Autoinducer-2 plays a crucial role in gut colonization and probiotic functionality of Bifidobacterium breve UCC2003

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Christiaen, Steven E A ^a   O'Connell Motherway, Mary ^b   Bottacini, Francesca ^b   Lanigan, Noreen ^b   Casey, Pat G ^b   Huys, Geert ^c   Nelis, Hans J ^a   Van Sinderen, Douwe ^b   Coenye, Tom ^a  

^a GHENT UNIVERSITY   (Belgium)

^b UNIVERSITY COLLEGE CORK   (Ireland)

^c GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOINDUCER 2 MOLECULE; BACTERIAL PROTEIN; PROBIOTIC AGENT; UNCLASSIFIED DRUG; HOMOSERINE; LACTONE; LUXS PROTEIN, BACTERIA; LYASE; N-OCTANOYLHOMOSERINE LACTONE; OLIGONUCLEOTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM IDENTIFICATION; BIFIDOBACTERIUM BREVE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFECT; FEMALE; GENE CLUSTER; GENE FUNCTION; GENE IDENTIFICATION; IN VIVO STUDY; INFECTION PREVENTION; INTESTINE FLORA; LUXS GENE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PROTEIN DETERMINATION; PROTEIN FUNCTION; QUORUM SENSING; SALMONELLOSIS; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION; UPREGULATION; ANALOGS AND DERIVATIVES; ANIMAL; BIFIDOBACTERIUM; GASTROINTESTINAL TRACT; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; MICROBIOLOGY; NONPARAMETRIC TEST; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; BACTERIAL PROTEINS; BIFIDOBACTERIUM; CAENORHABDITIS ELEGANS; CARBON-SULFUR LYASES; GASTROINTESTINAL TRACT; GENE EXPRESSION PROFILING; HOMOSERINE; LACTONES; MICE; OLIGONUCLEOTIDES; PROBIOTICS; REAL-TIME POLYMERASE CHAIN REACTION; STATISTICS, NONPARAMETRIC;

EID: 84901596289     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0098111     Document Type: Article

References (82)

1. Isolauri E, Rautava S, Kalliomaki M, Kirjavainen P, Salminen S (2002). Role of probiotics in food hypersensitivity. Curr Opin Allergy Clin Immunol 2: 263-271. (Pubitemid 34615122)
2. Butler CC, Duncan D, Hood K (2012). Does taking probiotics routinely with antibiotics prevent antibiotic associated diarrhoea? BMJ 344: e682.
3. Gourbeyre P, Denery S, Bodinier M (2011) Probiotics, prebiotics, and synbiotics: impact on the gut immune system and allergic reactions. J Leukoc Biol 89: 685-695.
4. Jonkers D, Penders J, Masclee A, Pierik M (2012) Probiotics in the management of inflammatory bowel disease: a systematic review of intervention studies in adult patients. Drugs 72: 803-823.
5. Damman CJ, Miller SI, Surawicz CM, Zisman TL (2012) The microbiome and inflammatory bowel disease: is there a therapeutic role for fecal microbiota transplantation? Am J Gastroenterol 107: 1452-1459.
6. de Vrese M, Schrezenmeir J (2008) Probiotics, prebiotics, and synbiotics. Adv Biochem Eng Biotechnol 111: 1-66.
7. Corr SC, Gahan CG, Hill C (2007) Impact of selected Lactobacillus and Bifidobacterium species on Listeria monocytogenes infection and the mucosal immune response. FEMS Immunol Med Microbiol 50: 380-388. (Pubitemid 47041463)
8. Fanning S, Hall LJ, Cronin M, Zomer A, MacSharry J et al (2012) Bifidobacterial surface-exopolysaccharide facilitates commensal-host interaction through immune modulation and pathogen protection. Proc Natl Acad Sci U S A 109: 2108-2113.
