Growth-dependent and adaptive mutation rates to ebgR and IS30 transposition in the bacteria Escherichia coli K-12 at different extracellular Mg2+ concentrations
DOI:
https://doi.org/10.14720/abs.53.1.15492Keywords:
Adaptive mutation, magnesium, Escherichia coli, PhoP-PhoQ, ebg operon, IS30, gene regulatory networkAbstract
During starvation on carbon and energy Escherichia coli K-12 cells, modified to possess EbgA51 as the only く-galactosidase enzyme, experience adaptive mutations in the ebgR repressor gene. In this way, cells acquire the capacity to utilize the lactulose as the only source of carbon and energy and begin to grow. Adaptive mutations at ebgR are mediated largely by insertion sequences, 40% of adaptive mutants contain IS30 insertions. Also, besides sensing extracellular Mg2+, a PhoP-PhoQ system decreases the adaptive mutation rate to ebgR in a to-date unknown way. By performing fluctuation tests and genetic analyses, we tested the hypothesis that Mg2+ plays an important role in the adaptive mutation at ebgR. Results gathered with phoP and phoQ mutant strains demonstrated that the adaptive, but not the growth-dependent, mutation rate is increased by a high extracellular Mg2+ concentration. In an Mg2+-rich environment, the phoQ cells experience a nearly identical adaptive mutation rate as the wild-type strain. Results with the wild-type strain show that the relation between the levels of PhoP-PhoQ expression and the adaptive mutation rate is not as straightforward as expected and that different Mg2+ concentrations do not affect IS30 transposition. We discuss the possible role of magnesium in the adaptive mutation process.
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Bjedov, I., Tenaillon, O., Gerard, B., Souza, V., Denamur, E., Radman, M., Taddei, F., Matic, I. 2003. Stress-induced mutagenesis in bacteria. Science, 300, 1404–1409. DOI: https://doi.org/10.1126/science.1082240
Buckstein, M.H., He, J., Rubin, H. 2008. Characterization of nucleotide pools as a Function of Physiological State in Escherichia coli. Journal of Bacteriology, 190, 718–726. DOI: https://doi.org/10.1128/JB.01020-07
Cairns, J., Overbaugh, J., Miller, S. 1988. The origin of mutants. Nature, 335, 142–145. DOI: https://doi.org/10.1038/335142a0
Castelli, M.E., Vescovi, E.G., Soncini, F.C. 2000. The phosphatase activity is the target for Mg2+ regulation of the sensor protein PhoQ in Salmonella. Journal of Biological Chemistry, 275, 22948–22954. DOI: https://doi.org/10.1074/jbc.M909335199
Cowan, J.A. 2002. Structural and catalytic chemistry of magnesium-dependent enzymes. Biometals, 15, 225–235. DOI: https://doi.org/10.1023/A:1016022730880
Eguchi, Y., Itou, J., Yamane, M., Demizu, R., Yamato, F., Okada, A., Mori, H., Kato, A., Utsumi, R. 2007. B1500, a small membrane protein, connects the two-component systems EvgS/EvgA and PhoQ/PhoP in Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America, 104, 18712–18717. DOI: https://doi.org/10.1073/pnas.0705768104
Foster, P.L. 1999. Mechanisms of stationary phase mutation: A decade of adaptive mutation. Annual Review of Genetics, 33, 57–88. DOI: https://doi.org/10.1146/annurev.genet.33.1.57
Foster, P.L. 2005. Stress responses and genetic variation in bacteria, Mutation Research, 569, 3–11. DOI: https://doi.org/10.1016/j.mrfmmm.2004.07.017
Garcia-Vescovi, E., Soncini, F.C., Groisman, E.A. 1996. Mg2+ as an extracellular signal: environmental regulation of Salmonella virulence. Cell, 84, 165–174. DOI: https://doi.org/10.1016/S0092-8674(00)81003-X
Gomez-Gomez, J.M., Blazquez, J., Baquero, F., Martinez, J.L. 1997. H-NS and RpoS regulate emer- gence of LacAra+ mutants of Escherichia coli MCS2. Journal of Bacteriology, 179, 4620–4622. Groisman, E.A. 2001. The pleiotropic two-component regulatory system PhoP-PhoQ. Journal of DOI: https://doi.org/10.1128/jb.179.14.4620-4622.1997
Bacteriology, 183, 1835–1842.
