Previous Article | Next Article 
Journal of Bacteriology, December 1998, p. 6375-6383, Vol. 180, No. 23
0021-9193/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
A Two-Component Signal Transduction System
Essential for Growth of Bacillus subtilis: Implications for
Anti-Infective Therapy
Céline
Fabret and
James A.
Hoch*
Division of Cellular Biology, Department of
Molecular and Experimental Medicine, The Scripps Research
Institute, La Jolla, California
Received 24 August 1998/Accepted 25 September 1998
A two-component signal transduction system encoded by the
yycF and yycG genes is part of an operon
containing three genes, yycH, yycI, and
yycJ, with no known function and a gene, yycK, coding for an HtrA-like protease. This operon was transcribed during
growth, and its transcription shut down as the cells approached stationary phase. This decreased transcription was not Spo0A dependent. The HtrA protease gene was separately controlled during sporulation from a
G promoter. Studies using insertional
inactivation plasmids revealed that neither yycF nor
yycG could be inactivated, whereas the other genes were
inactivated without loss of viability. A temperature-sensitive YycF
response regulator mutant was isolated and shown to have an H215P
mutation in a putative DNA-binding domain which is closely related to
the OmpR family of response regulators. At the nonpermissive temperature, cultures of the mutant strain stopped growth within 30 min, and this was followed by a decrease in optical density. Microscopically, many of the cells appeared to retain their structure while being empty of their contents. The essential processes regulated by this two-component system remain unknown. A search of the genome databases revealed YycF, YycG, and YycJ homologues encoded by three
linked genes in Streptococcus pyogenes. The high level of identity of these proteins (71% for YycF) suggests that this system may play a similar role in gram-positive pathogens.
*
Corresponding author. Mailing address: Division of
Cellular Biology, Department of Molecular and Experimental Medicine,
The Scripps Research Institute, 10550 North Torrey Pines Rd., La Jolla, CA 92037. Phone: (619) 784-7905. Fax: (619) 784-7966. E-mail: hoch{at}scripps.edu.

Publication 11729-MEM from the Department of Molecular and
Experimental Medicine at The Scripps Research
Institute.
Journal of Bacteriology, December 1998, p. 6375-6383, Vol. 180, No. 23
0021-9193/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Liu, Y., Burne, R. A.
(2009). Multiple Two-Component Systems Modulate Alkali Generation in Streptococcus gordonii in Response to Environmental Stresses. J. Bacteriol.
191: 7353-7362
[Abstract]
[Full Text]
-
Tremblay, Y. D. N., Lo, H., Li, Y.-H., Halperin, S. A., Lee, S. F.
(2009). Expression of the Streptococcus mutans essential two-component regulatory system VicRK is pH and growth-phase dependent and controlled by the LiaFSR three-component regulatory system. Microbiology
155: 2856-2865
[Abstract]
[Full Text]
-
Azcarate-Peril, M. A., Tallon, R., Klaenhammer, T. R.
(2009). Temporal gene expression and probiotic attributes of Lactobacillus acidophilus during growth in milk. J DAIRY SCI
92: 870-886
[Abstract]
[Full Text]
-
Azcarate-Peril, M. A., Altermann, E., Goh, Y. J., Tallon, R., Sanozky-Dawes, R. B., Pfeiler, E. A., O'Flaherty, S., Buck, B. L., Dobson, A., Duong, T., Miller, M. J., Barrangou, R., Klaenhammer, T. R.
(2008). Analysis of the Genome Sequence of Lactobacillus gasseri ATCC 33323 Reveals the Molecular Basis of an Autochthonous Intestinal Organism. Appl. Environ. Microbiol.
74: 4610-4625
[Abstract]
[Full Text]
-
Chong, P., Drake, L., Biswas, I.
(2008). LiaS Regulates Virulence Factor Expression in Streptococcus mutans. Infect. Immun.
76: 3093-3099
[Abstract]
[Full Text]
-
Winkler, M. E., Hoch, J. A.
(2008). Essentiality, Bypass, and Targeting of the YycFG (VicRK) Two-Component Regulatory System in Gram-Positive Bacteria. J. Bacteriol.
190: 2645-2648
[Full Text]
-
Szurmant, H., Bu, L., Brooks, C. L. III/, Hoch, J. A.
