PMID:20203013; http://dx.doi.org/10.1126/science. 1179721.
14. Camilleri M. Probiotics and irritable bowel syndrome: rationale, putative mechanisms, and evidence of clinical efficacy. J Clin Gastroenterol 2006; 40:264-9. PMID:16633134; http://dx.doi. org/10.1097/00004836-200603000-00020.
15. Tanabe S, Kinuta Y, Saito Y. Bifidobacterium infantis suppresses proinflammatory interleukin-17 production in murine splenocytes and dextran sodium sulfate-induced intestinal inflammation. Int J Mol Med 2008; 22:181-5. PMID:18636171.
16. Chouraqui JP, Van Egroo LD, Fichot MC. Acidified milk formula supplemented with Bifidobacterium lactis: impact on infant diarrhea in residential care settings. J Pediatr Gastroenterol Nutr 2004; 38:288-92. PMID:15076628; http://dx.doi. org/10.1097/00005176-200403000-00011.
17. Kim Y, Lee D, Kim D, Cho J, Yang J, Chung M, et al. Inhibition of proliferation in colon cancer cell lines and harmful enzyme activity of colon bacteria by Bifidobacterium adolescentis SPM0212. Arch Pharm Res 2008; 31:468-73. PMID:18449504; http:// dx.doi.org/10.1007/s12272-001-1180-y.
18. Sreekumar O, Hosono A. The antimutagenic properties of a polysaccharide produced by Bifidobacterium longum and its cultured milk against some heterocyclic amines. Can J Microbiol 1998; 44:1029-36. PMID:10029998.
19. Nikkilä J, de Vos WM. Advanced approaches to characterize the human intestinal microbiota by computational meta-analysis. J Clin Gastroenterol 2010; 44:2-5. PMID:20616744; http://dx.doi. org/10.1097/MCG.0b013e3181e5018f.
20. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, et al.; MetaHIT Consortium. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010; 464:59-65. PMID:20203603; http://dx.doi.org/10.1038/ nature08821.
21. Booijink CC, El-Aidy S, Rajilic-Stojanovic M, Heilig HG, Troost FJ, Smidt H, et al. High temporal and inter-individual variation detected in the human ileal microbiota. Environ Microbiol 2010; 12:3213-27. PMID:20626454; http://dx.doi.org/10.1111/j.1462- 2920.2010.02294.x.
22. Mariat D, Firmesse O, Levenez F, Guimaraes V, Sokol H, Doré J, et al. The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol 2009; 9:123. PMID:19508720; http://dx.doi.org/10.1186/1471-2180-9-123.
23. Salazar N, Ruas-Madiedo P, Kolida S, Collins M, Rastall R, Gibson G, et al. Exopolysaccharides produced by Bifidobacterium longum IPLA E44 and Bifidobacterium animalis subsp lactis IPLA R1 modify the composition and metabolic activity of human faecal microbiota in pH-controlled batch cultures. Int J Food Microbiol 2009; 135:260-7. PMID:19735956; http://dx.doi.org/10.1016/j.ijfoodmicro. 2009.08.017.
24. Sánchez JI, Martínez B, Guillén R, Jiménez-Díaz R, Rodríguez A. Culture conditions determine the balance between two different exopolysaccharides produced by Lactobacillus pentosus LPS26. Appl Environ Microbiol 2006; 72:7495-502. PMID:17012595; http://dx.doi.org/10.1128/AEM.01078-06.
25. Myszka K, Czaczyk K. Characterization of adhesive exopolysaccharide (EPS) produced by Pseudomonas aeruginosa under starvation conditions. Curr Microbiol 2009; 58:541-6. PMID:19194748; http:// dx.doi.org/10.1007/s00284-009-9365-3.
26. Tamaru Y, Takani Y, Yoshida T, Sakamoto T. Crucial role of extracellular polysaccharides in desiccation and freezing tolerance in the terrestrial cyanobacterium Nostoc commune. Appl Environ Microbiol 2005; 71:7327-33. PMID:16269775; http://dx.doi. org/10.1128/AEM.71.11.7327-33.2005.
27. Ozturk S, Aslim B. Modification of exopolysaccharide composition and production by three cyanobacterial isolates under salt stress. Environ Sci Pollut Res Int 2010; 17:595-602. PMID:19727881; http:// dx.doi.org/10.1007/s11356-009-0233-2.
28. Vinderola G, Perdigón G, Duarte J, Farnworth E, Matar C. Effects of the oral administration of the exopolysaccharide produced by Lactobacillus kefiranofaciens on the gut mucosal immunity. Cytokine 2006; 36:254-60. PMID:17363262; http://dx.doi. org/10.1016/j.cyto.2007.01.003.
