A bile-inducible membrane protein mediates bifidobacterial bile resistance

Microbial Biotechnology

Volumn 5, Issue 4, 2012, Pages 523-535

  Ruiz, Lorena ^a,b   O'Connell Motherway, Mary ^b   Zomer, Aldert ^b,c   de los Reyes Gavilán, Clara G ^a   Margolles, Abelardo ^a   van Sinderen, Douwe ^b  

^a DEPARTMENT OF MICROBIOLOGY AND BIOCHEMISTRY OF DAIRY PRODUCTS   (Spain)

^b UNIVERSITY COLLEGE CORK   (Ireland)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLIC ACID; CYSTATHIONINE BETA SYNTHASE; MACROLIDE; MEMBRANE PROTEIN; PROTEIN BBR 0838; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BIFIDOBACTERIUM BREVE; BILE; GENE LOCUS; GENETIC TRANSCRIPTION; MICROARRAY ANALYSIS; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; OPTICAL DENSITY; PHENOTYPE;

BIFIDOBACTERIUM; BILE; DETERGENTS; DRUG RESISTANCE, BACTERIAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENE KNOCKOUT TECHNIQUES; GENETIC COMPLEMENTATION TEST; MEMBRANE PROTEINS; MICROBIAL VIABILITY; MUTAGENESIS, INSERTIONAL; PROMOTER REGIONS, GENETIC; TRANSCRIPTION INITIATION SITE;

EID: 84862014264     PISSN: 17517907     EISSN: 17517915     Source Type: Journal    
DOI: 10.1111/j.1751-7915.2011.00329.x     Document Type: Article

References (56)