(2008). An essential sensor histidine kinase controlled by transmembrane helix interactions with its auxiliary proteins. Proc. Natl. Acad. Sci. USA
105: 5891-5896
[Abstract]
[Full Text]
-
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
[Abstract]
[Full Text]
-
Chan, Y. C., Raengpradub, S., Boor, K. J., Wiedmann, M.
(2007). Microarray-Based Characterization of the Listeria monocytogenes Cold Regulon in Log- and Stationary-Phase Cells. Appl. Environ. Microbiol.
73: 6484-6498
[Abstract]
[Full Text]
-
Stauff, D. L., Torres, V. J., Skaar, E. P.
(2007). Signaling and DNA-binding Activities of the Staphylococcus aureus HssR-HssS Two-component System Required for Heme Sensing. J. Biol. Chem.
282: 26111-26121
[Abstract]
[Full Text]
-
Lu, Z., Takeuchi, M., Sato, T.
(2007). The LysR-Type Transcriptional Regulator YofA Controls Cell Division through the Regulation of Expression of ftsW in Bacillus subtilis. J. Bacteriol.
189: 5642-5651
[Abstract]
[Full Text]
-
Deng, D.M., Liu, M.J., ten Cate, J.M., Crielaard, W.
(2007). The VicRK System of Streptococcus mutans Responds to Oxidative Stress. JDR
86: 606-610
[Abstract]
[Full Text]
-
Wall, T., Bath, K., Britton, R. A., Jonsson, H., Versalovic, J., Roos, S.
(2007). The Early Response to Acid Shock in Lactobacillus reuteri Involves the ClpL Chaperone and a Putative Cell Wall-Altering Esterase. Appl. Environ. Microbiol.
73: 3924-3935
[Abstract]
[Full Text]
-
Saskova, L., Novakova, L., Basler, M., Branny, P.
(2007). Eukaryotic-Type Serine/Threonine Protein Kinase StkP Is a Global Regulator of Gene Expression in Streptococcus pneumoniae. J. Bacteriol.
189: 4168-4179
[Abstract]
[Full Text]
-
Szurmant, H., Mohan, M. A., Imus, P. M., Hoch, J. A.
(2007). YycH and YycI Interact To Regulate the Essential YycFG Two-Component System in Bacillus subtilis. J. Bacteriol.
189: 3280-3289
[Abstract]
[Full Text]
-
Santelli, E., Liddington, R. C., Mohan, M. A., Hoch, J. A., Szurmant, H.
(2007). The Crystal Structure of Bacillus subtilis YycI Reveals a Common Fold for Two Members of an Unusual Class of Sensor Histidine Kinase Regulatory Proteins. J. Bacteriol.
189: 3290-3295
[Abstract]
[Full Text]
-
Fernandez, P., Saint-Joanis, B., Barilone, N., Jackson, M., Gicquel, B., Cole, S. T., Alzari, P. M.
(2006). The Ser/Thr Protein Kinase PknB Is Essential for Sustaining Mycobacterial Growth. J. Bacteriol.
188: 7778-7784
[Abstract]
[Full Text]
-
de Been, M., Francke, C., Moezelaar, R., Abee, T., Siezen, R. J.
(2006). Comparative analysis of two-component signal transduction systems of Bacillus cereus, Bacillus thuringiensis and Bacillus anthracis.. Microbiology
152: 3035-3048
[Abstract]
[Full Text]
-
Jordan, S., Junker, A., Helmann, J. D., Mascher, T.
(2006). Regulation of LiaRS-Dependent Gene Expression in Bacillus subtilis: Identification of Inhibitor Proteins, Regulator Binding Sites, and Target Genes of a Conserved Cell Envelope Stress-Sensing Two-Component System.. J. Bacteriol.
188: 5153-5166
[Abstract]
[Full Text]
-
Liu, M., Hanks, T. S., Zhang, J., McClure, M. J., Siemsen, D. W., Elser, J. L., Quinn, M. T., Lei, B.
(2006). Defects in ex vivo and in vivo growth and sensitivity to osmotic stress of group A Streptococcus caused by interruption of response regulator gene vicR.. Microbiology
152: 967-978
[Abstract]
[Full Text]
-
Paterson, G. K., Blue, C. E., Mitchell, T. J.
