The incongruent gelatinase genotype and phenotype in Enterococcus faecalis are due to shutting off the ability to respond to the gelatinase biosynthesis-activating pheromone (GBAP) quorum-sensing signal

Microbiology

Volumn 158, Issue 2, 2012, Pages 519-528

  Teixeira, Neuza ^a,b   Santos, Sofia ^a   Marujo, Paulo ^a   Yokohata, Ryoji ^c   Iyer, Vijayalakshmi S ^d   Nakayama, Jiro ^c   Hancock, Lynn E ^d   Serror, Pascale ^e   Lopes, Maria de Fátima Silva Lopes ^a,b  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^b Estacao Agronomica Nacional   (Portugal)

^c KYUSHU UNIVERSITY   (Japan)

^d KANSAS STATE UNIVERSITY   (United States)

^e UMR1319 MICALIS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; GELATINASE; PHEROMONE;

ARTICLE; BACTERIAL STRAIN; BIOSYNTHESIS; ENTEROCOCCUS FAECALIS; GENE EXPRESSION; GENOTYPE; NONHUMAN; NONSENSE MUTATION; NUCLEOTIDE SEQUENCE; OPERON; PHENOTYPE; PRIORITY JOURNAL; QUORUM SENSING; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BASE SEQUENCE; ENTEROCOCCUS FAECALIS; GELATINASES; GENE EXPRESSION REGULATION, BACTERIAL; GENOTYPE; LACTONES; MOLECULAR SEQUENCE DATA; PEPTIDES, CYCLIC; PHENOTYPE; QUORUM SENSING; SIGNAL TRANSDUCTION;

ENTEROCOCCUS FAECALIS;

EID: 84856696107     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.055574-0     Document Type: Article

References (41)