9. Siciliano RA, Mazzeo MF (2012). Molecular mechanisms of probiotic action: a proteomic perspective. Curr Opin Microbiol 15: 390-396.
10. Reid G, Kim SO, Kohler GA (2006) Selecting, testing and understanding probiotic microorganisms. FEMS Immunol Med Microbiol 46: 149-157.
11. Kim Y, Mylonakis E (2012) Caenorhabditis elegans immune conditioning with the probiotic bacterium Lactobacillus acidophilus strain NCFM enhances Gram-positive immune responses. Infect Immun 80: 2500-2508.
12. Russell DA, Ross RP, Fitzgerald GF, Stanton C (2011) Metabolic activities and probiotic potential of bifidobacteria. Int J Food Microbiol 149: 88-105.
13. Lebeer S, Vanderleyden J, De Keersmaecker SC (2010). Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Nat Rev Microbiol 8: 171-184.
14. Bassler BL (1999) How bacteria talk to each other: regulation of gene expression by quorum sensing. Curr Opin Microbiol 2: 582-587.
15. Hodgkinson JT, Welch M, Spring DR (2007) Learning the language of bacteria. ACS Chem Biol 2: 715-717. (Pubitemid 350285906)
16. Turovskiy Y, Kashtanov D, Paskhover B, Chikindas ML (2007). Quorum sensing: fact, fiction, and everything in between. Adv Appl Microbiol 62: 191-234. (Pubitemid 47380499)
17. Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21: 319-346. (Pubitemid 41740638)
18. Pollumaa L, Alamae T, Mae A (2012) Quorum sensing and expression of virulence in pectobacteria. Sensors 12: 3327-3349.
19. Schuster M, Greenberg EP (2006). A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. Int J Med Microbiol 296: 73-81. (Pubitemid 43375989)
20. Sjoblom S, Brader G, Koch G, Palva ET (2006) Cooperation of two distinct ExpR regulators controls quorum sensing specificity and virulence in the plant pathogen Erwinia carotovora. Mol Microbiol 60: 1474-1489. (Pubitemid 43801438)
21. Winson MK, Camara M, Latifi A, Foglino M, Chhabra SR, et al. (1995) Multiple N-acyl-L-homoserine lactone signal molecules regulate production of virulence determinants and secondary metabolites in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 92: 9427-9431.
22. Gordon C.P., Williams P, Chan WC (2013) Attenuating Staphylococcus aureus virulence gene regulation: a medicinal chemistry perspective. J Med Chem 56: 1389-1404.
23. Otto M (2012) Staphylococcal infections: mechanisms of biofilm maturation and detachment as critical determinants of pathogenicity. Annu Rev Med 64: 175-188.
24. Choi J, Shin D, Kim M, Park J, Lim S et al. (2012) LsrR-mediated quorum sensing controls invasiveness of Salmonella typhimurium by regulating SPI-1 and flagella genes. PLoS One 7: e37059.
25. Soni KA, Jesudhasan PR, Cepeda M, Williams B, Hume M et al. (2008) Autoinducer AI-2 is involved in regulating a variety of cellular processes in Salmonella Typhimurium. Foodborne Pathog Dis 5: 147-153. (Pubitemid 351535859)
26. Surette MG, Bassler BL (1999) Regulation of autoinducer production in Salmonella typhimurium. Mol Microbiol 31: 585-595. (Pubitemid 29046100)
27. Kim SY, Lee SE, Kim YR, Kim CM, Ryu PY, et al. (2003) Regulation of Vibrio vulnificus virulence by the LuxS quorum-sensing system. Mol Microbiol 48: 1647-1664. (Pubitemid 36751068)
28. Xavier KB, Bassler BL (2003) LuxS quorum sensing: more than just a numbers game. Curr Opin Microbiol 6: 191-197. (Pubitemid 36628665)
29. Xavier KB, Bassler BL (2005) Regulation of uptake and processing of the quorum-sensing autoinducer AI-2 in Escherichia coli. J Bacteriol 187: 238-248. (Pubitemid 40024200)
30. Rezzonico F, Duffy B (2008) Lack of genomic evidence of AI-2 receptors suggests a non-quorum sensing role for luxS in most bacteria. BMC Microbiol 8: 154.
