CymR, the master regulator of cysteine metabolism in Staphylococcus aureus, controls host sulphur source utilization and plays a role in biofilm formation

Molecular Microbiology

Volumn 73, Issue 2, 2009, Pages 194-211

  Soutourina, Olga ^a   Poupel, Olivier ^a   Coppée, Jean Yves ^b   Danchin, Antoine ^a   Msadek, Tarek ^a   Martin Verstraete, Isabelle ^a  

^a CNRS   (France)

^b INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; AMINO ACID TRANSPORTER; BACTERIAL PROTEIN; BETA GALACTOSIDASE; COMPLEMENTARY DNA; CYSTEINE; CYSTINE; HOMOCYSTEINE; METHIONINE; RNA; SULFUR; TAURINE; THIOSULFATE; TRANSCRIPTOME;

ADAPTATION; AMINO ACID METABOLISM; ARTICLE; BACILLUS SUBTILIS; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIUM CULTURE; BACTERIUM MUTANT; BIOFILM; CYMR GENE; DNA BINDING; DNA PROTEIN COMPLEX; ENZYME ACTIVITY; ESCHERICHIA COLI; GENE EXPRESSION; GENE REPRESSION; HOST; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; STAPHYLOCOCCUS AUREUS; SURVIVAL; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; WESTERN BLOTTING;

BACTERIAL PROTEINS; BIOFILMS; CYSTINE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; REPRESSOR PROTEINS; RNA, BACTERIAL; STAPHYLOCOCCUS AUREUS; SULFUR;

STAPHYLOCOCCUS AUREUS;

EID: 67650462310     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2009.06760.x     Document Type: Article

References (83)

