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Stress Responses of Enterococci

  • Yanick Auffray
  • Abdellah Benachour
  • Aurélie Budin-Verneuil
  • Jean-Christophe Giard
  • Axel Hartke
  • Vianney Pichereau
  • Alain Rincé
  • Nicolas Sauvageot
  • Nicolas Verneuil
Chapter
Part of the Food Microbiology and Food Safety book series (FMFS)

Abstract

Enterococcus faecalis is a common intestinal micro-organism used as an indicator of hygienic quality of food and water but also can be the causative agent of nosocomial infections. In this chapter we give an overview of the physiological responses of E. faecalis to several environmental modifications and then results and strategies concerning the identification of cellular effectors and transcriptional regulators of these responses. The identification of the mechanisms involved in the intrinsic as well as acquired resistances of E. faecalis toward harsh environments is an important step for understanding how this bacterium emerges as a prominent opportunistic pathogen.

Keywords

Bile Salt Sigma Factor Oxidative Stress Response Histidine Kinase Oligotrophic Condition 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Aakra A, Vebo H, Snipen L, Hirt H, Aastveit A, Kapur V, Dunny G, Murray BE, Nes IF (2005) Transcriptional response of Enterococcus faecalis V583 to erythromycin. Antimicrob Agents Chemother 49:2246–2259CrossRefGoogle Scholar
  2. Arnaud M, Chastanet A, Débarbouillé M (2004) New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, Gram-positive bacteria. Appl Environ Microbiol 70:6887–6891CrossRefGoogle Scholar
  3. Arthur MC, Molinas C, Courvalin P (1992) The VanS-VanR two-component regulatory system controls synthesis of depsipeptide peptidoglycan precursors in Enterococcus faecium BM4147. J Bacteriol 174:2582–2591Google Scholar
  4. Bashyam MD, Hasnain SE (2004) The extracytoplasmic function sigma factors: role in bacterial pathogenesis. Infect Genet Evol 4:301–308CrossRefGoogle Scholar
  5. Benachour A, Muller C, Dabrowski-Coton M, Le Breton Y, Giard JC, Rincé A, Auffray Y, Hartke A (2005) The Enterococcus faecalis SigV protein is an extracytoplasmic function sigma factor contributing to survival following heat, acid, and ethanol treatments. J Bacteriol 187:1022–1035CrossRefGoogle Scholar
  6. Bizzini A, Zhao C, Auffray Y, Hartke A (2009) The Enterococcus faecalis superoxide dismutase is essential for its tolerance to vancomycin and penicillin. J Antimicrob Chemother 64:1196–1202CrossRefGoogle Scholar
  7. Bourgogne A, Hilsenbeck SG, Dunny GM, Murray BE (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 188:2875–2884CrossRefGoogle Scholar
  8. Boutibonnes P, Giard JC, Hartke A, Thammavongs B, Auffray Y (1993) Characterization of the heat shock response of Enterococcus faecalis. Antonie von Leeuwenhoek 64:47–55CrossRefGoogle Scholar
  9. Brändle N, Zehnder M, Weiger R, Waltimo T (2008) Impact of growth conditions on susceptibility of five microbial species to alkaline stress. J Endod 34:579–582CrossRefGoogle Scholar
  10. Bsat N, Herbig A, Casillas-Martinez L, Setlow P, Helmann JD (1998) Bacillus subtilis contains multiple Fur homologs: identification of the iron uptake (Fur) and peroxide regulon (PerR) repressors. Mol Microbiol 29:189–198CrossRefGoogle Scholar
