This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Handa, N.
Right arrow Articles by Kobayashi, I.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Handa, N.
Right arrow Articles by Kobayashi, I.

 Previous Article  |  Next Article 

Journal of Bacteriology, April 2000, p. 2218-2229, Vol. 182, No. 8
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Cellular Responses to Postsegregational Killing by Restriction-Modification Genesdagger

Naofumi Handa, Asao Ichige, Kohji Kusano,Dagger and Ichizo Kobayashi*

Department of Molecular Biology, Institute of Medical Science, University of Tokyo, Shirokanedai, Tokyo 108-8639, Japan

Received 16 August 1999/Accepted 13 January 2000

Plasmids that carry one of several type II restriction modification gene complexes are known to show increased stability. The underlying mechanism was proposed to be the lethal attack by restriction enzyme at chromosomal recognition sites in cells that had lost the restriction modification gene complex. In order to examine bacterial responses to this postsegregational cell killing, we analyzed the cellular processes following loss of the EcoRI restriction modification gene complex carried by a temperature-sensitive plasmid in an Escherichia coli strain that is wild type with respect to DNA repair. A shift to the nonpermissive temperature blocked plasmid replication, reduced the increase in viable cell counts and resulted in loss of cell viability. Many cells formed long filaments, some of which were multinucleated and others anucleated. In a mutant defective in RecBCD exonuclease/recombinase, these cell death symptoms were more severe and cleaved chromosomes accumulated. Growth inhibition was also more severe in recA, ruvAB, ruvC, recG, and recN mutants. The cells induced the SOS response in a RecBC-dependent manner. These observations strongly suggest that bacterial cells die as a result of chromosome cleavage after loss of a restriction modification gene complex and that the bacterial RecBCD/RecA machinery helps the cells to survive, at least to some extent, by repairing the cleaved chromosomes. These and previous results have led us to hypothesize that the RecBCD/Chi/RecA system serves to destroy restricted "nonself" DNA and repair restricted "self" DNA.


* Corresponding author. Mailing address: Department of Molecular Biology, Institute of Medical Science, University of Tokyo, Shirokanedai, Tokyo 108-8639, Japan. Phone: (81) 3-5449-5326. Fax: (81) 3-5449-5422 and -5645. E-mail: ikobaya{at}ims.u-tokyo.ac.jp.

dagger Dedicated to Tokio Kogoma.

Dagger Present address: Laboratory of Genetics, University of Wisconsin, Madison, WI 53706.


Journal of Bacteriology, April 2000, p. 2218-2229, Vol. 182, No. 8
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.



This article has been cited by other articles:

  • Handa, N., Ichige, A., Kobayashi, I. (2009). Contribution of RecFOR machinery of homologous recombination to cell survival after loss of a restriction-modification gene complex. Microbiology 155: 2320-2332 [Abstract] [Full Text]  
  • Asakura, Y., Kobayashi, I. (2009). From damaged genome to cell surface: transcriptome changes during bacterial cell death triggered by loss of a restriction-modification gene complex. Nucleic Acids Res 37: 3021-3031 [Abstract] [Full Text]  
  • Dillingham, M. S., Kowalczykowski, S. C. (2008). RecBCD Enzyme and the Repair of Double-Stranded DNA Breaks. Microbiol. Mol. Biol. Rev. 72: 642-671 [Abstract] [Full Text]  
  • Mruk, I., Blumenthal, R. M. (2008). Real-time kinetics of restriction-modification gene expression after entry into a new host cell. Nucleic Acids Res 36: 2581-2593 [Abstract] [Full Text]  
  • Ohno, S., Handa, N., Watanabe-Matsui, M., Takahashi, N., Kobayashi, I. (2008). Maintenance Forced by a Restriction-Modification System Can Be Modulated by a Region in Its Modification Enzyme Not Essential for Methyltransferase Activity. J. Bacteriol. 190: 2039-2049 [Abstract] [Full Text]  
  • Pouillot, F., Fayolle, C., Carniel, E. (2007). A putative DNA adenine methyltransferase is involved in Yersinia pseudotuberculosis pathogenicity. Microbiology 153: 2426-2434 [Abstract] [Full Text]  
  • Yahara, K., Horie, R., Kobayashi, I., Sasaki, A. (2007). Evolution of DNA Double-Strand Break Repair by Gene Conversion: Coevolution Between a Phage and a Restriction-Modification System. Genetics 176: 513-526 [Abstract] [Full Text]  
  • Ivancic-Bace, I., Vlasic, I., Cogelja-Cajo, G., Brcic-Kostic, K., Salaj-Smic, E. (2006). Roles of PriA Protein and Double-Strand DNA Break Repair Functions in UV-Induced Restriction Alleviation in Escherichia coli. Genetics 174: 2137-2149 [Abstract] [Full Text]  
  • Watanabe, M., Yuzawa, H., Handa, N., Kobayashi, I. (2006). Hyperthermophilic DNA Methyltransferase M.PabI from the Archaeon Pyrococcus abyssi. Appl. Environ. Microbiol. 72: 5367-5375 [Abstract] [Full Text]  
  • Handa, N., Kobayashi, I. (2005). Type III Restriction Is Alleviated by Bacteriophage (RecE) Homologous Recombination Function but Enhanced by Bacterial (RecBCD) Function. J. Bacteriol. 187: 7362-7373 [Abstract] [Full Text]  
  • Ichige, A., Kobayashi, I. (2005). Stability of EcoRI Restriction-Modification Enzymes In Vivo Differentiates the EcoRI Restriction-Modification System from Other Postsegregational Cell Killing Systems. J. Bacteriol. 187: 6612-6621 [Abstract] [Full Text]  
  • Ito, T., Ma, X. X., Takeuchi, F., Okuma, K., Yuzawa, H., Hiramatsu, K. (2004). Novel Type V Staphylococcal Cassette Chromosome mec Driven by a Novel Cassette Chromosome Recombinase, ccrC. Antimicrob. Agents Chemother. 48: 2637-2651 [Abstract] [Full Text]  
  • Mruk, I., Cichowicz, M., Kaczorowski, T. (2003). Characterization of the LlaCI methyltransferase from Lactococcus lactis subsp. cremoris W15 provides new insights into the biology of type II restriction-modification systems. Microbiology 149: 3331-3341 [Abstract] [Full Text]  
  • Rowe-Magnus, D. A., Guerout, A.-M., Biskri, L., Bouige, P., Mazel, D. (2003). Comparative Analysis of Superintegrons: Engineering Extensive Genetic Diversity in the Vibrionaceae. Genome Res 13: 428-442 [Abstract] [Full Text]  
  • Takahashi, N., Naito, Y., Handa, N., Kobayashi, I. (2002). A DNA Methyltransferase Can Protect the Genome from Postdisturbance Attack by a Restriction-Modification Gene Complex. J. Bacteriol. 184: 6100-6108 [Abstract] [Full Text]  
  • Naderer, M., Brust, J. R., Knowle, D., Blumenthal, R. M. (2002). Mobility of a Restriction-Modification System Revealed by Its Genetic Contexts in Three Hosts. J. Bacteriol. 184: 2411-2419 [Abstract] [Full Text]  
  • Murray, N. E. (2002). Immigration control of DNA in bacteria: self versus non-self. Microbiology 148: 3-20 [Full Text]  
  • Sakamoto, J. J., Sasaki, M., Tsuchido, T. (2001). Purification and Characterization of a Bacillus subtilis 168 Nuclease, YokF, Involved in Chromosomal DNA Degradation and Cell Death Caused by Thermal Shock Treatments. J. Biol. Chem. 276: 47046-47051 [Abstract] [Full Text]  
  • Zhong, Z., Toukdarian, A., Helinski, D., Knauf, V., Sykes, S., Wilkinson, J. E., O'Bryne, C., Shea, T., DeLoughery, C., Caspi, R. (2001). Sequence Analysis of a 101-Kilobase Plasmid Required for Agar Degradation by a Microscilla Isolate. Appl. Environ. Microbiol. 67: 5771-5779 [Abstract] [Full Text]  
  • Dryden, D. T. F., Murray, N. E., Rao, D. N. (2001). Nucleoside triphosphate-dependent restriction enzymes. Nucleic Acids Res 29: 3728-3741 [Abstract] [Full Text]  
  • Kobayashi, I. (2001). Behavior of restriction-modification systems as selfish mobile elements and their impact on genome evolution. Nucleic Acids Res 29: 3742-3756 [Abstract] [Full Text]  
  • Chinen, A., Naito, Y., Handa, N., Kobayashi, I. (2000). Evolution of Sequence Recognition by Restriction-Modification Enzymes: Selective Pressure for Specificity Decrease. Mol Biol Evol 17: 1610-1619 [Abstract] [Full Text]  
  • Rocha, E. P.C., Danchin, A., Viari, A. (2001). Evolutionary Role of Restriction/Modification Systems as Revealed by Comparative Genome Analysis. Genome Res 11: 946-958 [Abstract] [Full Text]