The viable but nonculturable state and starvation are different stress responses of Enterococcus faecalis, as determined by proteome analysis

Journal of Bacteriology

Volumn 184, Issue 23, 2002, Pages 6739-6745

  Heim, Sabina ^a   Lleo, Maria Del Mar ^a   Bonato, Barbara ^a   Guzman, Carlos A ^a   Canepari, Pietro ^a  

^a HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEOME;

ARTICLE; BACTERIAL GROWTH; CONTROLLED STUDY; ENTEROCOCCUS FAECALIS; ENVIRONMENTAL FACTOR; LIFE CYCLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STARVATION; STRESS;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; ENTEROCOCCUS FAECALIS; GENE EXPRESSION REGULATION, BACTERIAL; HEAT-SHOCK RESPONSE; MOLECULAR SEQUENCE DATA; PROTEOME; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, BACTERIAL; RNA, MESSENGER;

BACTERIA (MICROORGANISMS); ENTEROCOCCUS; ENTEROCOCCUS FAECALIS; POSIBACTERIA;

EID: 0036889302     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.184.23.6739-6745.2002     Document Type: Article

References (32)

1. Barcina, I., P. Lebaron, and J. Vives-Rego. 1997. Survival of allochthonous bacteria in aquatic systems: A biological approach. FEMS Microbiol. Ecol. 23:1-9.
2. Bergmann, S., M. Rohde, S. Gursharan S. Chhatwal, and S. Hammer-schmidt. 2001. α-enolase of Streptococcus pneumoniae is a plasmin(ogen)-binding protein displayed on the bacterial cell surface. Mol. Microbiol. 40:1273-1287.
3. Blum, H., H. Beier, and H. J. Gross. 1987. Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 8:93-99.
4. Colwell, R. R. 2000. Bacterial death revisited, p. 325-342. In R. R. Colwell and D. J. Grimes (ed.), Nonculturable Microorganisms in the Environment. ASM Press, Washington, D.C.
5. Edmond, M. B., J. F. Ober, J. D. Dawson, D. L. Weinbaum, and R. P. Wenzel. 1996. Vancomycin-resistant enterococcal bacteremia: Natural history and attributable mortality. Clin. Infect. Dis. 23:1234-1239.
6. Giard, J. C., A. Hartke, S. Flahaut, A. Benachour, P. Boutibonnes, and Y. Auffray. 1996. Starvation-induced multiresistance in Enterococcus faecalis JH2-2. Curr. Microbiol. 32:264-271.
7. Giard, J. C., A. Hartke, S. Flahaut, P. Boutibonnes, and Y. Auffray. 1997. Glucose starvation response in Enterococcus faecalis JH2-2: Survival and protein analysis. Res. Microbiol. 148:27-35.
8. Giard, J. C., J. M. Laplace, A. Rincé, V. Pichereau, A. Benachour, C. Leboeuf, S. Flahaut, Y. Auffray, and A. Hartke. 2001. The stress proteome of Enterococcus faecalis. Electrophoresis 22:2947-2954.
9. Görg, A., G. Boguth, C. Obermaier, A. Posch, and W. Weiss. 1995. Two-dimensional polyacrylamide gel electrophoresis with immobilized pH gradients in the first dimension (IPG-DALT): The state of the art and the controversy of vertical versus horizontal systems. Electrophoresis 16:1079-1086.
10. Hartke, A., J. C. Giard, J. M. Laplace, and Y. Auffray. 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. 64:4238-4245.
11. Kogure, K., U. Simidu, and N. Taga. 1979. A tentative direct microscopic method for counting living bacteria. Can. J. Microbiol. 25:415-420.
12. Kurath, G., and Y. Morita. 1983. Starvation-survival physiological studies of a marine Pseudomonas sp. Appl. Environ. Microbiol. 45:1206-1211.
13. Leboeuf, C., L. Leblanc, Y. Auffray, and A. Hartke. 2000. Characterization of the ccpA gene of Enterococcus faecalis: Identification of starvation-inducible proteins regulated by CcpA. J. Bacteriol. 182:5799-5806.
14. Lleo, M. D. M., B. Bonato, M. C. Taft, C. Signoretto, M. Boaretti, and P. Canepari. 2001. Resuscitation rate in different enterococcal species in the viable but non-culturable state. J. Appl. Microbiol. 91:1095-1102.