  11. Capiaux H, Giard JC, Lemarinier S, Auffray Y (2000) Characterization and analysis of a new gene involved in glucose starvation response in Enterococcus faecalis. Int J Food Microbiol 55:99–102CrossRefGoogle Scholar
  12. Chenoweth C, Schaberg D (1990) The epidemiology of enterococci. Eur J Clin Microbiol Infect Dis 9:80–89CrossRefGoogle Scholar
  13. Cintas LM, Casaus P, Holo H, Hernandez PE, Nes IF, Håvarstein LS (1998) Enterocins L50A and L50B, two novel bacteriocins from Enterococcus faecium L50, are related to staphylococcal hemolysins. J Bacteriol 180:1988–1994Google Scholar
  14. Comenge YR, Quintiliani R Jr, Li L, Dubost L, Brouard JP, Hugonnet JE, Arthur M (2003) The CroRS two-component regulatory system is required for intrinsic beta-lactam resistance in Enterococcus faecalis. J Bacteriol 185:7184–7192CrossRefGoogle Scholar
  15. de Fátima Silva Lopes M, Ribeiro T, Abrantes M, Figueiredo Marques JJ, Tenreiro R, Crespo MT (2005) Antimicrobial resistance profiles of dairy and clinical isolates and type strains of enterococci. Int J Food Microbiol 103:191–198CrossRefGoogle Scholar
  16. Del Papa MF, Perego M (2008) Ethanolamine activates a sensor histidine kinase regulating its utilization in Enterococcus faecalis. J Bacteriol 190:7147–7156CrossRefGoogle Scholar
  17. Derré I, Rapoport G, Msadek T (1999) CtsR, a novel regulator of stress and heat shock response, controls clp and molecular chaperone gene expression in Gram-positive bacteria. Mol Microbiol 31:117–131CrossRefGoogle Scholar
  18. Evers S, Courvalin P (1996) Regulation of VanB-type vancomycin resistance gene expression by the VanS(B)-VanR(B) two-component regulatory system in Enterococcus faecalis V583. J Bacteriol 178:1302–1309Google Scholar
  19. Fabret C, Feher VA, Hoch JA (1999) Two-component signal transduction in Bacillus subtilis: how one organism sees its world. J Bacteriol 181:1975–1983Google Scholar
  20. Flahaut S, Benachour A, Giard JC, Boutibonnes P, Auffray Y (1996a) Defense against lethal treatments and de novo protein synthesis induced by NaCl in Enterococcus faecalis ATCC 19433. Arch Microbiol 165:317–324CrossRefGoogle Scholar
  21. Flahaut S, Frère J, Boutibonnes P, Auffray Y (1996b) Comparison of the bile salts and sodium dodecyl sulfate stress responses in Enterococcus faecalis. Appl Environ Microbiol 62: 2416–2420Google Scholar
  22. Flahaut S, Hartke A, Giard JC, Benachour A, Boutibonnes P, Auffray Y (1996c) Relationships between stress responses toward bile salts, acid and heat treatments in Enterococcus faecalis. FEMS Microbiol Lett 138:49–54CrossRefGoogle Scholar
  23. Flahaut S, Boutibonnes P, Auffray Y (1997a) Les enterocoques dans l’environnement proche de l’homme [in French]. Can J Microbiol 43:699–708CrossRefGoogle Scholar
  24. Flahaut S, Hartke A, Giard JC, Auffray Y (1997b) Alkaline stress response in Enterococcus faecalis: adaptation, cross-protection and changes in protein synthesis. Appl Environ Microbiol 63:812–814Google Scholar
  25. Flahaut S, Laplace JM, Frère J, Auffray Y (1998) The oxidative stress response in Enterococcus faecalis: relationship between H2O2 tolerance and H2O2 stress proteins. Lett Appl Microbiol 26:259–264CrossRefGoogle Scholar
  26. Foulquié Moreno MR, Sarantinopoulos P, Tsakalidou E, De Vuyst L (2006) The role and application of enterococci in food and health. Int J Food Microbiol 106:1–24CrossRefGoogle Scholar