(2006). Role of two-component systems in the virulence of Streptococcus pneumoniae.. J Med Microbiol
55: 355-363
[Abstract]
[Full Text]
-
Biswas, S., Biswas, I.
(2006). Regulation of the Glucosyltransferase (gtfBC) Operon by CovR in Streptococcus mutans. J. Bacteriol.
188: 988-998
[Abstract]
[Full Text]
-
Gilmour, R., Foster, J. E., Sheng, Q., McClain, J. R., Riley, A., Sun, P.-M., Ng, W.-L., Yan, D., Nicas, T. I., Henry, K., Winkler, M. E.
(2005). New Class of Competitive Inhibitor of Bacterial Histidine Kinases. J. Bacteriol.
187: 8196-8200
[Abstract]
[Full Text]
-
Sun, J., Zheng, L., Landwehr, C., Yang, J., Ji, Y.
(2005). Identification of a Novel Essential Two-Component Signal Transduction System, YhcSR, in Staphylococcus aureus. J. Bacteriol.
187: 7876-7880
[Abstract]
[Full Text]
-
Ng, W.-L., Tsui, H.-C. T., Winkler, M. E.
(2005). Regulation of the pspA Virulence Factor and Essential pcsB Murein Biosynthetic Genes by the Phosphorylated VicR (YycF) Response Regulator in Streptococcus pneumoniae. J. Bacteriol.
187: 7444-7459
[Abstract]
[Full Text]
-
Stack, H. M., Sleator, R. D., Bowers, M., Hill, C., Gahan, C. G. M.
(2005). Role for HtrA in Stress Induction and Virulence Potential in Listeria monocytogenes. Appl. Environ. Microbiol.
71: 4241-4247
[Abstract]
[Full Text]
-
Szurmant, H., Nelson, K., Kim, E.-J., Perego, M., Hoch, J. A.
(2005). YycH Regulates the Activity of the Essential YycFG Two-Component System in Bacillus subtilis. J. Bacteriol.
187: 5419-5426
[Abstract]
[Full Text]
-
Senadheera, M. D., Guggenheim, B., Spatafora, G. A., Huang, Y.-C. C., Choi, J., Hung, D. C. I., Treglown, J. S., Goodman, S. D., Ellen, R. P., Cvitkovitch, D. G.
(2005). A VicRK Signal Transduction System in Streptococcus mutans Affects gtfBCD, gbpB, and ftf Expression, Biofilm Formation, and Genetic Competence Development. J. Bacteriol.
187: 4064-4076
[Abstract]
[Full Text]
-
Williams, T., Bauer, S., Beier, D., Kuhn, M.
(2005). Construction and Characterization of Listeria monocytogenes Mutants with In-Frame Deletions in the Response Regulator Genes Identified in the Genome Sequence. Infect. Immun.
73: 3152-3159
[Abstract]
[Full Text]
-
Schar, J., Sickmann, A., Beier, D.
(2005). Phosphorylation-Independent Activity of Atypical Response Regulators of Helicobacter pylori. J. Bacteriol.
187: 3100-3109
[Abstract]
[Full Text]
-
Mohedano, M. L., Overweg, K., de la Fuente, A., Reuter, M., Altabe, S., Mulholland, F., de Mendoza, D., Lopez, P., Wells, J. M.
(2005). Evidence that the Essential Response Regulator YycF in Streptococcus pneumoniae Modulates Expression of Fatty Acid Biosynthesis Genes and Alters Membrane Composition. J. Bacteriol.
187: 2357-2367
[Abstract]
[Full Text]
-
Hancock, L. E., Perego, M.
(2004). Systematic Inactivation and Phenotypic Characterization of Two-Component Signal Transduction Systems of Enterococcus faecalis V583. J. Bacteriol.
186: 7951-7958
[Abstract]
[Full Text]
-
Ng, W.-L., Winkler, M. E.
(2004). Singular structures and operon organizations of essential two-component systems in species of Streptococcus. Microbiology
150: 3096-3098
[Full Text]
-
Hutchings, M. I., Hoskisson, P. A., Chandra, G., Buttner, M. J.