Grubbs, R.D. 2002. Intracellular magnesium and magnesium buffering. Biometals, 15, 251–259. DOI: https://doi.org/10.1023/A:1016026831789
Hagiwara, D., Yamashino, T., Mizuno, T. 2004. A genome wide view of the Escherichia coli BasS-BasR two component system implicated in iron responses. Bioscience Biotechnology and Biochemistry, 68, 1758–1767. DOI: https://doi.org/10.1271/bbb.68.1758
Hall, B.G. 1995. Adaptive mutations in Escherichia coli as a model for the multiple mutational origins of tumours. Proceedings of the National Academy of Sciences of the United States of America, 92, 5669–5673. DOI: https://doi.org/10.1073/pnas.92.12.5669
Hall, B.G. 1998. Adaptive Mutagenesis at ebgR is regulated by PhoPQ. Journal of Bacteriology, 180, 2862–2865. DOI: https://doi.org/10.1128/JB.180.11.2862-2865.1998
Hall, B.G. 1999a. Spectra of spontaneous growth-dependent and adaptive mutations at ebgR. Journal of Bacteriology, 181, 1149–1155. DOI: https://doi.org/10.1128/JB.181.4.1149-1155.1999
Hall, B.G. 1999b. Transposable elements as activators of cryptic genes in Escherichia coli. Genetica, 107, 181–187. DOI: https://doi.org/10.1007/978-94-011-4156-7_20
Hall, B.G., Betts, P.W., Wootton, J.C. 1989. DNA sequence analysis of artiicially evolved ebg enzyme and ebg repressor genes. Genetics, 123, 635–648. DOI: https://doi.org/10.1093/genetics/123.4.635
Hartl, D.L., Hall, B.G. 1974. A second naturally occurring beta-galactosidase in Escherichia coli. Nature, 248, 152–153. DOI: https://doi.org/10.1038/248152a0
Jerman, I., Ružič, R., Krašovec, R., Škarja, M., Mogilnicki, L. 2005. Electrical transfer of molecule information into water, its storage and bioeffects on plants and bacteria. Electromagnetic Biology and Medicine, 24, 341–353. DOI: https://doi.org/10.1080/15368370500381620
Lamrani, S., Ranquet, C., Gama, M-J., Nakai, H., Shapiro, J.A., Toussaint, A., Maenhaut-Michel, G. 1999. Starvation-induced Mucts62-mediated coding sequence fusion: a role for ClpXP, Lon, RpoS and Crp. Molecular Microbiology, 32, 327–343. DOI: https://doi.org/10.1046/j.1365-2958.1999.01352.x
Layton, J.C., Foster, P.L. 2003. Error-prone DNA polymerase IV is controlled by the stress-response sigma factor, RpoS, in Escherichia coli. Molecular Microbiology, 50, 549–561. DOI: https://doi.org/10.1046/j.1365-2958.2003.03704.x
Lejona, S., Castelli, M.E., Cabeza, M.L., Kenney, L.J., Vescovi, E.G., Soncini, F.C. 2004. PhoP can ac- tivate its target genes in a PhoQ-independent manner. Journal of Bacteriology, 186, 2476–2480. DOI: https://doi.org/10.1128/JB.186.8.2476-2480.2004
Lombardo, M.J., Aponyi, I., Rosenberg, S.M. 2004. General stress response regulator RpoS in adaptive mutation and ampliication in Escherichia coli. Genetics, 166, 669–680. DOI: https://doi.org/10.1093/genetics/166.2.669
Luria, S.E., Delbrück, M. 1943. Mutations of bacteria from virus sensitivity to virus resistance. Ge- netics, 28, 491–511. DOI: https://doi.org/10.1093/genetics/28.6.491
Ma, W.T., Sandri, Gv.H., Sarkar, S. 1992. Analysis of the Luria-Delbrück distribution using discrete convolution powers. Journal of Applied Probability, 29, 255–267. DOI: https://doi.org/10.2307/3214564
McKenzie, G.J., Harris, R.S., Lee, P.L., Rosenberg, S.M. 2000. The SOS response regulates adaptive mutation. Proceedings of the National Academy of Sciences of the United States of America, 97, 6646–6651. DOI: https://doi.org/10.1073/pnas.120161797
Minagawa, S., Ogasawara, H., Kato, A., Yamamoto, K., Eguchi, Y., Oshima, T., Mori, H., Ishihama, A., Utsumi, R. 2003. Identiication and molecular characterization of the Mg2+ stimulon of Escherichia coli. Journal of Bacteriology, 185, 3696–3702. DOI: https://doi.org/10.1128/JB.185.13.3696-3702.2003
Naas, T., Blot, M., Fitch, W.M., Arber, W. 1994. Insertion sequence-related genetic variation in resting Escherichia coli K-12. Genetics, 136, 721–730. DOI: https://doi.org/10.1093/genetics/136.3.721
Naas, T., Blot, M., Fitch, W.M., Arber, W. 1995. Dynamics of IS-related genetic rearrangements in resting Escherichia coli K-12. Molecular Biology and Evolution, 12, 198–207.