  27. Garsin DA, Urbach J, Huguet-Tapia JC, Peters JE, Ausubel FM (2004) Construction of an Enterococcus faecalis Tn917-mediated-gene-disruption library offers insight into Tn917 insertion patterns. J Bacteriol 186:7280–7289CrossRefGoogle Scholar
  28. Giard JC, Hartke A, Flahaut S, Benachour A, Boutibonnes P, Auffray Y (1996) Starvation induced multi-resistance in Enterococcus faecalis JH2-2. Curr Microbiol 32:264–271CrossRefGoogle Scholar
  29. Giard JC, Hartke A, Flahaut S, Boutibonnes P, Auffray Y (1997) Glucose starvation response in Enterococcus faecalis JH2-2: survival and protein analysis. Res Microbiol 148:27–35CrossRefGoogle Scholar
  30. Giard JC, Rincé A, Capiaux H, Auffray Y, Hartke A (2000) Inactivation of the stress- and starvation-inducible gls24 operon has a pleiotropic effect on cell morphology, stress sensitivity and gene expression in Enterococcus faecalis. J Bacteriol 182:4512–4520CrossRefGoogle Scholar
  31. Giard JC, Laplace JM, Rincé A, Pichereau V, Benachour A, Leboeuf C, Flahaut S, Auffray Y, Hartke A (2001) The stress proteome of Enterococcus faecalis. Electrophoresis 14:2947–2954CrossRefGoogle Scholar
  32. Giard JC, Auffray Y, Benachour A, Hartke A, Laplace JM, Rincé A, Verneuil N, Pichereau V (2004) Proteomics analysis: a powerful tool to identify proteome phenotype and proteome signature in Enterococcus faecalis. Curr Proteomics 1:273–282Google Scholar
  33. Giard JC, Riboulet E, Verneuil N, Sanguinetti M, Auffray Y, Hartke A (2006) Characterization of Ers, a PrfA-like regulator of Enterococcus faecalis. FEMS Immunol Med Microbiol 46:410–418CrossRefGoogle Scholar
  34. Gilmore MS (2002) The enterococci: pathogenesis, molecular biology and antimicrobial resistance. American Society for Microbiology, Washington, DCGoogle Scholar
  35. Giraffa G (2002) Enterococci from foods. FEMS Microbiol Rev 26:163–171CrossRefGoogle Scholar
  36. Haldenwang WG (1995) The sigma factors of Bacillus subtilis. Microbiol Rev 59:1–30Google Scholar
  37. Hancock L, Perego M (2002) Two-component signal transduction in Enterococcus faecalis. J Bacteriol 184:5819–5825CrossRefGoogle Scholar
  38. Hancock L, Perego M (2004a) The Enterococcus faecalis Fsr two-component system controls biofilm development through production of gelatinase. J Bacteriol 186:5629–5639CrossRefGoogle Scholar
  39. Hancock L, Perego M (2004b) Systematic inactivation and phenotypic characterization of two-component signal transduction systems of Enterococcus faecalis V583. J Bacteriol 186:7951–7958CrossRefGoogle Scholar
  40. Hartke A, Giard JC, Laplace JM, Auffray Y (1998) Survival of Enterococcus faecalis in an oligotrophic microcosm: changes in morphology, development of general stress resistance and analysis of protein synthesis. Appl Environ Microbiol 64:4238–4245Google Scholar
  41. Hébert L, Courtin P, Torelli R, Sanguinetti M, Chapot-Chartier MP, Auffray Y, Benachour A (2007) Enterococcus faecalis constitutes an unusual bacterial model in lysozyme resistance. Infect Immun75:5390–5398CrossRefGoogle Scholar
  42. Héchard Y, Pelletier C, Cenatiempo Y, Frère J (2001) Analysis of s   54-dependent genes in Enterococcus faecalis: a mannose PTS permease (EIIMan) is involved in sensitivity to a bacteriocin, mesentericin Y105. Microbiology 147:1575–1580Google Scholar
