DOI QR코드

DOI QR Code

Characterization of the BolA Homolog IbaG: A New Gene Involved in Acid Resistance

  • Received : 2011.07.18
  • Accepted : 2011.11.30
  • Published : 2012.04.28

Abstract

BolA protein homologs are widely distributed in nature. In this report, we have studied for the first time YrbA, the only BolA homolog present in Escherichia coli, which we have renamed ibaG. We have constructed single and multiple ibaG mutants, and overexpressed ibaG in wild-type strains, in order to characterize this gene. The ibaG phenotypes are different from the bolA-associated round morphologies or growth profiles. Interestingly, ibaG and bolA single-and double-deletion mutants grow faster and have higher viabilities in rich media, whereas the overexpressed strains are significantly growth impaired. However, the mutant strains have lower viabilities than the wild type in the late stationary phase, indicating that both bolA and ibaG are important for survival in difficult growth conditions. bolA, as a transcription factor, binds to some promoters, but ibaG does not interact with the same DNA regions. We have determined that ibaG is transcribed in an operon with the murA gene, involved in the synthesis of peptidoglycan precursors. ibaG was also seen to change its mRNA expression pattern in response to acidic stress. ibaG may thus represent a new gene involved in cell resistance against acid stress.

Keywords

References

  1. 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.
  2. 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.
  3. 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. https://doi.org/10.1128/jb.170.11.5169-5176.1988
  4. Baba, T., T. Ara, M. Hasegawa, Y. Takai, Y. Okumura, M. Baba, et al. 2006. Construction of Escherichia coli K-12 inframe, single-gene knockout mutants: The Keio collection. Mol. Syst. Biol. 2: 2006. 0008.
  5. Bachmann, B. J. and K. B. Low. 1980. Linkage map of Escherichia coli K-12, edition 6. Microbiol. Rev. 44: 1-56.
  6. Bearson, S., B. Bearson, and J. W. Foster. 1997. Acid stress responses in enterobacteria. FEMS Microbiol. Lett. 147: 173-180. https://doi.org/10.1111/j.1574-6968.1997.tb10238.x
  7. Brown, E. D., E. I. Vivas, C. T. Walsh, and R. Kolter. 1995. MurA (MurZ), the enzyme that catalyzes the first committed step in peptidoglycan biosynthesis, is essential in Escherichia coli. J. Bacteriol. 177: 4194-4197. https://doi.org/10.1128/jb.177.14.4194-4197.1995
  8. Cherepanov, P. P. and W. Wackernagel. 1995. Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158: 9-14. https://doi.org/10.1016/0378-1119(95)00193-A
  9. Datsenko, K. A. and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97: 6640-6645. https://doi.org/10.1073/pnas.120163297
  10. Fitzwater, T., X. Y. Zhang, R. Elble, and B. Polisky. 1988. Conditional high copy number ColE1 mutants: Resistance to RNA1 inhibition in vivo and in vitro. Embo J. 7: 3289-3297.
  11. 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. https://doi.org/10.1016/j.biochi.2005.09.004
  12. 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. https://doi.org/10.1016/j.jmb.2008.12.026
  13. 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. https://doi.org/10.1111/j.1574-6968.2006.00307.x
  14. Gama-Castro, S., H. Salgado, M. Peralta-Gil, A. Santos-Zavaleta, L. Muniz-Rascado, H. Solano-Lira, et al. 2011. RegulonDB version 7.0: Transcriptional regulation of Escherichia coli K-12 integrated within genetic sensory response units (Gensor Units). Nucleic Acids Res. 39: D98-D105. https://doi.org/10.1093/nar/gkq1110
  15. Guinote, I. B., R. G. Matos, P. Freire, and C. M. Arraiano. 2011. BolA affects growth and binds to the promoters of penicillin-binding proteins 5 and 6 regulating their expression. J. Microbiol. Biotechnol. 21: 243-251.
  16. Herring, C. D. and F. R. Blattner. 2004. Conditional lethal amber mutations in essential Escherichia coli genes. J. Bacteriol. 186: 2673-2681. https://doi.org/10.1128/JB.186.9.2673-2681.2004
  17. Kasai, T., M. Inoue, S. Koshiba, T. Yabuki, M. Aoki, E. Nunokawa, et al. 2004. Solution structure of a BolA-like protein from Mus musculus. Protein Sci. 13: 545-548. https://doi.org/10.1110/ps.03401004
  18. 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.
  19. 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. https://doi.org/10.1128/jb.173.14.4474-4481.1991
  20. Lin, J., I. S. Lee, J. Frey, J. L. Slonczewski, and J. W. Foster. 1995. Comparative analysis of extreme acid survival in Salmonella Typhimurium, Shigella flexneri, and Escherichia coli. J Bacteriol. 177: 4097-4104. https://doi.org/10.1128/jb.177.14.4097-4104.1995
  21. Malinverni, J. C. and T. J. Silhavy. 2009. An ABC transport system that maintains lipid asymmetry in the Gram-negative outer membrane. Proc. Natl. Acad. Sci. USA 106: 8009-8014. https://doi.org/10.1073/pnas.0903229106
  22. Marquardt, J. L., D. A. Siegele, R. Kolter, and C. T. Walsh. 1992. Cloning and sequencing of Escherichia coli murZ and purification of its product, a UDP-N-acetylglucosamine enolpyruvyl transferase. J. Bacteriol. 174: 5748-5752. https://doi.org/10.1128/jb.174.17.5748-5752.1992
  23. Martinez-Antonio, A., S. C. Janga, and D. Thieffry. 2008. Functional organisation of Escherichia coli transcriptional regulatory network. J. Mol. Biol. 381: 238-247. https://doi.org/10.1016/j.jmb.2008.05.054
  24. Miksch, G. and P. Dobrowolski. 1995. Growth phase-dependent induction of stationary-phase promoters of Escherichia coli in different Gram-negative bacteria. J. Bacteriol. 177: 5374-5378. https://doi.org/10.1128/jb.177.18.5374-5378.1995
  25. Miksch, G. and P. Dobrowolski. 1995. Growth phase-dependent induction of stationary-phase promoters of Escherichia coli in different gram-negative bacteria. J. Bacteriol. 177: 5374-5378. https://doi.org/10.1128/jb.177.18.5374-5378.1995
  26. Miller, J. H. 1972. Experiments in Molecular Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
  27. Muffler, A., D. D. Traulsen, R. Lange, and R. Hengge-Aronis. 1996. Posttranscriptional osmotic regulation of the sigma(s) subunit of RNA polymerase in Escherichia coli. J. Bacteriol. 178: 1607-1613. https://doi.org/10.1128/jb.178.6.1607-1613.1996
  28. Reese, M. 2000. Computational prediction of gene structure and regulation in the genome of Drosophila melanogaster.
  29. 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.
  30. Santos, J. M., D. Drider, P. E. Marujo, P. Lopez, and C. M. Arraiano. 1997. Determinant role of E. coli RNase III in the decay of both specific and heterologous mRNAs. FEMS Microbiol. Lett. 157: 31-38. https://doi.org/10.1111/j.1574-6968.1997.tb12749.x
  31. Santos, J. M., P. Freire, F. S. Mesquita, F. Mika, R. Hengge, and C. M. Arraiano. 2006. Poly(A)-polymerase I links transcription with mRNA degradation via sigmaS proteolysis. Mol. Microbiol. 60: 177-188. https://doi.org/10.1111/j.1365-2958.2006.05078.x
  32. 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. https://doi.org/10.1046/j.1365-2958.1999.01397.x
  33. 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. https://doi.org/10.1046/j.1365-2958.2002.03131.x
  34. Vieira, H. L., P. Freire, and C. M. Arraiano. 2004. Effect of Escherichia coli morphogene bolA on biofilms. Appl. Environ. Microbiol. 70: 5682-5684. https://doi.org/10.1128/AEM.70.9.5682-5684.2004