Olasz, F., Kiss, J., KQnig, P., Buzas, Zs., Stalder, R., Arber, W. 1998. Target speciicity of insertion element IS30. Molecular Microbiology, 28, 691–704. DOI: https://doi.org/10.1046/j.1365-2958.1998.00824.x
Regelmann, A.G., Lesley, J.A., Mott, C., Stokes, L., Waldburger, C.D. 2002. Mutational analysis of the Escherichia coli PhoQ sensor kinase: Differences with the Salmonella enterica serovar typhi- murium PhoQ protein and in the mechanism of Mg2+ and Ca2+ sensing. Journal of Bacteriology, 184, 5468–5478. DOI: https://doi.org/10.1128/JB.184.19.5468-5478.2002
Riesenfeld, C., Everett, M., Piddock, L.J.V., Hall, B.G. 1997. Adaptive mutations produce resistance to ciproloxacin. Antimicrobial Agents and Chemotherapy, 41, 2059–2060. DOI: https://doi.org/10.1128/AAC.41.9.2059
Saumaa, S., Tover, A., Kasak, L., Kivisaar, M. 2002. Different spectra of stationary-phase mutations in early-arising versus late-arising mutants of Pseudomonas putida: Involvement of the DNA repair enzyme MutY and the stationary-phase sigma factor RpoS. Journal of Bacteriology, 184, 6957–6965. DOI: https://doi.org/10.1128/JB.184.24.6957-6965.2002
Smith, R.L., Maguire, M.E. 1998. Microbial magnesium transport: unusual transporters searching for identity. Molecular Microbiology, 28, 217–226. DOI: https://doi.org/10.1046/j.1365-2958.1998.00810.x
Soncini, F.C., Vescovi, E.G., Solomon, F., Groisman, E.A. 1996. Molecular basis of the magnesium deprivation response in Salmonella typhimurium: identiication of PhoP regulated genes. Journal of Bacteriology, 178, 5092–5099. DOI: https://doi.org/10.1128/jb.178.17.5092-5099.1996
Sreedhara, A., Cowan, J.A. 2002. Structural and catalytic roles for divalent magnesium in nucleic acid biochemistry. Biometals, 15, 211–223. DOI: https://doi.org/10.1023/A:1016070614042
Szabó, M., Kiss, J., Nagy, Z., Chandler, M., Olasz, F. 2008. Sub-terminal sequences modulating IS30 transposition in vivo and in vitro. Journal of Molecular Biology, 375, 337–352. DOI: https://doi.org/10.1016/j.jmb.2007.10.043
Szabó, M., Muller, F., Kiss, J., Balduf, C., Strahle, U., Olasz, F. 2003. Transposition and targeting of the prokaryotic mobile element IS30 in zebraish. FEBS Letters, 550, 46–50. DOI: https://doi.org/10.1016/S0014-5793(03)00814-7
Utsumi, R. (Ed.) 2008. Bacterial Signal Transduction: Networks and Drug Targets. Advances in Ex- perimental Medicine and Biology, 631, 242 pp. DOI: https://doi.org/10.1007/978-0-387-78885-2
Weber, H., Polen, T., Heuveling, J., Wendisch, V.F., Hengge, R. 2005. Genome-wide analysis of the general stress response network in Escherichia coli: sigmaS-dependent genes, promoters, and sigma factor selectivity. Journal of Bacteriology, 187, 1591–1603. DOI: https://doi.org/10.1128/JB.187.5.1591-1603.2005
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