  43. Heim S, Lleo MM, Bonato B, Guzman CA, Canepari P (2002) The viable but nonculturable state and starvation are different stress responses of Enterococcus faecalis, as determined by proteome analysis. J Bacteriol 184:6739–6745CrossRefGoogle Scholar
  44. Huycke MM, Sahm DF, Gilmore MS (1998) Multiple-drug resistant enterococci: the nature of the problem and an agenda for the future. Emerg Infect Dis 4:239–249CrossRefGoogle Scholar
  45. Jett BD, Huycke MM, Gilmore MS (1994) Virulence of enterococci. Clin Microbiol Rev 7:462–478Google Scholar
  46. Kazmierczak MJ, Wiedmann M, Boor KJ (2005) Alternative sigma factors and their roles in bacterial virulence. Microbiol Mol Biol Rev 69:527–543CrossRefGoogle Scholar
  47. Kristich CJ, Chandler JR, Dunny GM (2007) Development of a host-genotype-independent counterselectable marker and a high-frequency conjugative delivery system and their use in genetic analysis of Enterococcus faecalis. Plasmid 57:131–144CrossRefGoogle Scholar
  48. Kristich CJ, Nguyen VT, Le T, Barnes AMT, Grindle S, Dunny GM (2008) Development and use of an efficient system for random mariner transposon mutagenesis to identify novel genetic determinants of biofilm formation in the core Enterococcus faecalis genome. Appl Environ Microbiol 74:3377–3386CrossRefGoogle Scholar
  49. La Carbona S, Sauvageot N, Giard JC, Benachour A, Posteraro B, Auffray Y, Sanguinetti M, Hartke A (2007) Comparative study of the physiological roles of three peroxidases (NADH peroxidase, Alkyl hydroperoxide reductase and Thiol peroxidase) in oxidative stress response, survival inside macrophages and virulence of Enterococcus faecalis. Mol Microbiol 66:1148–1163CrossRefGoogle Scholar
  50. Laplace JM, Boutibonnes P, Auffray Y (1996) Unusual resistance and acquired tolerance to cadmium chloride in Enterococcus faecalis. J Basic Microbiol 36:311–317CrossRefGoogle Scholar
  51. Laplace JM, Thuault M, Hartke A, Boutibonnes P, Auffray Y (1997) Sodium hypochlorite stress in Enterococcus faecalis: influence of antecedent growth conditions and induced proteins. Curr Microbiol 34:284–289CrossRefGoogle Scholar
  52. 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: 7011–7018Google Scholar
  53. Le Breton Y, Mazé A, Hartke A, Lemarinier S, Auffray Y, Rincé A (2002a) Isolation and characterization of bile salts-sensitive mutants of Enterococcus faecalis. Curr Microbiol 45:434–439Google Scholar
  54. Le Breton Y, Pichereau V, Flahaut S, Auffray Y, Rincé A (2002b) Identification of new genes related to osmotic adaptation in Enterococcus faecalis. Sci Alim 22:87–96CrossRefGoogle Scholar
  55. Le Breton Y, Boël G, Benachour A, Prévost H, Auffray Y, Rincé A (2003) Molecular characterization of Enterococcus faecalis two-component signal transduction pathways related to environmental stresses. Environ Microbiol 5:329–337CrossRefGoogle Scholar
  56. Le Breton Y, Muller C, Auffray Y, Rincé A (2007) New insights about the Enterococcus faecalis CroRS two-component system using a differential-display RAP-PCR approach. Appl Environ Microbiol 73:3738–3741CrossRefGoogle Scholar
  57. Leboeuf C, Leblanc L, Auffray Y, Hartke A (2000) Characterization of the ccpA gene of Enterococcus faecalis: identification of starvation-inducible proteins regulated by ccpA. J Bacteriol 182:5799–5806CrossRefGoogle Scholar