Cited by

  1. Genomic analysis of the regulatory elements and links with intrinsic DNA structural properties in the shrunken genome of Buchnera vol.14, pp.None, 2012, https://doi.org/10.1186/1471-2164-14-73
  2. Morphogenes bolA and mreB mediate the photoregulation of cellular morphology during complementary chromatic acclimation in Fremyella diplosiphon vol.93, pp.1, 2012, https://doi.org/10.1111/mmi.12649
  3. Breaking through the stress barrier: the role of BolA in Gram-negative survival vol.30, pp.10, 2012, https://doi.org/10.1007/s11274-014-1702-4
  4. The Escherichia coli BolA Protein IbaG Forms a Histidine-Ligated [2Fe-2S]-Bridged Complex with Grx4 vol.55, pp.49, 2012, https://doi.org/10.1021/acs.biochem.6b00812
  5. A Vibrio cholerae BolA-Like Protein Is Required for Proper Cell Shape and Cell Envelope Integrity vol.10, pp.4, 2012, https://doi.org/10.1128/mbio.00790-19
  6. NMR-Metabolomics Shows That BolA Is an Important Modulator of Salmonella Typhimurium Metabolic Processes under Virulence Conditions vol.9, pp.11, 2012, https://doi.org/10.3390/metabo9110243