1. Álvarez-Martín, P., Flórez, A.B., Margolles, A., Solar, G., and Mayo, B. (2008) Improved cloning vectors for bifidobacteria, based on the Bifidobacterium catenulatum pBC1 replicon. Appl Environ Microbiol 74: 4656-4665.
2. Begley, M., Gaham, C.G., and Hill, C. (2005) The interaction between bacteria and bile. FEMS Microbiol Rev 29: 625-651.
3. Cerda-Maira, F.A., Ringelberg, C.S., and Taylor, R.K. (2008) The bile response repressor BreR regulates expression of the Vibrio cholerae breAB efflux system operon. J Bacteriol 190: 6809-6814.
4. Coppins, R.L., Hall, K.D., and Groisman, E.A. (2007) The intricate world of riboswitches. Curr Opin Microbiol 10: 176-181.
5. Diwa, A., Bricker, A.L., Jain, C., and Belasco, J.G. (2000) An evolutionarily conserved RNA stem-loop functions as a sensor that directs feedback regulation of RNase E gene expression. Genes Dev 14: 1249-1260.
6. Elkins, C.A., and Savage, D.C. (2003) CbsT2 from Lactobacillus johnsonii 100-100 is a transport protein of the major facilitator superfamily that facilitates bile acid antiport. J Mol Microbiol Biotechnol 6: 76-87.
7. Estrem, S.T., Gaal, T., Ross, W., and Gourse, R.L. (1998) Identification of an UP element consensus sequence for bacterial promoters. Proc Natl Acad Sci USA 95: 9761-9766.
8. Gasteiger, E., Gattiker, A., Hoogland, C., Ivanyi, I., Appel, R.D., and Baroch, A. (2003) ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res 31: 3784-3788.
9. Gueimonde, M., Garrigues, C., van Sinderen, D., de los Reyes-Gavilán, C.G., and Margolles, A. (2009) Bile-inducible efflux transporter from Bifidobacterium longum NCC2705, conferring bile resistance. Appl Environ Microbiol 75: 3153-3160.
10. Hambraeus, G., Karhumaa, K., and Rutberg, B. (2002) A 5' stem-loop and ribosome binding but not translation are important for the stability of Bacillus subtilis aprE leader mRNA. Microbiology 148: 1795-1803.
11. Hofman, A.F. (1998) Bile secretion and the enterohepatic circulation of bile acids. In Gastrointestinal and Liver Disease. Feldman, M., Scharschmidt, B.F., and Sleisenger, M.H. (eds). Philadelphia, PA, USA: W.B. Saunders, pp. 937-948.
12. Ignoul, S., and Eggermont, J. (2005) CBS domains: structure, function, and pathology in human proteins. Am J Physiol Cell Physiol 289: 1369-1378.
13. Jones, B.V., Begley, M., Hill, C., Gahan, C.G., and Marchesi, J.R. (2008) Functional and comparative metagenomic analysis of bile salt hydrolase activity in the human gut microbiome. Proc Natl Acad Sci USA 105: 13580-13585.
14. Ke, W.J., Chang, B.Y., Lin, T.P., and Liu, S.T. (2009) Activation of the promoter of the fengycin synthetase operon by the UP element. J Bacteriol 191: 4615-4623.
15. Krogh, A., Larsson, B., von Hejine, G., and Sonnhammer, E.L.L. (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305: 567-580.
16. Kurokawa, K., Itoh, H., Kuwhara, T., Oshima, K., Toh, H., Toyoda, A., etal. (2007) Comparative metagenomics revealed commonly enriched gene sets in human gut microbiome. DNA Res 14: 169-181.
17. Law, J., Buist, G., Haandrikman, A., Kok, J., Venema, G., and Leenhouts, K. (1995) A system to generate chromosomal mutations in Lactococcus lactis which allows fast analysis of targeted genes. J Bacteriol 177: 7011-7018.
18. Lin, J., Sahin, O., Michel, L.O., and Zhang, Q. (2003) Critical role of multidrug efflux pump CmeABC in bile resistance and in vivo colonization of Campylobacter jejuni. Infect Immun 71: 4250-4259.
19. Lomax, A.R., and Calder, P.C. (2009) Probiotics, immune function, infection and inflammation: a review of the evidence from studies conducted in humans. Curr Pharm Des 15: 1428-1518.
20. Lubelski, J., de Jong, A., van Merkerk, R., Agustiandari, H., Kuipers, O.P., Kok, J., and Driessen, A.J. (2006) LmrCD is a major multidrug resistance transporter in Lactococcus lactis. Mol Microbiol 61: 771-781.
21. MacConaill, L.E., Butler, D., O'Connell-Motherway, M., Fitzgerald, G.F., and van Sinderen, D. (2003) Identification of two-component regulatory systems in Bifidobacterium infantis by functional complementation and degenerate PCR approaches. Appl Environ Microbiol 69: 4219-4226.
22. Mahmood, N.A.B., Biemans-Oldehinkel, E., and Poolman, B. (2009) Engineering of ion sensing by the cystathionine β-synthase module of the ABC transporter OpuA. J Biol Chem 284: 14368-14376.
23. Margolles, A., and de los Reyes-Gavilán, C.G. (2003) Purification and functional characterization of a novel alpha-L-arabinofuranosidase from Bifidobacterium longum B667. Appl Environ Microbiol 69: 5096-5103.
24. Margolles, A., García, L., Sánchez, B., Gueimonde, M., and de los Reyes-Gavilán, C.G. (2003) Characterisation of a Bifidobacterium strain with acquired resistance to cholate - a preliminary study. Int J Food Microbiol 82: 191-198.
25. Margolles, A., Moreno, J.A., van Sinderen, D., and de los Reyes-Gavilán, C.G. (2005) Macrolide resistance mediated by a Bifidobacterium breve membrane protein. Antimicrob Agents Chemother 49: 4379-4381.
26. Margolles, A., Flórez, A.B., Moreno, J.A., van Sinderen, D., and de los Reyes-Gavilán, C.G. (2006) Two membrane proteins from Bifidobacterium breve UCC2003 constitute and ABC-type multidrug transporter. Microbiology 152: 3497-3505.
27. Mazé, A., O'Connell-Motherway, M., Fitgerald, G.F., Deutscher, J., and van Sinderen, D. (2007) Identification and characterization of a fructose phosphotransferase system in Bifidobacterium breve UCC2003. Appl Environ Microbiol 75: 545-553.
28. Noriega, L., Gueimonde, M., Sánchez, B., Margolles, A., and de los Reyes-Gavilán, C.G. (2004) Effect of the adaptation to high bile salts concentrations on glycosidic activity, suvival at low pH and cross-resistance to bile salts in Bifidobacterium. Int J Food Microbiol 94: 79-86.