  58. Lewenstein A, Frigerio G, Moroni M (1979) Biological properties of SF68, a new approach for the treatment of diarrheal diseases. Curr Ther Res 26:967–981Google Scholar
  59. Livny J, Teonadi H, Livny M, Waldor MK (2008). High-throughput, kingdom-wide prediction and annotation of bacterial non-coding RNAs. PLoS One. 3: e3197CrossRefGoogle Scholar
  60. Lonetto MA, Brown KL, Rudd KE, Buttner MJ (1994) Analysis of the Streptomyces coelicolor sigE gene reveals the existence of a subfamily of eubacterial RNA polymerase σ factors involved in the regulation of extracytoplasmic functions. Proc Natl Acad Sci USA 91:7573–7577CrossRefGoogle Scholar
  61. Low DE, Willey BM, Betschel S, Kreiswirth B (1994) Enterococcis: pathogens of the 90s. Eur J Surg Suppl 573:19–24Google Scholar
  62. Mittenhuber G (2002) An inventory of genes encoding RNA polymerase sigma factors in 31 completely sequenced eubacterial genomes. J Mol Microbiol Biotechnol 4:77–91Google Scholar
  63. Mizuno T (1997) Compilation of all gene encoding two-component phosphotransfer signal transducers in the genome of Escherichia coli. DNA Res 4:161–168CrossRefGoogle Scholar
  64. Morrison D, Woodford N, Cookson B (1997) Enterococci as emerging pathogens of humans. Soc Appl Bacteriol Symp Suppl 83:89S–99SGoogle Scholar
  65. Muller C, Le Breton Y, Morin T, Benachour A, Auffray Y, Rincé A (2006) The response regulator CroR modulates expression of the secreted stress-induced SalB protein in Enterococcus faecalis. J Bacteriol 188:2636–2645CrossRefGoogle Scholar
  66. Muller C, Sanguinetti M, Riboulet E, Hébert L, Posteraro B, Fadda G, Auffray Y, Rincé A (2008) Characterization of two signal transduction systems involved in intracellular macrophage survival and environmental stress response in Enterococcus faecalis. J Mol Microbiol Biotechnol 14:59–66CrossRefGoogle Scholar
  67. Mylonakis E, Engelbert M, Qin X, Sifri CD, Murray BE, Ausubel FM, Gilmore MS, Calderwood SB (2002). The Enterococcus faecalis fsrB gene, a key component of the fsr quorum-sensing system, is associated with virulence in the rabbit endophthalmitis model. Infect Immun 70:4678–4681CrossRefGoogle Scholar
  68. Nagel, G, Lahrz A, Dersch P (2001) Environmental control of invasin expression in Yersinia pseudotuberculosis is mediated by regulation of RovA, a transcriptional activator of the SlyA/Hor family. Mol Microbiol 41:1249–1269CrossRefGoogle Scholar
  69. Nakayama J, Cao Y, Horii T, Sakuda S, Akkermans DL, de Vos W, Nagasawa H (2001) Gelatinase biosynthesis-activating pheromone: a peptide lactone that mediates a quorum-sensing in Enterococcus faecalis. Mol Microbiol 41:145–154CrossRefGoogle Scholar
  70. O’Farrell PH (1975) High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250:4007–4021Google Scholar
  71. O’Sullivan MG, Thornton GM, O’Sullivan GC, Collins JK (1992) Probiotic bacteria: myth or reality? Trends Food Sci Technol 3:309–314CrossRefGoogle Scholar
  72. Pichereau V, Bourot S, Flahaut S, Blanco C, Auffray Y, Bernard T (1999) The osmoprotectant glycine betaine inhibits salt-induced cross-tolerance towards lethal treatment in Enterococcus faecalis. Microbiology 145:427–435CrossRefGoogle Scholar