29. Xu CL, Wang YZ, Jin ML, Yang XQ. Preparation, characterization and immunomodulatory activity of selenium-enriched exopolysaccharide produced by bacterium Enterobacter cloacae Z0206. Bioresour Technol 2009; 100:2095-7. PMID:19056259; http://dx.doi.org/10.1016/j.biortech.2008.10.037.
30. Grijpstra J, Gerwig GJ, Wösten H, Kamerling JP, de Cock H. Production of extracellular polysaccharides by CAP mutants of Cryptococcus neoformans. Eukaryot Cell 2009; 8:1165-73. PMID:19542308; http://dx.doi.org/10.1128/EC.00013-09.
31. Dan T, Fukuda K, Sugai-Bannai M, Takakuwa N, Motoshima H, Urashima T. Characterization and expression analysis of the exopolysaccharide gene cluster in Lactobacillus fermentum TDS030603. Biosci Biotechnol Biochem 2009; 73:2656-64. PMID:19966483; http://dx.doi.org/10.1271/ bbb.90502.
32. Dabour N, LaPointe G. Identification and molecular characterization of the chromosomal exopolysaccharide biosynthesis gene cluster from Lactococcus lactis subsp cremoris SMQ-461. Appl Environ Microbiol 2005; 71:7414-25. PMID:16269783; http://dx.doi. org/10.1128/AEM.71.11.7414-25.2005.
33. Fanning S, Hall LJ, Cronin M, Zomer A, MacSharry J, Goulding D, et al. Bifidobacterial surface-exopolysaccharide facilitates commensal-host interaction through immune modulation and pathogen protection. Proc Natl Acad Sci USA 2012; 109:2108-13. PMID:22308390; http://dx.doi.org/10.1073/ pnas.1115621109.
34. Chapot-Chartier MP, Vinogradov E, Sadovskaya I, Andre G, Mistou MY, Trieu-Cuot P, et al. Cell surface of Lactococcus lactis is covered by a protective polysaccharide pellicle. J Biol Chem 2010; 285:10464-71. PMID:20106971; http://dx.doi. org/10.1074/jbc.M109.082958.
35. Lebeer S, Verhoeven TL, Francius G, Schoofs G, Lambrichts I, Dufrêne Y, et al. Identification of a Gene Cluster for the Biosynthesis of a Long, Galactose-Rich Exopolysaccharide in Lactobacillus rhamnosus GG and Functional Analysis of the Priming Glycosyltransferase. Appl Environ Microbiol 2009; 75:3554-63. PMID:19346339; http://dx.doi. org/10.1128/AEM.02919.
36. Videira PA, Garcia AP, Sá-Correia I. Functional and topological analysis of the Burkholderia cenocepacia priming glucosyltransferase BceB, involved in the biosynthesis of the cepacian exopolysaccharide. J Bacteriol 2005; 187:5013-8. PMID:15995219; http://dx.doi.org/10.1128/JB.187.14.5013-8.2005.
37. van Kranenburg R, van Swam II, Marugg JD, Kleerebezem M, de Vos WM. Exopolysaccharide biosynthesis in Lactococcus lactis NIZO B40: functional analysis of the glycosyltransferase genes involved in synthesis of the polysaccharide backbone. J Bacteriol 1999; 181:338-40. PMID:9864348.
38. Breedveld M, Bonting K, Dijkhuizen L. Mutational analysis of exopolysaccharide biosynthesis by Lactobacillus sakei 0-1. FEMS Microbiol Lett 1998; 169:241-9. PMID:9868768.
39. Audy J, Labrie S, Roy D, Lapointe G. Sugar source modulates exopolysaccharide biosynthesis in Bifidobacterium longum subsp longum CRC 002. Microbiology 2010; 156:653-64. PMID:19850611; http://dx.doi.org/10.1099/mic.0.033720-0.
40. Chatzidaki-Livanis M, Coyne MJ, Roche-Hakansson H, Comstock LE. Expression of a uniquely regulated extracellular polysaccharide confers a largecapsule phenotype to Bacteroides fragilis. J Bacteriol 2008; 190:1020-6. PMID:18039760; http://dx.doi. org/10.1128/JB.01519-07.
41. Alp G, Aslim B. Relationship between the resistance to bile salts and low pH with exopolysaccharide (EPS) production of Bifidobacterium spp isolated from infants feces and breast milk. Anaerobe 2010; 16:101-5. PMID:19576995; http://dx.doi.org/10.1016/j. anaerobe.2009.06.006.
42. Salazar N, Gueimonde M, Hernández-Barranco AM, Ruas-Madiedo P, de los Reyes-Gavilán CG. Exopolysaccharides produced by intestinal Bifidobacterium strains act as fermentable substrates for human intestinal bacteria. Appl Environ Microbiol 2008; 74:4737-45. PMID:18539803; http://dx.doi.org/10.1128/AEM.00325-08.