(2004). Sensing and responding to diverse extracellular signals? Analysis of the sensor kinases and response regulators of Streptomyces coelicolor A3(2). Microbiology
150: 2795-2806
[Abstract]
[Full Text]
-
Bent, C. J., Isaacs, N. W., Mitchell, T. J., Riboldi-Tunnicliffe, A.
(2004). Crystal Structure of the Response Regulator 02 Receiver Domain, the Essential YycF Two-Component System of Streptococcus pneumoniae in both Complexed and Native States. J. Bacteriol.
186: 2872-2879
[Abstract]
[Full Text]
-
Foster, J. E., Sheng, Q., McClain, J. R., Bures, M., Nicas, T. I., Henry, K., Winkler, M. E., Gilmour, R.
(2004). Kinetic and mechanistic analyses of new classes of inhibitors of two-component signal transduction systems using a coupled assay containing HpkA-DrrA from Thermotoga maritima. Microbiology
150: 885-896
[Abstract]
[Full Text]
-
Dubrac, S., Msadek, T.
(2004). Identification of Genes Controlled by the Essential YycG/YycF Two-Component System of Staphylococcus aureus. J. Bacteriol.
186: 1175-1181
[Abstract]
[Full Text]
-
Kobayashi, K., Ehrlich, S. D., Albertini, A., Amati, G., Andersen, K. K., Arnaud, M., Asai, K., Ashikaga, S., Aymerich, S., Bessieres, P., Boland, F., Brignell, S. C., Bron, S., Bunai, K., Chapuis, J., Christiansen, L. C., Danchin, A., Debarbouille, M., Dervyn, E., Deuerling, E., Devine, K., Devine, S. K., Dreesen, O., Errington, J., Fillinger, S., Foster, S. J., Fujita, Y., Galizzi, A., Gardan, R., Eschevins, C., Fukushima, T., Haga, K., Harwood, C. R., Hecker, M., Hosoya, D., Hullo, M. F., Kakeshita, H., Karamata, D., Kasahara, Y., Kawamura, F., Koga, K., Koski, P., Kuwana, R., Imamura, D., Ishimaru, M., Ishikawa, S., Ishio, I., Le Coq, D., Masson, A., Mauel, C., Meima, R., Mellado, R. P., Moir, A., Moriya, S., Nagakawa, E., Nanamiya, H., Nakai, S., Nygaard, P., Ogura, M., Ohanan, T., O'Reilly, M., O'Rourke, M., Pragai, Z., Pooley, H. M., Rapoport, G., Rawlins, J. P., Rivas, L. A., Rivolta, C., Sadaie, A., Sadaie, Y., Sarvas, M., Sato, T., Saxild, H. H., Scanlan, E., Schumann, W., Seegers, J. F. M. L., Sekiguchi, J., Sekowska, A., Seror, S. J., Simon, M., Stragier, P., Studer, R., Takamatsu, H., Tanaka, T., Takeuchi, M., Thomaides, H. B., Vagner, V., van Dijl, J. M., Watabe, K., Wipat, A., Yamamoto, H., Yamamoto, M., Yamamoto, Y., Yamane, K., Yata, K., Yoshida, K., Yoshikawa, H., Zuber, U., Ogasawara, N.
(2003). Essential Bacillussubtilis genes. Proc. Natl. Acad. Sci. USA
100: 4678-4683
[Abstract]
[Full Text]
-
Birck, C., Chen, Y., Hulett, F. M., Samama, J.-P.
(2003). The Crystal Structure of the Phosphorylation Domain in PhoP Reveals a Functional Tandem Association Mediated by an Asymmetric Interface. J. Bacteriol.
185: 254-261
[Abstract]
[Full Text]
-
Wagner, C., Saizieu, A. d., Schonfeld, H.-J., Kamber, M., Lange, R., Thompson, C. J., Page, M. G.
(2002). Genetic Analysis and Functional Characterization of the Streptococcus pneumoniae vic Operon. Infect. Immun.
70: 6121-6128
[Abstract]
[Full Text]
-
Hancock, L., Perego, M.
(2002). Two-Component Signal Transduction in Enterococcus faecalis. J. Bacteriol.