31. Sun J, Daniel R, Wagner-Dobler I, Zeng AP (2004) Is autoinducer-2 a universal signal for interspecies communication: a comparative genomic and phylogenetic analysis of the synthesis and signal transduction pathways. BMC Evol Biol 4: 36.
32. Buck BL, Azcarate-Peril MA, Klaenhammer TR. (2009) Role of autoinducer-2 on the adhesion ability of Lactobacillus acidophilus . J Appl Microbiol 107: 269-279.
33. Lebeer S, Claes IJ, Verhoeven TL, Shen C, Lambrichts I, et al. (2008) Impact of luxS and suppressor mutations on the gastrointestinal transit of Lactobacillus rhamnosus GG. Appl Environ Microbiol 74: 4711-4718.
34. Lebeer S, De Keersmaecker SC, Verhoeven TL, Fadda AA, Marchal K, et al. (2007) Functional analysis of luxS in the probiotic strain Lactobacillus rhamnosus GG reveals a central metabolic role important for growth and biofilm formation. J Bacteriol 189: 860-871. (Pubitemid 46183860)
35. Wilson CM, Aggio RB, O'Toole PW, Villas-Boas S, Tannock GW (2012) Transcriptional and metabolomic consequences of LuxS inactivation reveal a metabolic rather than quorum-sensing role for LuxS in Lactobacillus reuteri 100-23. J Bacteriol 194: 1743-1746.
36. Sun Z, He X, Brancaccio VF, Yuan J, Riedel CU (2014) Bifidobacteria exhibit LuxS-dependent autoinducer 2 activity and biofilm formation. PLoS One9: e88260.
37. Janssens JC, Steenackers H, Metzger K, Daniels R, Ptacek D, et al. (2007) Interference with the quorum sensing systems of Salmonella enterica serovar typhimurium: possibilities and implications. Commun Agric Appl Biol Sci 72: 35-39.
38. Bassler BL, Wright M, Showalter RE, Silverman MR (1993) Intercellular signalling in Vibrio harveyi: sequence and function of genes regulating expression of luminescence. Mol Microbiol 9: 773-786. (Pubitemid 23253503)
39. Masco L, Huys G, Gevers D, Verbrugghen L, Swings J (2003) Identification of Bifidobacterium species using rep-PCR fingerprinting. Syst Appl Microbiol 26: 557-563. (Pubitemid 37486514)
40. Sambrook J. 2001 Molecular Cloning: a laboratory manual (.Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY) 3rd Ed
41. O'Connell Motherway M, O'Driscoll J, Fitzgerald GF, van Sinderen D (2009) Overcoming the restriction barrier to plasmid transformation and targeted mutagenesis in Bifidobacterium breve UCC2003. Microb Biotechnol 2: 321-332.
42. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, et al. (2000) Artemis: sequence visualization and annotation. Bioinformatics 16: 944-945.
43. O'Connell Motherway M, Zomer A, Leahy SC, Reunanen J, Bottacini F, et al. (2011) 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 U S A 108: 11217-11222.
44. Law J, Buist G, Haandrikman A, Kok J, Venema G, Leenhouts K (1995) A system to generate chromosomal mutations in Lactococcus lactis which allows fast analysis of targeted genes. J Bacteriol 177: 7011-7018.
45. Alvarez-Martin P, O'Connell-Motherway M, van Sinderen D, Mayo B (2007) Functional analysis of the pBC1 replicon from Bifidobacterium catenulatum L48. Appl Microbiol Biotechnol 76: 1395-1402.