1. Albanesi, D., Mansilla, M.C., Schujman, G.E. de Mendoza, D. (2005) Bacillus subtilis cysteine synthetase is a global regulator of the expression of genes involved in sulfur assimilation. J Bacteriol 187 : 7631 7638. (Pubitemid 41587701)
2. Arnaud, M., Chastanet, A. Debarbouille, M. (2004) New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Appl Environ Microbiol 70 : 6887 6891. (Pubitemid 39518603)
3. Ayala-Castro, C., Saini, A. Outten, F.W. (2008) Fe-S cluster assembly pathways in bacteria. Microbiol Mol Biol Rev 72 : 110 125.
4. Becker, S.A. Palsson, B.O. (2005) Genome-scale reconstruction of the metabolic network in Staphylococcus aureus N315: an initial draft to the two-dimensional annotation. BMC Microbiol 5 : 8.
5. Beenken, K.E., Dunman, P.M., McAleese, F., Macapagal, D., Murphy, E., Projan, S.J., et al. (2004) Global gene expression in Staphylococcus aureus biofilms. J Bacteriol 186 : 4665 4684. (Pubitemid 38891030)
6. Bernier, S.P. Sokol, P.A. (2005) Use of suppression-subtractive hybridization to identify genes in the Burkholderia cepacia complex that are unique to Burkholderia cenocepacia. J Bacteriol 187 : 5278 5291. (Pubitemid 41022947)
7. Bhave, D.P., Muse, W.B., 3rd Carroll, K.S. (2007) Drug targets in mycobacterial sulfur metabolism. Infect Disord Drug Targets 7 : 140 158. (Pubitemid 47099125)
8. Bieber, E.J. Wilkinson, B.J. (1984) Sodium-dependent uptake of taurine in encapsulated Staphylococcus aureus strain M. Biochim Biophys Acta 770 : 127 135.
9. Bischoff, M., Dunman, P., Kormanec, J., Macapagal, D., Murphy, E., Mounts, W., et al. (2004) Microarray-based analysis of the Staphylococcus aureus sigmaB regulon. J Bacteriol 186 : 4085 4099. (Pubitemid 38802556)
10. Bodenmiller, D.M. Spiro, S. (2006) The yjeB (nsrR) gene of Escherichia coli encodes a nitric oxide-sensitive transcriptional regulator. J Bacteriol 188 : 874 881. (Pubitemid 43146402)
11. Bogdan, J.A., Nazario-Larrieu, J., Sarwar, J., Alexander, P. Blake, M.S. (2001) Bordetella pertussis autoregulates pertussis toxin production through the metabolism of cysteine. Infect Immun 69 : 6823 6830. (Pubitemid 32995441)
12. Boles, B.R. Horswill, A.R. (2008) Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog 4 : e1000052.
13. Brady, R.A., Leid, J.G., Camper, A.K., Costerton, J.W. Shirtliff, M.E. (2006) Identification of Staphylococcus aureus proteins recognized by the antibody-mediated immune response to a biofilm infection. Infect Immun 74 : 3415 3426. (Pubitemid 43794532)
14. Burguiere, P., Auger, S., Hullo, M.F., Danchin, A. Martin-Verstraete, I. (2004) Three different systems participate in L-cystine uptake in Bacillus subtilis. J Bacteriol 186 : 4875 4884. (Pubitemid 38970814)
15. Burguiere, P., Fert, J., Guillouard, I., Auger, S., Danchin, A. Martin-Verstraete, I. (2005) Regulation of the Bacillus subtilis ytmI operon, involved in sulfur metabolism. J Bacteriol 187 : 6019 6030. (Pubitemid 41262799)
16. Cassat, J., Dunman, P.M., Murphy, E., Projan, S.J., Beenken, K.E., Palm, K.J., et al. (2006) Transcriptional profiling of a Staphylococcus aureus clinical isolate and its isogenic agr and sarA mutants reveals global differences in comparison to the laboratory strain RN6390. Microbiology 152 : 3075 3090. (Pubitemid 44542387)
17. Choi, S.Y., Reyes, D., Leelakriangsak, M. Zuber, P. (2006) The global regulator Spx functions in the control of organosulfur metabolism in Bacillus subtilis. J Bacteriol 188 : 5741 5751. (Pubitemid 44384082)
