Physiological Characterization of a Heme-Deficient Mutant of Staphylococcus aureus by a Proteomic Approach

Journal of Bacteriology

Volumn 185, Issue 23, 2003, Pages 6928-6937

  Kohler, Christian ^a   Von Eiff, Christof ^b   Peters, Georg ^b   Proctor, Richard A ^c   Hecker, Michael ^a   Engelmann, Susanne ^a  

^a UNIVERSITY OF GREIFSWALD   (Germany)

^b UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; ACONITATE HYDRATASE; ADENOSINE TRIPHOSPHATE; ALCOHOL; ALCOHOL DEHYDROGENASE; ARGININE DEIMINASE; BACTERIAL PROTEIN; ENOLASE; FRUCTOSE; GLUCOSE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HEME; LACTATE DEHYDROGENASE; NITRATE; OXYGEN; PHOSPHOGLYCERATE KINASE; PHOSPHOTRANSFERASE; PYRUVATE FORMATE KINASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIUM MUTANT; CONTROLLED STUDY; ELECTRON TRANSPORT; ENZYME ACTIVITY; FERMENTATION; GENETIC TRANSCRIPTION; GLYCOLYSIS; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS; TWO DIMENSIONAL GEL ELECTROPHORESIS; WILD TYPE;

ACETYLTRANSFERASES; ACONITATE HYDRATASE; ADENOSINE TRIPHOSPHATE; ALCOHOL DEHYDROGENASE; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CULTURE MEDIA; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; HEME; L-LACTATE DEHYDROGENASE; MOLECULAR SEQUENCE DATA; MUTATION; PHOSPHOGLYCERATE KINASE; PHOSPHOPYRUVATE HYDRATASE; PROTEOMICS; STAPHYLOCOCCUS AUREUS;

BACTERIA (MICROORGANISMS); POSIBACTERIA; STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS;

EID: 0344393465     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.185.23.6928-6937.2003     Document Type: Article

References (38)

1. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
2. Baumert, N., C. von Eiff, F. Schaaff, G. Peters, R. A. Proctor, and H. G. Sahl. 2002. Physiology and antibiotic susceptibility of Staphylococcus aureus small colony variants. Microb. Drug Resist. 8:253-260.
3. Bernhardt, J., K. Büttner, C. Scharf, and M. Hecker. 1999. Dual channel imaging of two-dimensional electropherograms in Bacillus subtilis. Electrophoresis 20:2225-2240.
4. Casiano-Colon, A., and R. E. Marquis. 1988. Role of the arginine deiminase system in protecting oral bacteria and an enzymatic basis for acid tolerance. Appl. Environ. Microbiol. 54:1318-1324.
5. Cunin, R., N. Glansdorff, A. Pierard, and V. Stalon. 1986. Biosynthesis and metabolism of arginine in bacteria. Microbiol. Rev. 50:314-352.
6. Curran, T. M., Y. Ma, G. C. Rutherford, and R. E. Marquis. 1998. Turning on and turning off the arginine deiminase system in oral streptococci. Can. J. Microbiol. 44:1078-1085.
7. Dunman, P. M., E. Murphy, S. Haney, D. Palacios, G. Tucker-Kellogg, S. Wu, E. L. Brown, R. J. Zagursky, D. Shlaes, and S. J. Projan. 2001. Transcription profiling-based identification of Staphylococcus aureus genes regulated by the agr and/or sarA loci. J. Bacteriol. 183:7341-7353.
8. Gertz, S., S. Engelmann, R. Schmid, K. Ohlsen, J. Hacker, and M. Hecker. 1999. Regulation of sigmaB-dependent transcription of sigB and asp23 in two different Staphylococcus aureus strains. Mol. Gen. Genet. 261:558-566.
9. Granick, S., and S. I. Beale. 1978. Hemes, chlorophylls, and related compounds: biosynthesis and metabolic regulation. Adv. Enzymol. Relat. Areas Mol. Biol. 46:33-203.
10. Hartmann, R., H. D. Sickinger, and D. Oesterhelt. 1980. Anaerobic growth of halobacteria. Proc. Natl. Acad. Sci. USA 77:3821-3825.
11. Jorgensen, E. D., R. K. Durbin, S. S. Risman, and W. T. McAllister. 1991. Specific contacts between the bacteriophage T3, T7, and SP6 RNA polymerases and their promoters. J. Biol. Chem. 266:645-651.
12. Kahl, B., M. Herrmann, A. S. Everding, H. G. Koch, K. Becker, E. Harms, R. A. Proctor, and G. Peters. 1998. Persistent infection with small colony variant strains of Staphylococcus aureus in patients with cystic fibrosis. J. Infect. Dis. 177:1023-1029.
13. Kessler, D., I. Leibrecht, and J. Knappe. 1991. Pyruvate-formate-lyase-deactivase and acetyl-CoA reductase activities of Escherichia coli reside on a polymeric protein particle encoded by adhE. FEBS Lett. 281:59-63.
14. Looney, W. J. 2000. Small-colony variants of Staphylococcus aureus. Br. J. Biomed. Sci. 57:317-322.
15. Maghnouj, A., T. F. de Sousa Cabral, V. Stalon, and C. Vander Wauven. 1998. The arcABDC gene cluster, encoding the arginine deiminase pathway of Bacillus licheniformis, and its activation by the arginine repressor, argR. J. Bacteriol. 180:6468-6475.
16. McNamara, P. J., and R. A. Proctor. 2000. Staphylococcus aureus small colony variants, electron transport and persistent infections. Int. J. Antimicrob. Agents 14:117-122.
17. Nakano, M. M., Y. P. Dailly, P. Zuber, and D. P. Clark. 1997. Characterization of anaerobic fermentative growth of Bacillus subtilis: identification of fermentation end products and genes required for growth. J. Bacteriol. 179:6749-6755.
18. Nakano, M. M., and Y. Zhu. 2001. Involvement of ResE phosphatase activity in down-regulation of ResD-controlled genes in Bacillus subtilis during aerobic growth. J. Bacteriol. 183:1938-1944.
19. Nakano, M. M., Y. Zhu, M. Lacelle, X. Zhang, and F. M. Hulett. 2000. Interaction of ResD with regulatory regions of anaerobically induced genes in Bacillus subtilis. Mol. Microbiol. 37:1198-1207.
20. Nakano, M. M., P. Zuber, P. Glaser, A. Danchin, and F. M. Hulett. 1996. Two-component regulatory proteins ResD-ResE are required for transcriptional activation of fnr upon oxygen limitation in Bacillus subtilis. J. Bacteriol. 178:3796-3802.
21. Peng, H. L., R. P. Novick, B. Kreiswirth, J. Kornblum, and P. Schlievert. 1988. Cloning, characterization, and sequencing of an accessory gene regulator (agr) in Staphylococcus aureus. J. Bacteriol. 170:4365-4372.