43. O'Connell Motherway M, Zomer A, Leahy SC, Reunanen J, Bottacini F, Claesson MJ, et al. Functional genome analysis of Bifidobacterium breve UCC2003 reveals type IVb tight adherence (Tad) pili as an essential and conserved host-colonization factor. Proc Natl Acad Sci USA 2011; 108:11217-22. PMID:21690406; http://dx.doi.org/10.1073/ pnas.1105380108.
44. Conover MS, Sloan GP, Love CF, Sukumar N, Deora R. The Bps polysaccharide of Bordetella pertussis promotes colonization and biofilm formation in the nose by functioning as an adhesin. Mol Microbiol 2010; 77:1439-55. PMID:20633227; http://dx.doi. org/10.1111/j.1365-2958.2010.07297.x.
45. Coyne MJ, Chatzidaki-Livanis M, Paoletti LC, Comstock LE. Role of glycan synthesis in colonization of the mammalian gut by the bacterial symbiont Bacteroides fragilis. Proc Natl Acad Sci USA 2008; 105:13099-104. PMID:18723678; http://dx.doi. org/10.1073/pnas.0804220105.
46. Merino S, Tomás JM. Bacterial Capsules and Evasion of Immune Responses. John Wiley & Sons, Ltd. 2010.
47. Hyams C, Yuste J, Bax K, Camberlein E, Weiser JN, Brown JS. Streptococcus pneumoniae resistance to complement-mediated immunity is dependent on the capsular serotype. Infect Immun 2010; 78:716-25. PMID:19948838; http://dx.doi.org/10.1128/ IAI.01056-09.
48. Weintraub A. Immunology of bacterial polysaccharide antigens. Carbohydr Res 2003; 338:2539-47. PMID:14670715; http://dx.doi.org/10.1016/j. carres.2003.07.008.
49. Mond JJ, Vos Q, Lees A, Snapper CM. T cell independent antigens. Curr Opin Immunol 1995; 7:349-54. PMID:7546399; http://dx.doi.org/10.1016/0952- 7915(95)80109-X.
50. Ada G, Isaacs D. Carbohydrate-protein conjugate vaccines. Clin Microbiol Infect 2003; 9:79-85. PMID:12588327; http://dx.doi.org/10.1046/j.1469- 0691.2003.00530.x.
51. Jansen AM, Hall LJ, Clare S, Goulding D, Holt KE, Grant AJ, et al. A Salmonella typhimurium- Typhi genomic chimera: a model to study Vi polysaccharide capsule function in vivo. PLoS Pathog 2011; 7:1002131. PMID:21829346; http://dx.doi. org/10.1371/journal.ppat.1002131.
52. Mundy R, MacDonald TT, Dougan G, Frankel G, Wiles S. Citrobacter rodentium of mice and man. Cell Microbiol 2005; 7:1697-706. PMID:16309456; http://dx.doi.org/10.1111/j.1462- 5822.2005.00625.x.
53. Frederick MR, Kuttler C, Hense BA, Eberl HJ. A mathematical model of quorum sensing regulated EPS production in biofilm communities. Theor Biol Med Model 2011; 8:8. PMID:21477365; http:// dx.doi.org/10.1186/1742-4682-8-8.
54. Wiles S, Clare S, Harker J, Huett A, Young D, Dougan G, et al. Organ specificity, colonization and clearance dynamics in vivo following oral challenges with the murine pathogen Citrobacter rodentium. Cell Microbiol 2004; 6:963-72. PMID:15339271; http://dx.doi.org/10.1111/j.1462-5822.2004.00414.x.
55. Cronin M, Sleator RD, Hill C, Fitzgerald GF, van Sinderen D. Development of a luciferase-based reporter system to monitor Bifidobacterium breve UCC2003 persistence in mice. BMC Microbiol 2008; 8:161. PMID:18816375; http://dx.doi. org/10.1186/1471-2180-8-161.
56. Rodrigues DM, Sousa AJ, Johnson-Henry KC, Sherman PM, Gareau MG. Probiotics Are Effective for the Prevention and Treatment of Citrobacter rodentium-Induced Colitis in Mice. J Infect Dis 2012; In press. PMID:22430833; http://dx.doi. org/10.1093/infdis/jis177.
57. Chen CC, Chiu CH, Lin TY, Shi HN, Walker WA. Effect of probiotics Lactobacillus acidophilus on Citrobacter rodentium colitis: the role of dendritic cells. Pediatr Res 2009; 65:169-75. PMID:19262293; http://dx.doi.org/10.1203/PDR.0b013e31818d5a06.