46. van Hijum SA, de Jong A, Baerends RJ, Karsens HA, Kramer NE, et al. (2005) A generally applicable validation scheme for the assessment of factors involved in reproducibility and quality of DNA-microarray data. BMC Genomics 6: 77.
47. Garcia de la Nava J, van Hijum S, Trelles O (2003) PreP: gene expression data pre-processing. Bioinformatics 19: 2328-2329. (Pubitemid 37483995)
48. Long A D, Mangalam HJ, Chan BY, Tolleri L, Hatfield GW, Baldi P (2001) Improved statistical inference from DNA microarray data using analysis of variance and a Bayesian statistical framework. Analysis of global gene expression in Escherichia coli K12. J Biol Chem. 276: 19937-19944.
49. EUCAST (2003) Determination of minimum inhibitory concentrations (MICs) of antibacterial agents by broth dilution. Clin Microbiol Infect 9: 1-7.
50. Cooper VS, Carlson WA, LiPuma JJ (2009) Susceptibility of Caenorhabditis elegans to Burkholderia infection depends on prior diet and secreted bacterial attractants. PLoS One 4: e7961.
51. Stiernagle T (2006) Maintenance of C. elegans. WormBook: 1-11.
52. Garsin DA, Sifri CD, Mylonakis E, Qin X, Singh KV, et al. (2001) A simple model host for identifying Gram-positive virulence factors. Proc Natl Acad Sci U S A 98: 10892-10897. (Pubitemid 32878715)
53. Portal-Celhay C,Blaser MJ (2012) Competition and resilience between founder and introduced bacteria in the Caenorhabditis elegans gut. Infect Immun 80: 1288-1299.
54. Sivamaruthi BS, Ganguli A, Kumar M, Bhaviya S, Pandian SK, et al. (2011) Caenorhabditis elegans as a model for studying Cronobacter sakazakii ATCC BAA-894 pathogenesis. J Basic Microbiol 51: 540-549.
55. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: RESEARCH0034.
56. Brackman G, Cos P, Maes L, Nelis HJ, Coenye T (2011) Quorum sensing inhibitors increase the susceptibility of bacterial biofilms to antibiotics in vitro and in vivo. Antimicrob Agents Chemother 55: 2655-2661.
57. Cronin M, Zomer A, Fitzgerald GF, van Sinderen D (2012) Identification of iron-regulated genes of Bifidobacterium breve UCC2003 as a basis for controlled gene expression. Bioeng Bugs 3: 157-167.
58. Clark LC, Hodgkin J (2014) Commensals, probiotics and pathogens in the Caenorhabditis elegans model. Cell Microbiol 16: 27-38.
59. Ikeda T, Yasui C, Hoshino K, Arikawa K, Nishikawa Y (2007) Influence of lactic acid bacteria on longevity of Caenorhabditis elegans and host defense against Salmonella enterica serovar enteritidis. Appl Environ Microbiol 73: 6404-6409. (Pubitemid 47623697)
60. Turroni F, Peano C, Pass DA, Foroni E, Severgnini M, et al. (2012) Diversity of Bifidobacteria within the Infant Gut Microbiota. PLoS One 7: e36957.
61. O'Toole PW, Claesson MJ (2010) Gut microbiota: Changes throughout the lifespan from infancy to elderly. Int Dairy J 20: 281-291.
62. Koenig JE, Spor A, Scalfone N, Fricker AD, Stombaugh J, et al. (2011) Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci U S A 108 Suppl 1: 4578-4585.
63. Turroni F, Ventura M, Buttó LF, Duranti S, O'Toole PW, et al. (2014). Molecular dialogue between the human gut microbiota and the host: a Lactobacillus and Bifidobacterium perspective. Cell Mol Life Sci 71: 183-203.
64. Ventura M, Turroni F, O'Connell Motherway M, MacSharry J, van Sinderen D (2012) Host-microbe interactions that facilitate gut colonization by commensal bifidobacteria. Trends Microbiol 20: 467-476.