22. Proctor, R. A., J. M. Balwit, and O. Vesga. 1994. Variant subpopulations of Staphylococcus aureus as cause of persistent and recurrent infections. Infect. Agents Dis. 3:302-312.
23. Proctor, R. A., P. van Langevelde, M. Kristjansson, J. N. Maslow, and R. D. Arbeit. 1995. Persistent and relapsing infections associated with small-colony variants of Staphylococcus aureus. Clin. Infect. Dis. 20:95-102.
24. Rompf, A., R. Schmid, and D. Jahn. 1998. Changes in protein synthesis as a consequence of heme depletion in Escherichia coli. Curr. Microbiol. 37:226-230.
25. Seifert, H., C. von Eiff, and G. Fatkenheuer. 1999. Fatal case due to methicillin-resistant Staphylococcus aureus small colony variants in an AIDS patient. Emerg. Infect. Dis. 5:450-453.
26. Shafer, W. M., and J. J. Iandolo. 1979. Genetics of staphylococcal enterotoxin B in methicillin-resistant isolates of Staphylococcus aureus. Infect. Immun. 25:902-911.
27. Sun, G., E. Sharkova, R. Chesnut, S. Birkey, M. F. Duggan, A. Sorokin, P. Pujic, S. D. Ehrlich, and F. M. Hulett. 1996. Regulators of aerobic and anaerobic respiration in Bacillus subtilis. J. Bacteriol. 178:1374-1385.
28. Takahashi, N., K. Abbe, S. Takahashi-Abbe, and T. Yamada. 1987. Oxygen sensitivity of sugar metabolism and interconversion of pyruvate formatelyase in intact cells of Streptococcus mutans and Streptococcus sanguis. Infect. Immun. 55:652-656.
29. Throup, J. P., F. Zappacosta, R. D. Lunsford, R. S. Annan, S. A. Carr, J. T. Lonsdale, A. P. Bryant, D. McDevitt, M. Rosenberg, and M. K. Burnham. 2001. The srhSR gene pair from Staphylococcus aureus: genomic and proteomic approaches to the identification and characterization of gene function. Biochemistry 40:10392-10401.
30. Unkrig, V., F. A. Neugebauer, and J. Knappe. 1989. The free radical of pyruvate formate-lyase. Characterization by EPR spectroscopy and involvement in catalysis as studied with the substrate-analogue hypophosphite. Eur. J. Biochem. 184:723-728.
31. Vander Wauven, C., A. Pierard, M. Kley-Raymann, and D. Haas. 1984. Pseudomonas aeruginosa mutants affected in anaerobic growth on arginine: evidence for a four-gene cluster encoding the arginine deiminase pathway. J. Bacteriol. 160:928-934.
32. Vaudaux, P., P. Francois, C. Bisognano, W. L. Kelley, D. P. Lew, J. Schrenzel, R. A. Proctor, P. J. McNamara, G. Peters, and C. Von Eiff. 2002. Increased expression of clumping factor and fibronectin-binding proteins by hemB mutants of Staphylococcus aureus expressing small-colony variant phenotypes. Infect. Immun. 70:5428-5437.
33. von Eiff, C., K. Becker, D. Metze, G. Lubritz, J. Hockmann, T. Schwarz, and G. Peters. 2001. Intracellular persistence of Staphylococcus aureus small-colony variants within keratinocytes: a cause for antibiotic treatment failure in a patient with darier's disease. Clin. Infect. Dis. 32:1643-1647.
34. von Eiff, C., D. Bettin, R. A. Proctor, B. Rolauffs, N. Lindner, W. Winkelmann, and G. Peters. 1997. Recovery of small colony variants of Staphylococcus aureus following gentamicin bead placement for osteomyelitis. Clin. Infect. Dis. 25:1250-1251.
35. von Eiff, C., C. Heilmann, R. A. Proctor, C. Woltz, G. Peters, and F. Gotz. 1997. A site-directed Staphylococcus aureus hemB mutant is a small-colony variant which persists intracellularly. J. Bacteriol. 179:4706-4712.
36. Wetzstein, M., U. Völker, J. Dedio, S. Löbau, U. Zuber, M. Schiesswohl, C. Herget, M. Hecker, and W. Schumann. 1992. Cloning, sequencing, and molecular analysis of the dnaK locus from Bacillus subtilis. J. Bacteriol. 174:3300-3310.
37. Yamada, T., S. Takahashi-Abbe, and K. Abbe. 1985. Effects of oxygen on pyruvate formate-lyase in situ and sugar metabolism of Streptococcus mutans and Streptococcus sanguis. Infect. Immun. 47:129-134.
38. Ziebandt, A. K., H. Weber, J. Rudolph, R. Schmid, D. Höper, S. Engelmann, and M. Hecker. 2001. Extracellular proteins of Staphylococcus aureus and the role of SarA and sigma B. Proteomics 1:480-493.