18. Cucarella, C., Solano, C., Valle, J., Amorena, B., Lasa, I. Penades, J.R. (2001) Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J Bacteriol 183 : 2888 2896. (Pubitemid 32319293)
19. Derre, I., Rapoport, G. Msadek, T. (2000) The CtsR regulator of stress response is active as a dimer and specifically degraded in vivo at 37 degrees C. Mol Microbiol 38 : 335 347. (Pubitemid 30815991)
20. Dubrac, S., Boneca, I.G., Poupel, O. Msadek, T. (2007) New insights into the WalK/WalR (YycG/YycF) essential signal transduction pathway reveal a major role in controlling cell wall metabolism and biofilm formation in Staphylococcus aureus. J Bacteriol 189 : 8257 8269. (Pubitemid 350178938)
21. Dunman, P.M., Murphy, E., Haney, S., Palacios, D., Tucker-Kellogg, G., Wu, S., et al. (2001) Transcription profiling-based identification of Staphylococcus aureus genes regulated by the agr and/or sarA loci. J Bacteriol 183 : 7341 7353. (Pubitemid 33121868)
22. Ejim, L.J., D'Costa, V.M., Elowe, N.H., Loredo-Osti, J.C., Malo, D. Wright, G.D. (2004) Cystathionine beta-lyase is important for virulence of Salmonella enterica serovar Typhimurium. Infect Immun 72 : 3310 3314. (Pubitemid 38697753)
23. Even, S., Burguière, P., Auger, S., Soutourina, O., Danchin, A. Martin-Verstraete, I. (2006) Global control of cysteine metabolism by CymR in Bacillus subtilis. J Bacteriol 188 : 2184 2197. (Pubitemid 43376472)
24. Filenko, N., Spiro, S., Browning, D.F., Squire, D., Overton, T.W., Cole, J. Constantinidou, C. (2007) The NsrR regulon of Escherichia coli K-12 includes genes encoding the hybrid cluster protein and the periplasmic, respiratory nitrite reductase. J Bacteriol 189 : 4410 4417. (Pubitemid 46919627)
25. Gagnon, Y., Breton, R., Putzer, H., Pelchat, M., Grunberg-Manago, M. Lapointe, J. (1994) Clustering and co-transcription of the Bacillus subtilis genes encoding the aminoacyl-tRNA synthetases specific for glutamate and for cysteine and the first enzyme for cysteine biosynthesis. J Biol Chem 269 : 7473 7482. (Pubitemid 24217950)
26. Garzoni, C., Francois, P., Huyghe, A., Couzinet, S., Tapparel, C., Charbonnier, Y., et al. (2007) A global view of Staphylococcus aureus whole genome expression upon internalization in human epithelial cells. BMC Genomics 8 : 171.
27. Giehl, T.J., Qoronfleh, M.W. Wilkinson, B.J. (1987) Transport, nutritional and metabolic studies of taurine in staphylococci. J Gen Microbiol 133 : 849 856. (Pubitemid 17062674)
28. Gooder, H. Gehring, L.B. (1954) Inhibition by cystine of lecithinase (alpha-toxin) production in Clostridium welchii (perfringens) BP6K. Nature 174 : 1054 1055.
29. Gordon, R.J. Lowy, F.D. (2008) Pathogenesis of methicillin-resistant Staphylococcus aureus infection. Clin Infect Dis 46 (Suppl. 5 S350 S359.
30. Gotz, F. (2002) Staphylococcus and biofilms. Mol Microbiol 43 : 1367 1378. (Pubitemid 34595531)
31. Graham, J.E. Wilkinson, B.J. (1992) Staphylococcus aureus osmoregulation: roles for choline, glycine betaine, proline, and taurine. J Bacteriol 174 : 2711 2716.
32. Grifantini, R., Bartolini, E., Muzzi, A., Draghi, M., Frigimelica, E., Berger, J., et al. (2002) Previously unrecognized vaccine candidates against group B meningococcus identified by DNA microarrays. Nat Biotechnol 20 : 914 921. (Pubitemid 35001129)
33. Guillouard, I., Auger, S., Hullo, M.F., Chetouani, F., Danchin, A. Martin-Verstraete, I. (2002) Identification of Bacillus subtilis CysL, a regulator of the cysJI operon, which encodes sulfite reductase. J Bacteriol 184 : 4681 4689. (Pubitemid 34898254)
