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http://dx.doi.org/10.4014/jmb.1009.09034

BolA Affects Cell Growth, and Binds to the Promoters of Penicillin-Binding Proteins 5 and 6 and Regulates Their Expression  

Guinote, Ines Batista (Instituto de Tecnologia Quimica e Biologica/Universidade Nova de Lisboa)
Matos, Rute Goncalves (Instituto de Tecnologia Quimica e Biologica/Universidade Nova de Lisboa)
Freire, Patrick (Instituto de Tecnologia Quimica e Biologica/Universidade Nova de Lisboa)
Arraiano, Cecilia Maria (Instituto de Tecnologia Quimica e Biologica/Universidade Nova de Lisboa)
Publication Information
Journal of Microbiology and Biotechnology / v.21, no.3, 2011 , pp. 243-251 More about this Journal
Abstract
The gene bolA was discovered in the 80's, but unraveling its function in the cell has proven to be a complex task. The BolA protein has pleiotropic effects over cell physiology, altering growth and morphology, inducing biofilm formation, and regulating the balance of several membrane proteins. Recently, BolA was shown to be a transcription factor by repressing the expression of the mreB gene. The present report shows that BolA is a transcriptional regulator of the dacA and dacC genes, thus regulating both DD-carboxypeptidases PBP5 and PBP6 and thereby demonstrating the versatility of BolA as a cellular regulator. In this work, we also demonstrate that reduction of cell growth and survival can be connected to the overexpression of the bolA gene in different E. coli backgrounds, particularly in the exponential growth phase. The most interesting finding is that overproduction of BolA affects bacterial growth differently depending on whether the cells were inoculated directly from a plate culture or from an overnight batch culture. This strengthens the idea that BolA can be engaged in the coordination of genes that adapt the cell physiology in order to enhance cell adaptation and survival under stress conditions.
Keywords
BolA; DD-carboxypeptidase; transcriptional regulator; PBP;
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1 Freire, P., H. L. Vieira, A. R. Furtado, M. A. de Pedro, and C. M. Arraiano. 2006. Effect of the morphogene bolA on the permeability of the Escherichia coli outer membrane. FEMS Microbiol. Lett. 260: 106-111.   DOI   ScienceOn
2 Aldea, M., C. Hernandez-Chico, A. G. de la Campa, S. R. Kushner, and M. Vicente. 1988. Identification, cloning, and expression of bolA, an ftsZ-dependent morphogene of Escherichia coli. J. Bacteriol. 170: 5169-5176.   DOI
3 Bachmann, B. J. and K. B. Low. 1980. Linkage map of Escherichia coli K-12, edition 6. Microbiol. Rev. 44: 1-56.
4 Barbas, A., R. G. Matos, M. Amblar, E. Lopez-Vinas, P. Gomez-Puertas, and C. M. Arraiano. 2008. New insights into the mechanism of RNA degradation by ribonuclease II: Identification of the residue responsible for setting the RNase II end product. J. Biol. Chem. 283: 13070-13076.   DOI
5 Broome-Smith, J. K. 1985. Construction of a mutant of Eschrichia coli that has deletions of both the penicillin-binding protein 5 and 6 genes. J. Gen. Microbiol. 131: 2115-2118.
6 Broome-Smith, J. K. and B. G. Spratt. 1982. Deletion of the penicillin-binding protein 6 gene of Escherichia coli. J. Bacteriol. 152: 904-906.
7 Aldea, M., T. Garrido, C. Hernandez-Chico, M. Vicente, and S. R. Kushner. 1989. Induction of a growth-phase-dependent promoter triggers transcription of bolA, an Escherichia coli morphogene. EMBO J. 8: 3923-3931.
8 Aldea, M., T. Garrido, J. Pla, and M. Vicente. 1990. Division genes in Escherichia coli are expressed coordinately to cell septum requirements by gearbox promoters. EMBO J. 9: 3787-3794.
9 Nelson, D. E. and K. D. Young. 2001. Contributions of PBP 5 and DD-carboxypeptidase penicillin binding proteins to maintenance of cell shape in Escherichia coli. J. Bacteriol. 183: 3055-3064.   DOI   ScienceOn
10 Sambrook, J., T. Maniatis, and E. F. Fritsch. 1989. Molecular Cloning: A Laboratory Manual, 2nd Ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
11 Santos, J. M., P. Freire, M. Vicente, and C. M. Arraiano. 1999. The stationary-phase morphogene bolA from Escherichia coli is induced by stress during early stages of growth. Mol. Microbiol. 32: 789-798.   DOI   ScienceOn
12 Santos, J. M., M. Lobo, A. P. Matos, M. A. De Pedro, and C. M. Arraiano. 2002. The gene bolA regulates dacA (PBP5), dacC (PBP6) and ampC (AmpC), promoting normal morphology in Escherichia coli. Mol. Microbiol. 45: 1729-1740.   DOI   ScienceOn
13 Spratt, B. G. 1980. Deletion of the penicillin-binding protein 5 gene of Escherichia coli. J. Bacteriol. 144: 1190-1192.
14 Kim, M. J., H. S. Kim, J. K. Lee, C. B. Lee, and S. D. Park. 2002. Regulation of septation and cytokinesis during resumption of cell division requires uvi31+, a UV-inducible gene of fission yeast. Mol. Cells 14: 425-430.
15 van den Ent, F., L. A. Amos, and J. Lowe. 2001. Prokaryotic origin of the actin cytoskeleton. Nature 413: 39-44.   DOI   ScienceOn
16 Vieira, H. L., P. Freire, and C. M. Arraiano. 2004. Effect of Escherichia coli morphogene bolA on biofilms. Appl. Environ. Microbiol. 70: 5682-5684.   DOI   ScienceOn
17 Jones, L. J., R. Carballido-Lopez, and J. Errington. 2001. Control of cell shape in bacteria: Helical, actin-like filaments in Bacillus subtilis. Cell 104: 913-922.   DOI   ScienceOn
18 Lange, R. and R. Hengge-Aronis. 1991. Growth phase-regulated expression of bolA and morphology of stationary-phase Escherichia coli cells are controlled by the novel sigma factor sigma S. J. Bacteriol. 173: 4474-4481.   DOI
19 Markiewicz, Z., J. K. Broome-Smith, U. Schwarz, and B. G. Spratt. 1982. Spherical E. coli due to elevated levels of Dalanine carboxypeptidase. Nature 297: 702-704.   DOI   ScienceOn
20 Miller, J. H. 1972. Experiments in Molecular Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
21 Buchanan, C. E. and M. O. Sowell. 1982. Synthesis of penicillinbinding protein 6 by stationary-phase Escherichia coli. J. Bacteriol. 151: 491-494.
22 Freire, P., J. D. Amaral, J. M. Santos, and C. M. Arraiano. 2006. Adaptation to carbon starvation: RNase III ensures normal expression levels of bolA1p mRNA and sigma(S). Biochimie 88: 341-346.   DOI
23 Freire, P., R. N. Moreira, and C. M. Arraiano. 2009. BolA inhibits cell elongation and regulates MreB expression levels. J. Mol. Biol. 385: 1345-1351.   DOI   ScienceOn