1. Bourgogne, A., Hilsenbeck, S. G., Dunny, G. M. & Murray, B. E. (2006). Comparison of OG1RF and an isogenic fsrB deletion mutant by transcriptional analysis: the Fsr system of Enterococcus faecalis is more than the activator of gelatinase and serine protease. J Bacteriol 188, 2875-2884.
2. Braga, T. M., Marujo, P. E., Pomba, C. & Lopes, M. F. (2011). Involvement, and dissemination, of the enterococcal small multidrug resistance transporter QacZ in resistance to quaternary ammonium compounds. J Antimicrob Chemother 66, 283-286.
3. Brinster, S., Furlan, S. & Serror, P. (2007). C-terminal WxL domain mediates cell wall binding in Enterococcus faecalis and other Grampositive bacteria. J Bacteriol 189, 1244-1253.
4. Dower, W. J., Miller, J. F. & Ragsdale, C. W. (1988). High efficiency transformation of E. coli by high voltage electroporation. Nucleic Acids Res 16, 6127-6145.
5. Dunny, G. M., Lee, L. N. & LeBlanc, D. J. (1991). Improved electroporation and cloning vector system for Gram-positive bacteria. Appl Environ Microbiol 57, 1194-1201.
6. Eaton, T. J. & Gasson, M. J. (2001). Molecular screening of Enterococcus virulence determinants and potential for genetic exchange between food and medical isolates. Appl Environ Microbiol 67, 1628-1635.
7. Galloway-Peña, J. R., Bourgogne, A., Qin, X. & Murray, B. E. (2011). Diversity of the fsr-gelE region of the Enterococcus faecalis genome but conservation in strains with partial deletions of the fsr operon. Appl Environ Microbiol 77, 442-451.
8. Gaspar, F., Teixeira, N., Rigottier-Gois, L., Marujo, P., Nielsen- LeRoux, C., Crespo, M. T., Lopes, M. F. & Serror, P. (2009). Virulence of Enterococcus faecalis dairy strains in an insect model: the role of fsrB and gelE. Microbiology 155, 3564-3571.
9. Gilmore, M. S., Coburn, P. S., Nallapareddy, S. R. & Murray, B. E. (2002). Enterococcal virulence. In The Enterococci - Pathogenesis, Molecular Biology, and Antibiotic Resistance, pp. 301-354. Edited by M. S. Gilmore. Washington, DC: American Society for Microbiology.
10. Grant, S. G., Jessee, J., Bloom, F. R. & Hanahan, D. (1990). Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants. Proc Natl Acad Sci U S A 87, 4645-4649.
11. Hancock, L. E. & Perego, M. (2004). The Enterococcus faecalis fsr twocomponent system controls biofilm development through production of gelatinase. J Bacteriol 186, 5629-5639.
12. Jha, A. K., Bais, H. P. & Vivanco, J. M. (2005). Enterococcus faecalis mammalian virulence-related factors exhibit potent pathogenicity in the Arabidopsis thaliana plant model. Infect Immun 73, 464-475.
13. 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.
14. Leenhouts, K., Buist, G., Bolhuis, A., ten Berge, A., Kiel, J., Mierau, I., Dabrowska, M., Venema, G. & Kok, J. (1996). A general system for generating unlabelled gene replacements in bacterial chromosomes. Mol Gen Genet 253, 217-224.
15. Lopes, M. F., Pereira, C. I., Rodrigues, F. M., Martins, M. P., Mimoso, M. C., Barros, T. C., Figueiredo Marques, J. J., Tenreiro, R. P., Almeida, J. S. & Barreto Crespo, M. T. (1999). Registered designation of origin areas of fermented food products defined by microbial phenotypes and artificial neural networks. Appl Environ Microbiol 65, 4484-4489.
16. Lopes, M. F., Simões, A. P., Tenreiro, R., Marques, J. J. & Crespo, M. T. (2006). Activity and expression of a virulence factor, gelatinase, in dairy enterococci. Int J Food Microbiol 112, 208-214.
17. Maguin, E., Prévost, H., Ehrlich, S. D. & Gruss, A. (1996). Efficient insertional mutagenesis in lactococci and other Gram-positive bacteria. J Bacteriol 178, 931-935.
18. Mäkinen, P. L., Clewell, D. B., An, F. & Mäkinen, K. K. (1989). Purification and substrate specificity of a strongly hydrophobic extracellular metalloendopeptidase ("gelatinase") from Streptococcus faecalis (strain 0G1-10). J Biol Chem 264, 3325-3334.
19. Mohamed, J. A. & Murray, B. E. (2006). Influence of the fsr locus on biofilm formation by Enterococcus faecalis lacking gelE. J Med Microbiol 55, 1747-1750.
20. Mundt, J. O. (1986). Enterococci. In Bergey's Manual of Systematic Bacteriology, pp. 1063-1065. Edited by P. H. A. Sneath, N. S. Mair, M. E. Sharpe & J. G. Holt. Baltimore: Williams & Wilkins.
21. Nakayama, J., Cao, Y., Horii, T., Sakuda, S., Akkermans, A. D., de Vos, W. M. & Nagasawa, H. (2001a). Gelatinase biosynthesisactivating pheromone: a peptide lactone that mediates a quorum sensing in Enterococcus faecalis. Mol Microbiol 41, 145-154.