34. Heinemann, M., Kummel, A., Ruinatscha, R. Panke, S. (2005) In silico genome-scale reconstruction and validation of the Staphylococcus aureus metabolic network. Biotechnol Bioeng 92 : 850 864.
35. Horsburgh, M.J., Aish, J.L., White, I.J., Shaw, L., Lithgow, J.K. Foster, S.J. (2002) sigmaB modulates virulence determinant expression and stress resistance: characterization of a functional rsbU strain derived from Staphylococcus aureus 8325-4. J Bacteriol 184 : 5457 5467. (Pubitemid 35024393)
36. Hryniewicz, M., Sirko, A., Palucha, A., Bock, A. Hulanicka, D. (1990) Sulfate and thiosulfate transport in Escherichia coli K-12: identification of a gene encoding a novel protein involved in thiosulfate binding. J Bacteriol 172 : 3358 3366. (Pubitemid 20179795)
37. Hullo, M.F., Auger, S., Dassa, E., Danchin, A. Martin-Verstraete, I. (2004) The metNPQ operon of Bacillus subtilis encodes an ABC permease transporting methionine sulfoxide, D- and L-methionine. Res Microbiol 155 : 80 86. (Pubitemid 38249557)
38. Hullo, M.F., Auger, S., Soutourina, O., Barzu, O., Yvon, M., Danchin, A. Martin-Verstraete, I. (2007) Conversion of methionine to cysteine in Bacillus subtilis and its regulation. J Bacteriol 189 : 187 197. (Pubitemid 46036234)
39. Ito, K. Inaba, K. (2008) The disulfide bond formation (Dsb) system. Curr Opin Struct Biol 18 : 450 458.
40. Karlsson, S., Lindberg, A., Norin, E., Burman, L.G. Akerlund, T. (2000) Toxins, butyric acid, and other short-chain fatty acids are coordinately expressed and down-regulated by cysteine in Clostridium difficile. Infect Immun 68 : 5881 5888. (Pubitemid 30739378)
41. Kredich, N.M. (1996) Biosynthesis of cysteine. In Escherichia coli and Salmonella, Cellular and Molecular Biology. Neidhardt, F.C. (eds). Washington, DC : American Society for Microbiology Press, pp. 514 527.
42. Krin, E., Chakroun, N., Turlin, E., Givaudan, A., Gaboriau, F., Bonne, I., et al. (2006) Pleiotropic role of quorum-sensing autoinducer 2 in Photorhabdus luminescens. Appl Environ Microbiol 72 : 6439 6451. (Pubitemid 44582879)
43. Kunst, F. Rapoport, G. (1995) Salt stress is an environmental signal affecting degradative enzyme synthesis in Bacillus subtilis. J Bacteriol 177 : 2403 2407.
44. Lauderdale, K.J., Boles, B.R., Cheung, A.L. Horswill, A.R. (2009) Interconnections between Sigma B, agr, and proteolytic activity in Staphylococcus aureus biofilm maturation. Infect Immun 77 : 1623 1635.
45. Lestrate, P., Delrue, R.M., Danese, I., Didembourg, C., Taminiau, B., Mertens, P., et al. (2000) Identification and characterization of in vivo attenuated mutants of Brucella melitensis. Mol Microbiol 38 : 543 551. (Pubitemid 30947468)
46. Liang, X., Zheng, L., Landwehr, C., Lunsford, D., Holmes, D. Ji, Y. (2005) Global regulation of gene expression by ArlRS, a two-component signal transduction regulatory system of Staphylococcus aureus. J Bacteriol 187 : 5486 5492. (Pubitemid 41022967)
47. Liles, W.C., Thomsen, A.R., O'Mahony, D.S. Klebanoff, S.J. (2001) Stimulation of human neutrophils and monocytes by staphylococcal phenol-soluble modulin. J Leukoc Biol 70 : 96 102. (Pubitemid 32613668)
48. Lithgow, J.K., Hayhurst, E.J., Cohen, G., Aharonowitz, Y. Foster, S.J. (2004) Role of a cysteine synthase in Staphylococcus aureus. J Bacteriol 186 : 1579 1590. (Pubitemid 38314502)
49. Livak, K.J. Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25 : 402 408. (Pubitemid 34164012)