65. Pereira CS, Thompson JA, Xavier KB (2013) AI-2-mediated signalling in bacteria. FEMS Microbiol Rev 37:156-181.
66. Fanning S, Hall LJ, van Sinderen D (2012) Bifidobacterium breve UCC2003 surface exopolysaccharide production is a beneficial trait mediating commensal-host interaction through immune modulation and pathogen protection. Gut Microbes 3: 420-425.
67. James CE, Hasegawa Y, Park Y, Yeung V, Tribble GD, et al. (2006) LuxS involvement in the regulation of genes coding for hemin and iron acquisition systems in Porphyromonas gingivalis. Infect Immun 74: 3834-3844. (Pubitemid 43993314)
68. Kim SY, Lee SE, Kim YR, Kim CM, Ryu PY, et al (2003) Regulation of Vibrio vulnificus virulence by the LuxS quorum-sensing system. Mol Microbiol 48: 1647-1664. (Pubitemid 36751068)
69. van der Vinne AN, Lo RY, Shewen PE (2005) Construction and analysis of a Mannheimia haemolytica A1 luxS mutant. Vet Microbiol 110: 53-66. (Pubitemid 41265835)
70. Li L, Xu Z, Zhou Y, Li T, Sun L, et al. (2011) Analysis on Actinobacillus pleuropneumoniae LuxS regulated genes reveals pleiotropic roles of LuxS/AI-2 on biofilm formation, adhesion ability and iron metabolism. Microb Pathog 50: 293-302.
71. Kortman GA, Boleij A, Swinkels DW, Tjalsma H (2012) Iron availability increases the pathogenic potential of Salmonella typhimurium and other enteric pathogens at the intestinal epithelial interface. PLoS One 7: e29968.
72. Brown JS, Holden DW (2002) Iron acquisition by Gram-positive bacterial pathogens. Microbes Infect. 4: 1149-1156. (Pubitemid 35279522)
73. Gray MJ, Freitag NE, Boor KJ (2006) How the bacterial pathogen Listeria monocytogenes mediates the switch from environmental Dr. Jekyll to pathogenic Mr. Hyde. Infect Immun 74: 2505-2512.
74. Rautava S, Luoto R, Salminen S, Isolauri E (2012) Microbial contact during pregnancy, intestinal colonization and human disease. Nat Rev Gastroenterol Hepatol 9: 565-576.
75. Mshvildadze M, Neu J (2010) The infant intestinal microbiome: Friend or foe? Early Hum Dev 86: S67-S71.
76. Carlisle EM,Morowitz MJ (2013). The intestinal microbiome and necrotizing enterocolitis. Curr Opin Pediatr 25: 382-387.
77. Barrett E, Kerr C, Murphy K, O'Sullivan O, Ryan CA, et al. (2013). The individual-specific and diverse nature of the preterm infant microbiota. Arch Dis Childhood Fet Neonatal Ed 98: F334-340.
78. Li D, Rosito G, Slagle T (2013) Probiotics for the prevention of necrotizing enterocolitis in neonates: an 8-year retrospective cohort study. J Clin Pharm Ther 38: 445-449.
79. Chen CC, Allan Walker W (2013) Probiotics and the mechanism of necrotizing enterocolitis.Semin Pediatr Surg 22: 94-100.
80. Ofek Shlomai N, Deshpande G, Rao S, Patole S (2014) Probiotics for preterm neonates: what will it take to change clinical practice? Neonatology 105: 64-70.
81. Lin HY, Chang JH, Chung MY, Lin HC (2013) Prevention of necrotizing enterocolitis in preterm very low birth weight infants: Is it feasible? J Form Med Ass http://dx.doi.org/10.1016/j.jfma.2013.03.010
82. Cabana MD (2010) Evidence increasing that probiotics reduce incidence of necrotizing enterocolitis in very low birth weight infants. J Pediatr 157: 864-865.