15. Lleo, M. D. M., M. C. Taft, C. Signoretto, C. Dal Cero, and P. Canepari. 1999. Competitive polymerase chain reaction for quantification of nonculturable Enterococcus faecalis cells in lake water. FEMS Microbiol. Ecol. 30:345-353.
16. Lleo, M. D. M., M. C. Taft, and P. Canepari. 1998. Nonculturable Enterococcus faecalis cells are metabolically active and capable of resuming active growth. Syst. Appl. Microbiol. 21:333-339.
17. Lleò, M. D. M., S. Pierobon, M. C. Taft, C. Signoretto, and P. Canepari. 2000. mRNA detection by reverse transcription-PCR for monitoring viability over time in an Enterococcus faecalis viable but nonculturable population maintained in a laboratory microcosm. Appl. Environ. Microbiol. 66:4564-4567.
18. Morita, R. Y. 1993. Bioavailability of energy and the starvation state, p. 8-16. In S. Kjelleberg (ed.), Starvation in Bacteria. Plenum Press, Inc., New York, N.Y.
19. Oliver, J. D. 2000. The public health significance of viable but nonculturable bacteria, p. 277-300. In R. R. Colwell and D. J. Grimes (ed.), Nonculturable microorganisms in the environment. ASM Press, Washington, D.C.
20. Oliver, J. D., L. Nilsson, and S. Kjelleberg. 1991. Formation of nonculturable Vibrio vulnificus cells and its relationship to the starvation state. Appl. Environ. Microbiol. 57:2640-2644.
21. Paludan-Muller, C., D. Weichart, D. McDougald, and S. Kjelleberg. 1996. Analysis of starvation conditions that allow for prolonged culturability of Vibrio vulnificus at low temperature. Microbiology. 142:1675-1684.
22. Pruzzo, C., R. Tarsi, M. M. Lleó, C. Signoretto, M. Zampini, R. R. Colwell, and P. Canepari. 2002. In vitro adhesion to human cells by viable but nonculturable Enterococcus faecalis. Curr. Microbiol. 45:105-110.
23. Robbi, C., C. Signoretto, M. Boaretti, and P. Canepari. 1996. The gene encoding for penicillin binding protein 5 of Enterococcus faecalis is useful for development of a species-specific DNA probe. Microb. Drug Resist. 2:215-218.
24. Roszak, D. B., and R. R. Colwell. 1987. Survival strategies of bacteria in the natural environment. Microbiol. Rev. 51:365-379.
25. Schmi, R., E. M. Uhlemann, L. Nolden, G. Wersch, R. Hecker, T. Hermann, A. Marx, and A. Burkovski. 2000. Response to nitrogen starvation in Corynebacterium glutamicum. FEMS Microbiol. Lett. 187:83-88.
26. Seshadri, R., L. R. Hendrix, and J. E. Samuel. 1999. Differential expression of translational elements by life cycle variants of Coxiella burnetii. Infect. Immun. 67:6026-6033.
27. Signoretto, C., M. D. M. Lleb, M. C. Taft, and P. Canepari. 2000. Cell wall chemical composition of Enterococcus faecalis in the viable but nonculturable state. Appl. Environ. Microbiol. 66:1953-1959.
28. Stülke, J., and W. Hillen. 2000. Regulation of carbon metabolism in Bacillus species. Annu. Rev. Microbiol. 54:849-880.
29. Toranzos, G. A., and G. A. McFeters. 1997. Detection of indicator microorganisms in environmental freshwaters and drinking waters, p. 184-194. In C. J. Hurst, G. R. Knudsen, M. J. McInerney, L. D. Stetzenbach, and M. V. Walter (ed.). Manual of Environmental Microbiology. ASM Press, Washington, D.C.
30. Wissing, J., S. Heim, L. Flohè, U. Bilitewski, and R. Frank. 2000. Enrichment of hydrophobic proteins via Triton X-114 phase partitioning and hydroxyapatite column chromatography for mass spectrometry. Electrophoresis 21:2589-2593.
31. Wong, D. K., B. Lee, M. A. Horwitz, and B. W. Gibson. 1999. Identification of Fur, aconitase, and other proteins expressed by Mycobacterium tuberculosis under conditions of low and high concentrations of iron by combined two-dimensional gel electrophoresis and mass spectrometry. Infect. Immun. 67:327-336.
32. Young, C. C., and R. W. Bernlohr. 1991. Elongation factor Tu is methylated in response to nutrient deprivation in Escherichia coli. J. Bacteriol. 173:3096-3100.