184: 5819-5825
[Full Text]
-
Kobayashi, K., Ogura, M., Yamaguchi, H., Yoshida, K.-I., Ogasawara, N., Tanaka, T., Fujita, Y.
(2001). Comprehensive DNA Microarray Analysis of Bacillus subtilis Two-Component Regulatory Systems. J. Bacteriol.
183: 7365-7370
[Abstract]
[Full Text]
-
Wouters, J. A., Frenkiel, H., de Vos, W. M., Kuipers, O. P., Abee, T.
(2001). Cold Shock Proteins of Lactococcus lactis MG1363 Are Involved in Cryoprotection and in the Production of Cold-Induced Proteins. Appl. Environ. Microbiol.
67: 5171-5178
[Abstract]
[Full Text]
-
Ogura, M., Yamaguchi, H., Yoshida, K.-i., Fujita, Y., Tanaka, T.
(2001). DNA microarray analysis of Bacillus subtilis DegU, ComA and PhoP regulons: an approach to comprehensive analysis of B.subtilis two-component regulatory systems. Nucleic Acids Res
29: 3804-3813
[Abstract]
[Full Text]
-
Jones, C. H., Bolken, T. C., Jones, K. F., Zeller, G. O., Hruby, D. E.
(2001). Conserved DegP Protease in Gram-Positive Bacteria Is Essential for Thermal and Oxidative Tolerance and Full Virulence in Streptococcus pyogenes. Infect. Immun.
69: 5538-5545
[Abstract]
[Full Text]
-
Echenique, J. R., Trombe, M.-C.
(2001). Competence Repression under Oxygen Limitation through the Two-Component MicAB Signal-Transducing System in Streptococcus pneumoniae and Involvement of the PAS Domain of MicB. J. Bacteriol.
183: 4599-4608
[Abstract]
[Full Text]
-
Noone, D., Howell, A., Collery, R., Devine, K. M.
(2001). YkdA and YvtA, HtrA-Like Serine Proteases in Bacillus subtilis, Engage in Negative Autoregulation and Reciprocal Cross-Regulation of ykdA and yvtA Gene Expression. J. Bacteriol.
183: 654-663
[Abstract]
[Full Text]
-
Zahrt, T. C., Deretic, V.
(2000). An Essential Two-Component Signal Transduction System in Mycobacterium tuberculosis. J. Bacteriol.
182: 3832-3838
[Abstract]
[Full Text]
-
Fukuchi, K., Kasahara, Y., Asai, K., Kobayashi, K., Moriya, S., Ogasawara, N.
(2000). The essential two-component regulatory system encoded by yycF and yycG modulates expression of the ftsAZ operon in Bacillus subtilis. Microbiology
146: 1573-1583
[Abstract]
[Full Text]
-
Beier, D., Frank, R.
(2000). Molecular Characterization of Two-Component Systems of Helicobacter pylori. J. Bacteriol.
182: 2068-2076
[Abstract]
[Full Text]
-
Noone, D., Howell, A., Devine, K. M.
(2000). Expression of ykdA, Encoding a Bacillus subtilis Homologue of HtrA, Is Heat Shock Inducible and Negatively Autoregulated. J. Bacteriol.
182: 1592-1599
[Abstract]
[Full Text]
-
Deschenes, R. J., Lin, H., Ault, A. D., Fassler, J. S.
(1999). Antifungal Properties and Target Evaluation of Three Putative Bacterial Histidine Kinase Inhibitors. Antimicrob. Agents Chemother.
43: 1700-1703
[Abstract]
[Full Text]
-
Federle, M. J., McIver, K. S., Scott, J. R.
(1999). A Response Regulator That Represses Transcription of Several Virulence Operons in the Group A Streptococcus. J. Bacteriol.
181: 3649-3657
[Abstract]
[Full Text]
-
Martin, P. K., Li, T., Sun, D., Biek, D. P., Schmid, M. B.
(1999). Role in Cell Permeability of an Essential Two-Component System in Staphylococcus aureus. J. Bacteriol.
181: 3666-3673
[Abstract]
[Full Text]
-
Fabret, C., Feher, V. A., Hoch, J. A.
(1999). Two-Component Signal Transduction in Bacillus subtilis: How One Organism Sees Its World. J. Bacteriol.
181: 1975-1983
[Full Text]