  73. Poh CH, Oh HM, Tan AL (2006) Epidemiology and clinical outcome of enterococcal bacteraemia in an acute care hospital. J Infect 52:383–386CrossRefGoogle Scholar
  74. Qin X, Singh KV, Xu Y, Weinstock GM, Murray BE (1998) Effect of disruption of a gene encoding an autolysin of Enterococcus faecalis OG1RF. Antimicrob Agents Chemother 42:2883–2888Google Scholar
  75. Qin X, Singh KV, Weinstock GM, Murray BE (2000) Effects of Enterococcus faecalis fsr genes on production of gelatinase and a serine protease and virulence. Infect Immun 68:2579–2586CrossRefGoogle Scholar
  76. Qin X, Singh KV, Weinstock GM, Murray BE (2001) Characterization of Fsr, a regulator controlling expression of gelatinase and serine protease in Enterococcus faecalis OG1RF. J Bacteriol 183:3372–3382CrossRefGoogle Scholar
  77. Rincé A, Flahaut S, Auffray Y (2000) Identification of general stress genes in Enterococcus faecalis. Int J Food Microbiol 55:87–91CrossRefGoogle Scholar
  78. Rincé A, Giard JC, Pichereau V, Flahaut S, Auffray Y (2001) Identification and characterization of gsp65, an organic hydroperoxide resistance (ohr) gene encoding a general stress protein in Enterococcus faecalis. J Bacteriol 183:1482–1488CrossRefGoogle Scholar
  79. Rincé A, Uguen M, Le Breton Y, Giard J, Flahaut S, Dufour A, Auffray Y (2002) The Enterococcus faecalis gene encoding the novel general stress protein Gsp62. Microbiology 148:703–711Google Scholar
  80. Rincé A, Le Breton Y, Verneuil N, Giard JC, Hartke A, Auffray Y (2003) Physiological and molecular aspects of Enterococcus faecalis bile salts response. Int J Food Microbiol 88:207–213CrossRefGoogle Scholar
  81. Ross RP, Claiborne A (1997) Evidence for regulation of the NADH peroxidase gene (npr) from Enterococcus faecalis by OxyR. FEMS Microbiol Lett 151:177–183CrossRefGoogle Scholar
  82. Scott JR, Bringel F, Marra D, Van Alstine G, Rudy CK (1994) Conjugative transposition of Tn916: preferred targets and evidence for conjugative transfer of a single strand and for a double-stranded circular intermediate. Mol Microbiol 11:1099–1108CrossRefGoogle Scholar
  83. Shepard BD, Gilmore MS (2002) Differential expression of virulence-related genes in Enterococcus faecalis in response to biological cues in serum and urine. Infect Immun 70:4344–4352CrossRefGoogle Scholar
  84. Sherman JM (1937) The enterococci. Bacteriol Rev 1:3–97Google Scholar
  85. Sherman JM (1938) The enterococci and related streptococci. J Bacteriol 35:81–93Google Scholar
  86. Sifri CD, Mylonakis E, Singh KV, Qin X, Garsin DA, Murray BE, Ausubel FM, Calderwood SB (2002) Virulence effect of Enterococcus faecalis protease genes and quorum-sensing locus fsr in Caenorhabditis elegans and mice. Infect Immun 70:5647–5650CrossRefGoogle Scholar
  87. Solheim M, Aakra A, Vebo H, Snipen L, Nes I (2007) Transcriptional response of Enterococcus faecalis V583 to bovine bile and sodium dodecyl sulphate. J Bacteriol 73:5767–5774Google Scholar
  88. Spory A, Bosserhoff A, von Rhein C, Goebel W, Ludwig A (2002) Differential regulation of multiple proteins of Escherichia coli and Salmonella enterica serovar Typhimurium by the transcriptional regulator SlyA. J Bacteriol 184: 3549–3559CrossRefGoogle Scholar
  89. Stiles ME, Holzapfel WH (1997) Lactic acid bacteria of foods and their current taxonomy. Int J Food Microbiol 36:1–29CrossRefGoogle Scholar