22. Nakayama, J., Cao, Y., Horii, T., Sakuda, S. & Nagasawa, H. (2001b). Chemical synthesis and biological activity of the gelatinase biosynthesis- activating pheromone of Enterococcus faecalis and its analogs. Biosci Biotechnol Biochem 65, 2322-2325.
23. Nakayama, J., Kariyama, R. & Kumon, H. (2002). Description of a 23.9-kilobase chromosomal deletion containing a region encoding fsr genes which mainly determines the gelatinase-negative phenotype of clinical isolates of Enterococcus faecalis in urine. Appl Environ Microbiol 68, 3152-3155.
24. Ogier, J. C. & Serror, P. (2007). Safety assessment of dairy microorganisms: the Enterococcus genus. Int J Food Microbiol 126, 291-301.
25. Park, S. Y., Kim, K. M., Lee, J. H., Seo, S. J. & Lee, I. H. (2007). Extracellular gelatinase of Enterococcus faecalis destroys a defense system in insect hemolymph and human serum. Infect Immun 75, 1861-1869.
26. Park, S. Y., Shin, Y. P., Kim, C. H., Park, H. J., Seong, Y. S., Kim, B. S., Seo, S. J. & Lee, I. H. (2008). Immune evasion of Enterococcus faecalis by an extracellular gelatinase that cleaves C3 and iC3b. J Immunol 181, 6328-6336.
27. Parkinson, J. S. & Kofoid, E. C. (1992). Communication modules in bacterial signaling proteins. Annu Rev Genet 26, 71-112.
28. Qin, X., Singh, K. V., Weinstock, G. M. & Murray, B. E. (2000). Effects of Enterococcus faecalis fsr genes on production of gelatinase and a serine protease and virulence. Infect Immun 68, 2579-2586.
29. Que, Y. A., Haefliger, J. A., Francioli, P. & Moreillon, P. (2000). Expression of Staphylococcus aureus clumping factor A in Lactococcus lactis subsp. cremoris using a new shuttle vector. Infect Immun 68, 3516-3522.
30. Sahm, D. F., Kissinger, J., Gilmore, M. S., Murray, P. R., Mulder, R., Solliday, J. & Clarke, B. (1989). In vitro susceptibility studies of vancomycin-resistant Enterococcus faecalis. Antimicrob Agents Chemother 33, 1588-1591.
31. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
32. Sifri, C. D., Mylonakis, E., Singh, K. V., Qin, X., Garsin, D. A., Murray, B. E., Ausubel, F. M. & Calderwood, S. B. (2002). Virulence effect of Enterococcus faecalis protease genes and the quorum-sensing locus fsr in Caenorhabditis elegans and mice. Infect Immun 70, 5647-5650.
33. Steck, N., Hoffmann, M., Sava, I. G., Kim, S. C., Hahne, H., Tonkonogy, S. L., Mair, K., Krueger, D., Pruteanu, M. & other authors (2011). Enterococcus faecalis metalloprotease compromises epithelial barrier and contributes to intestinal inflammation. Gastroenterology 141, 959-971.
34. Su, Y. A., Sulavik, M. C., He, P., Makinen, K. K., Makinen, P. L., Fiedler, S., Wirth, R. & Clewell, D. B. (1991). Nucleotide sequence of the gelatinase gene (gelE) from Enterococcus faecalis subsp. liquefaciens. Infect Immun 59, 415-420.
35. Thomas, V. C., Thurlow, L. R., Boyle, D. & Hancock, L. E. (2008). Regulation of autolysis-dependent extracellular DNA release by Enterococcus faecalis extracellular proteases influences biofilm development. J Bacteriol 190, 5690-5698.
36. Thomas, V. C., Hiromasa, Y., Harms, N., Thurlow, L., Tomich, J. & Hancock, L. E. (2009). A fratricidal mechanism is responsible foreDNA release and contributes to biofilm development of Enterococcus faecalis. Mol Microbiol 72, 1022-1036.
37. Thurlow, L. R., Thomas, V. C. & Hancock, L. E. (2009). Capsular polysaccharide production in Enterococcus faecalis and contribution of CpsF to capsule serospecificity. J Bacteriol 191, 6203-6210.
38. Vebø, H. C., Snipen, L., Nes, I. F. & Brede, D. A. (2009). The transcriptome of the nosocomial pathogen Enterococcus faecalis V583 reveals adaptive responses to growth in blood. PLoS ONE 4, e7660.
39. Vebø, H. C., Solheim, M., Snipen, L., Nes, I. F. & Brede, D. A. (2010). Comparative genomic analysis of pathogenic and probiotic Enterococcus faecalis isolates, and their transcriptional responses to growth in human urine. PLoS ONE 5, e12489.
40. Yan, X., Zhao, C., Budin-Verneuil, A., Hartke, A., Rincé, A., Gilmore, M. S., Auffray, Y. & Pichereau, V. (2009). The (p)ppGpp synthetase RelA contributes to stress adaptation and virulence in Enterococcus faecalis V583. Microbiology 155, 3226-3237.
41. Zhu, Y. & Inouye, M. (2002). The role of the G2 box, a conserved motif in the histidine kinase superfamily, in modulating the function of EnvZ. Mol Microbiol 45, 653-663.