29. O'Connell-Motherway, M., Fitzgerald, G.F., Neirynck, S., Ryan, S., Steidler, L., and van Sinderen, D. (2008) Characterization of ApuB, an extracellular type II amylopullulanase from Bifidobacterium breve UCC2003. Appl Environ Microbiol 74: 6271-6279.
30. O'Connell-Motherway, M., O'Driscoll, J., Fitzgerald, G.F., and van Sinderen, D. (2009) Overcoming the restriction barrier to plasmid transformation and targeted mutagenesis in Bifidobacterium breve UCC2003. Microb Biotechnol 2: 321-332.
31. O'Connell-Motherway, M., Zomer, A., Leahy, S.C., Reunanen, J., Bottacini, F., Claesson, M.J., etal. (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 USA 108: 11217-11222.
32. Pfeiler, E.A., and Klaenhammer, T.R. (2009) The role of transporter proteins in bile tolerance in Lactobacillus acidophilus. Appl Environ Microbiol 75: 6013-6016.
33. Piddock, L.J.V. (2006) Multidrug-resistance efflux-pumps-not just for resistance. Nat Rev Microbiol 4: 629-636.
34. Platteeuw, C., Simons, G., and de Vos, W.M. (1994) Use of the Escherichia coli beta-glucuronidase (gusA) as a reporter gene for analyzing promoters in lactic acid bacteria. Appl Environ Microbiol 60: 587-593.
35. Pokusaeva, K., Neves, A.R., Zomer, A., O'Connell-Motherway, M., MacSharry, J., Curley, P., etal. (2010) Ribose utilization by the human commensal Bifidobacterium breve UCC2003. Microb Biotechnol 3: 311-323.
36. Pokusaeva, K., O'Connell-Motherway, M., Zomer, A., MacSharry, J., Fitzgerald, G.F., and van Sinderen, D. (2011) Cellodextrin utilization by Bifidobacterium breve UCC2003. Appl Environ Microbiol 77: 1681-1690.
37. Price, C.E., Reid, S.J., Driessen, A.J., and Abratt, V.R. (2006) The Bifidobacterium longum NCIMB 702259 ctr gene codes for a novel cholate transporter. Appl Environ Microbiol 72: 78-87.
38. Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K.S., Manichanh, C., etal. (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464: 59-65.
39. Quillin, S.J., Schwartz, K.T., and Leber, J.H. (2011) The novel Listeria monocytogenes bile sensor BrtA controls expression of the cholic acid efflux pump MdrT. Mol Microbiol 81: 129-142.
40. Ruiz, L., Zomer, A., O'Connell-Motherway, M., van Sinderen, D., and Margolles, A. (2011) Discovering novel bile protection systems in Bifidobacterium breve UCC2003 through functional genomics. Appl Environ Microbiol. doi:10.1128/AEM.06060-11.
41. de Ruyter, P.G., Kuipers, O.P., and de Vos, W.M. (1996) Controlled gene expression systems for Lactococcus lactis with the food-grade inducer nisin. Appl Environ Microbiol 62: 3662-3667.
42. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor, NY, USA: Cold String Harbor Laboratory.
43. Sánchez, B., Champomier-Vergès, M.C., Stuer-Lauridsen, B., Ruas-Madiedo, P., Anglade, P., Baragie, F., etal. (2007a) Adaptation and response of Bifidobacterium animalis subsp. lactis to bile: a proteomic and physiological approach. Appl Environ Microbiol 73: 6757-6767.
44. Sánchez, B., Champomier-Vergès, M.C., Collado, M.C., Anglade, P., Baraige, F., Sanz, Y., etal. (2007b) Low-pH adaptation and the acid tolerance response of Bifidobacterium longum biotype longum. Appl Environ Microbiol 73: 6450-6459.
45. Sánchez, B., Ruiz, L., de los Reyes-Gavilán, C.G., and Margolles, A. (2008) Proteomics of stress response in Bifidobacterium. Front Biosci 13: 6905-6919.
46. Stanton, C., Ross, R.P., Fitzgerald, G.F., and van Sinderen, D. (2005) Fermented functional foods based on probiotics and their biogenic metabolites. Curr Opin Biotechnol 16: 198-203.
47. Ventura, M., van Sinderen, D., Fitzgerald, G.F., and Zink, R. (2004) Insights into the taxonomy, genetics and physiology of bifidobacteria. Antonie Van Leeuwenhoek 86: 205-223.
48. Ventura, M., Fitzgerald, G.F., and van Sinderen, D. (2005) Genetic and transcriptional organization of the clpC locus in Bifidobacterium breve UCC2003. Appl Environ Microbiol 71: 6282-6291.
49. Ventura, M., O'Flaherty, S., Claesson, M.J., Turroni, F., Klaenhammer, T.R., van Sinderen, D., and O'Toole, P.W. (2009) Genome-scale analyses of health-promoting bacteria: probiogenomics. Nat Rev Microbiol 7: 61-71.
50. Waters, L.S., and Storz, G. (2009) Regulatory RNAs in Bacteria. Cell 136: 615-628.
51. Watson, D., Sleator, R.D., Hill, C., and Gahan, C.G. (2008) Enhancing bile tolerance improves survival and persistence of Bifidobacterium and Lactococcus in the murine gastrointestinal tract. BMC Microbiol 8: 176.
52. Watson, D., Sleator, R.D., Casey, P.G., Hill, C., and Gahan, C.G. (2009) Specific osmolyte transporters mediate bile tolerance in Listeria monocytogenes. Infect Immun 77: 4895-4904.
53. Wells, J.M., Wilson, P.W., and Le Page, R.W. (1993) Improved cloning vectors and transformation procedure for Lactococcus lactis. J Appl Bacteriol 74: 629-636.
54. Yokota, A., Veenstra, M., Kurdi, P., van Veen, H.W., and Konings, W.N. (2000) Cholate resistance in Lactococcus lactis is mediated by an ATP-dependent multispecific organic anion transporter. J Bacteriol 182: 5196-5201.
55. Zaidi, A.H., Bakkes, P.J., Lubelski, J., Agustiandari, H., Kuipers, O.P., and Driessen, A.J. (2008) The ABC-type multidrug resistance transporter LmrCD is responsible for an extrusion-based mechanism of bile acid resistance in Lactococcus lactis. J Bacteriol 190: 7357-7366.
56. Zomer, A., Fernández, M., Kearney, B., Fitzgerald, G.F., Ventura, M., and van Sinderen, D. (2009) An interactive regulatory network controls stress response in Bifidobacterium breve UCC2003. J Bacteriol 191: 7039-7049.