  90. Stock AM, Robinson VL, Goudreau PN (2000) Two-component signal transduction. Annu Rev Biochem 69:183–215CrossRefGoogle Scholar
  91. Storz G, Imlay JA (1999) Oxidative stress. Curr Opin Microbiol 2:188–194CrossRefGoogle Scholar
  92. Teng F, Wang L, Singh KV, Murray BE, Weinstock GM (2002) Involvement of PhoP-PhoS homologs in Enterococcus faecalis virulence. Infect Immun 70:1991–1996CrossRefGoogle Scholar
  93. Teng F, Nannini EC, Murray BE (2005) Importance of gls24 in virulence and stress response of Enterococcus faecalis and use of the Gls24 protein as a possible immunotherapy target. J Infect Dis 191:472–480CrossRefGoogle Scholar
  94. Thammavongs B, Corroler D, Panoff JM, Auffray Y, Boutibonnes P (1996) Physiological response of Enterococcus faecalis JH2-2 to cold shock: growth at low temperatures and freezing/thawing challenge. Lett Appl Microbiol 23:398–402CrossRefGoogle Scholar
  95. Verneuil N, Le Breton Y, Hartke A, Auffray Y, Giard JC (2004a) Identification of a new oxidative stress transcriptional regulator in Enterococcus faecalis. Lait 84:69–76CrossRefGoogle Scholar
  96. Verneuil N, Sanguinetti M, Le Breton Y, Posteraro B, Fadda G, Auffray Y, Hartke A, Giard JC (2004b) Effects of the Enterococcus faecalis hypR gene encoding a new transcriptional regulator on oxidative stress response and intracellular survival within macrophages. Infect Immun 72:4424–4431CrossRefGoogle Scholar
  97. Verneuil N, Rincé A, Sanguinetti M, Posteraro B, Fadda G, Auffray Y, Hartke A, Giard JC (2005) Contribution of a PerR-like regulator to the oxidative-stress response and virulence of Enterococcus faecalis. Microbiology 151:3997–4004CrossRefGoogle Scholar
  98. Verneuil N, Mazé A, Sanguinetti M, Laplace J, Benachour A, Auffray Y, Giard J, Hartke A (2006) Implication of (Mn)superoxide dismutase of Enterococcus faecalis in oxidative stress responses and survival inside macrophages. Microbiology 152:2579–2589CrossRefGoogle Scholar
  99. Werner G, Coque TM, Hammerum AM, Hope R, Hryniewicz W, Johnson A, Klare I, Kristinsson KG, Leclercq R, Lester CH, Lillie M, Novais C, Olsson-Liljequist B, Peixe LV, Sadowy E, Simonsen GS, Top J, Vuopio-Varkila J, Willems RJ, Witte W, Woodford N (2008) Emergence and spread of vancomycin resistance among enterococci in Europe. Eur Surveill 13:1–11Google Scholar
  100. Wu RY, Zhang RG, Zagnitko O, Dementieva I, Maltzev N, Watson JD, Laskowski R, Gornicki P, Joachimiak A (2003) Crystal structure of Enterococcus faecalis SlyA-like transcriptional factor. J Biol Chem 278: 20240–20244CrossRefGoogle Scholar
  101. Yother J, Trieu-Cuot P, Klaenhammer TR, de Vos WM (2002) Genetics of streptococci, lactococci, and enterococci: review of the Sixth International Conference. J Bacteriol 84:6085–6092CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Yanick Auffray
    • 1
  • Abdellah Benachour
    • 2
  • Aurélie Budin-Verneuil
    • 2
  • Jean-Christophe Giard
    • 2
  • Axel Hartke
    • 2
  • Vianney Pichereau
    • 2
  • Alain Rincé
    • 2
  • Nicolas Sauvageot
    • 2
  • Nicolas Verneuil
    • 2
  1. 1.Laboratoire de Microbiologie de l’Environnement, USC INRA2017/EA UCBN956Université de CaenCaen CedexFrance
  2. 2.Laboratoire de Microbiologie de l’EnvironnementUniversité de CaenCaen CedexFrance

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