50. Lowy, F.D. (1998) Staphylococcus aureus infections. N Engl J Med 339 : 520 532.
51. Mack, D., Davies, A.P., Harris, L.G., Rohde, H., Horstkotte, M.A. Knobloch, J.K. (2007) Microbial interactions in Staphylococcus epidermidis biofilms. Anal Bioanal Chem 387 : 399 408. (Pubitemid 46067457)
52. Masip, L., Veeravalli, K. Georgiou, G. (2006) The many faces of glutathione in bacteria. Antioxid Redox Signal 8 : 753 762. (Pubitemid 44036494)
53. Maxam, A.M. Gilbert, W. (1977) A new method for sequencing DNA. Proc Natl Acad Sci USA 74 : 560 564. (Pubitemid 8038842)
54. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY : Cold Spring Harbor Laboratory.
55. Nagarajan, V. Elasri, M.O. (2007) SAMMD: Staphylococcus aureus microarray meta-database. BMC Genomics 8 : 351.
56. Novick, R.P. (1991) Genetic systems in staphylococci. Methods Enzymol 204 : 587 636.
57. Nygard, O., Vollset, S.E., Refsum, H., Brattstrom, L. Ueland, P.M. (1999) Total homocysteine and cardiovascular disease. J Intern Med 246 : 425 454. (Pubitemid 29529786)
58. O'Gara, J.P. (2007) ica and beyond: biofilm mechanisms and regulation in Staphylococcus epidermidis and Staphylococcus aureus. FEMS Microbiol Lett 270 : 179 188. (Pubitemid 46597372)
59. van der Ploeg, J.R., Cummings, N.J., Leisinger, T. Connerton, I.F. (1998) Bacillus subtilis genes for the utilization of sulfur from aliphatic sulfonates. Microbiology 144 : 2555 2561. (Pubitemid 28457165)
60. van der Ploeg, J.R., Barone, M. Leisinger, T. (2001) Functional analysis of the Bacillus subtilis cysK and cysJI genes. FEMS Microbiol Lett 201 : 29 35. (Pubitemid 32607515)
61. Resch, A., Leicht, S., Saric, M., Pasztor, L., Jakob, A., Gotz, F. Nordheim, A. (2006) Comparative proteome analysis of Staphylococcus aureus biofilm and planktonic cells and correlation with transcriptome profiling. Proteomics 6 : 1867 1877.
62. Rey, D.A., Nentwich, S.S., Koch, D.J., Ruckert, C., Puhler, A., Tauch, A. Kalinowski, J. (2005) The McbR repressor modulated by the effector substance S-adenosylhomocysteine controls directly the transcription of a regulon involved in sulphur metabolism of Corynebacterium glutamicum ATCC 13032. Mol Microbiol 56 : 871 887. (Pubitemid 40646762)
63. Rodionov, D.A., Vitreschak, A.G., Mironov, A.A. Gelfand, M.S. (2004) Comparative genomics of the methionine metabolism in Gram-positive bacteria: a variety of regulatory systems. Nucleic Acids Res 32 : 3340 3353. (Pubitemid 39117450)
64. Ruckert, C., Milse, J., Albersmeier, A., Koch, D.J., Puhler, A. Kalinowski, J. (2008) The dual transcriptional regulator CysR in Corynebacterium glutamicum ATCC 13032 controls a subset of genes of the McbR regulon in response to the availability of sulphide acceptor molecules. BMC Genomics 9 : 483.
65. Sambrook, J., Fritsch, E.F. Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor, NY : Cold Spring Harbor Laboratory.
66. Schuller-Levis, G.B. Park, E. (2003) Taurine: new implications for an old amino acid. FEMS Microbiol Lett 226 : 195 202. (Pubitemid 38444940)
67. Schwartz, C.J., Giel, J.L., Patschkowski, T., Luther, C., Ruzicka, F.J., Beinert, H. Kiley, P.J. (2001) IscR, an Fe-S cluster-containing transcription factor, represses expression of Escherichia coli genes encoding Fe-S cluster assembly proteins. Proc Natl Acad Sci USA 98 : 14895 14900. (Pubitemid 34013941)
68. Seidl, K., Goerke, C., Wolz, C., Mack, D., Berger-Bachi, B. Bischoff, M. (2008) Staphylococcus aureus CcpA affects biofilm formation. Infect Immun 76 : 2044 2050. (Pubitemid 351656137)
69. Shelver, D., Rajagopal, L., Harris, T.O. Rubens, C.E. (2003) MtaR, a regulator of methionine transport, is critical for survival of group B streptococcus in vivo. J Bacteriol 185 : 6592 6599. (Pubitemid 37385878)
70. Sirko, A., Zatyka, M., Sadowy, E. Hulanicka, D. (1995) Sulfate and thiosulfate transport in Escherichia coli K-12: evidence for a functional overlapping of sulfate- and thiosulfate-binding proteins. J Bacteriol 177 : 4134 4136.
71. Smith, K., Perez, A., Ramage, G., Lappin, D., Gemmell, C.G. Lang, S. (2008) Biofilm formation by Scottish clinical isolates of Staphylococcus aureus. J Med Microbiol 57 : 1018 1023.
72. Soutourina, O. Martin-Verstraete, I. (2007) Global regulatory network of sulfur metabolism in Bacillus subtilis. In Global Regulatory Networks in Bacillus subtilis. Fujita, Y. (ed.). Kerala, India : Transworld Research Network, pp. 111 141.
73. Sperandio, B., Polard, P., Ehrlich, D.S., Renault, P. Guedon, E. (2005) Sulfur amino acid metabolism and its control in Lactococcus lactis IL1403. J Bacteriol 187 : 3762 3778. (Pubitemid 40705580)
74. Sperandio, B., Gautier, C., McGovern, S., Ehrlich, D.S., Renault, P., Martin-Verstraete, I. Guedon, E. (2007) Control of methionine synthesis and uptake by MetR and homocysteine in Streptococcus mutans. J Bacteriol 189 : 7032 7044. (Pubitemid 47525448)
75. Stülke, J., Martin-Verstraete, I., Zagorec, M., Rose, M., Klier, A. Rapoport, G. (1997) Induction of the Bacillus subtilis ptsGHI operon by glucose is controlled by a novel antiterminator, GlcT. Mol Microbiol 25 : 65 78. (Pubitemid 27316122)
76. Sullivan, M.A., Yasbin, R.E. Young, F.E. (1984) New shuttle vectors for Bacillus subtilis and Escherichia coli which allow rapid detection of inserted fragments. Gene 29 : 21 26. (Pubitemid 14030928)
77. Tanous, C., Soutourina, O., Raynal, B., Hullo, M.F., Mervelet, P., Gilles, A.M., et al. (2008) The CymR regulator in complex with the enzyme CysK controls cysteine metabolism in Bacillus subtilis. J Biol Chem 283 : 35551 35560.
78. Toledo-Arana, A., Merino, N., Vergara-Irigaray, M., Debarbouille, M., Penades, J.R. Lasa, I. (2005) Staphylococcus aureus develops an alternative, ica-independent biofilm in the absence of the arlRS two-component system. J Bacteriol 187 : 5318 5329. (Pubitemid 41022951)
79. Vitreschak, A.G., Mironov, A.A., Lyubetsky, V.A. Gelfand, M.S. (2008) Comparative genomic analysis of T-box regulatory systems in bacteria. RNA 14 : 717 735.
80. Yao, Y., Sturdevant, D.E. Otto, M. (2005) Genomewide analysis of gene expression in Staphylococcus epidermidis biofilms: insights into the pathophysiology of S. epidermidis biofilms and the role of phenol-soluble modulins in formation of biofilms. J Infect Dis 191 : 289 298. (Pubitemid 40096388)
81. Yeoman, K.H., Curson, A.R., Todd, J.D., Sawers, G. Johnston, A.W. (2004) Evidence that the Rhizobium regulatory protein RirA binds to cis-acting iron-responsive operators (IROs) at promoters of some Fe-regulated genes. Microbiology 150 : 4065 4074. (Pubitemid 40045335)
82. Zeller, T. Klug, G. (2006) Thioredoxins in bacteria: functions in oxidative stress response and regulation of thioredoxin genes. Naturwissenschaften 93 : 259 266. (Pubitemid 43829312)
83. Zhao, C., Moriga, Y., Feng, B., Kumada, Y., Imanaka, H., Imamura, K. Nakanishi, K. (2006) On the interaction site of serine acetyltransferase in the cysteine synthase complex from Escherichia coli. Biochem Biophys Res Commun 341 : 911 916. (Pubitemid 43221752)