1887

Abstract

Loss of a type II restriction–modification (RM) gene complex, such as EcoRI, from a bacterial cell leads to death of its descendent cells through attack by residual restriction enzymes on undermethylated target sites of newly synthesized chromosomes. Through such post-segregational host killing, these gene complexes impose their maintenance on their host cells. This finding led to the rediscovery of type II RM systems as selfish mobile elements. The host prokaryote cells were found to cope with such attacks through a variety of means. The RecBCD pathway of homologous recombination in repairs the lethal lesions on the chromosome, whilst it destroys restricted non-self DNA. homologues, however, appear very limited in distribution among bacterial genomes, whereas homologues of the RecFOR proteins, responsible for another pathway, are widespread in eubacteria, just like the RM systems. In the present work, therefore, we examined the possible contribution of the RecFOR pathway to cell survival after loss of an RM gene complex. A mutation reduced survival in an otherwise -positive background and, more severely, in a background. We also found that its effect is prominent in the presence of specific non-null mutant forms of the RecBCD enzyme: the resistance to killing seen with , , and is severely reduced to the level of a null allele when combined with a , or mutant allele. Such resistance was also dependent on RecJ and RecQ functions. UV resistance of these non-null mutants is also reduced by , or mutation. These results demonstrate that the RecFOR pathway of recombination can contribute greatly to resistance to RM-mediated host killing, depending on the genetic background.

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2009-07-01
2020-10-27
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References

  1. Amundsen S. K., Smith G. R.. 2003; Interchangeable parts of the Escherichia coli recombination machinery. Cell112:741–744
    [Google Scholar]
  2. Amundsen S. K., Neiman A. M., Thibodeaux S. M., Smith G. R.. 1990; Genetic dissection of the biochemical activities of RecBCD enzyme. Genetics126:25–40
    [Google Scholar]
  3. Amundsen S. K., Taylor A. F., Smith G. R.. 2000; The RecD subunit of the Escherichia coli RecBCD enzyme inhibits RecA loading, homologous recombination, and DNA repair. Proc Natl Acad Sci U S A97:7399–7404
    [Google Scholar]
  4. Amundsen S. K., Fero J., Hansen L. M., Cromie G. A., Solnick J. V., Smith G. R., Salama N. R.. 2008; Helicobacter pylori AddAB helicase-nuclease and RecA promote recombination-related DNA repair and survival during stomach colonization. Mol Microbiol69:994–1007
    [Google Scholar]
  5. Anderson D. G., Kowalczykowski S. C.. 1997; The recombination hot spot χ is a regulatory element that switches the polarity of DNA degradation by the RecBCD enzyme. Genes Dev11:571–581
    [Google Scholar]
  6. Arnold D. A., Bianco P. R., Kowalczykowski S. C.. 1998; The reduced levels of χ recognition exhibited by the RecBC1004D enzyme reflect its recombination defect in vivo. J Biol Chem273:16476–16486
    [Google Scholar]
  7. Bachmann B. J.. 1987; Derivation and genotypes of some mutant derivatives of Escherichia coli K-12. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology pp1190–1219 Edited by Neidhardt F. C., Ingraham J. L., Low K. B., Magasanik B., Schaechter M., Umbarger H. E.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  8. Beernink H. T., Morrical S. W.. 1999; RMPs: recombination/replication mediator proteins. Trends Biochem Sci24:385–389
    [Google Scholar]
  9. Bianco P. R., Kowalczykowski S. C.. 1997; The recombination hotspot Chi is recognized by the translocating RecBCD enzyme as the single strand of DNA containing the sequence 5′-GCTGGTGG-3′. Proc Natl Acad Sci U S A94:6706–6711
    [Google Scholar]
  10. Bochner B. R., Huang H. C., Schieven G. L., Ames B. N.. 1980; Positive selection for loss of tetracycline resistance. J Bacteriol143:926–933
    [Google Scholar]
  11. Bork J. M., Cox M. M., Inman R. B.. 2001; The RecOR proteins modulate RecA protein function at 5′ ends of single-stranded DNA. EMBO J20:7313–7322
    [Google Scholar]
  12. Chedin F., Kowalczykowski S. C.. 2002; A novel family of regulated helicases/nucleases from Gram-positive bacteria: insights into the initiation of DNA recombination. Mol Microbiol43:823–834
    [Google Scholar]
  13. Chedin F., Handa N., Dillingham M. S., Kowalczykowski S. C.. 2006; The AddAB helicase/nuclease forms a stable complex with its cognate χ sequence during translocation. J Biol Chem281:18610–18617
    [Google Scholar]
  14. Churchill J. J., Kowalczykowski S. C.. 2000; Identification of the RecA protein-loading domain of RecBCD enzyme. J Mol Biol297:537–542
    [Google Scholar]
  15. Corrette-Bennett S. E., Lovett S. T.. 1995; Enhancement of RecA strand-transfer activity by the RecJ exonuclease of Escherichia coli. J Biol Chem270:6881–6885
    [Google Scholar]
  16. Courcelle J., Donaldson J. R., Chow K. H., Courcelle C. T.. 2003; DNA damage-induced replication fork regression and processing in Escherichia coli. Science299:1064–1067
    [Google Scholar]
  17. Criss A. K., Kline K. A., Seifert H. S.. 2005; The frequency and rate of pilin antigenic variation in Neisseria gonorrhoeae. Mol Microbiol58:510–519
    [Google Scholar]
  18. Fukuda E., Kaminska K. H., Bujnicki J. M., Kobayashi I.. 2008; Cell death upon epigenetic genome methylation: a novel function of methyl-specific deoxyribonucleases. Genome Biol9:R163
    [Google Scholar]
  19. Gravel S., Chapman J. R., Magill C., Jackson S. P.. 2008; DNA helicases Sgs1 and BLM promote DNA double-strand break resection. Genes Dev22:2767–2772
    [Google Scholar]
  20. Handa N., Kobayashi I.. 1999; Post-segregational killing by restriction modification gene complexes: observations of individual cell deaths. Biochimie81:931–938
    [Google Scholar]
  21. Handa N., Kobayashi I.. 2003; Accumulation of large non-circular forms of the chromosome in recombination-defective mutants of Escherichia coli. BMC Mol Biol4:5
    [Google Scholar]
  22. Handa N., Kobayashi I.. 2005; Type III restriction is alleviated by bacteriophage (RecE) homologous recombination function but enhanced by bacterial (RecBCD) function. J Bacteriol187:7362–7373
    [Google Scholar]
  23. Handa N., Kowalczykowski S. C.. 2007; A RecA mutant, RecA730, suppresses the recombination deficiency of the RecBC1004D– χ* interaction in vitro and in vivo. J Mol Biol365:1314–1325
    [Google Scholar]
  24. Handa N., Ohashi S., Kusano K., Kobayashi I.. 1997; χ*, a χ-related 11-mer sequence partially active in an E. coli recC* strain. Genes Cells2:525–536
    [Google Scholar]
  25. Handa N., Ichige A., Kusano K., Kobayashi I.. 2000; Cellular responses to postsegregational killing by restriction-modification genes. J Bacteriol182:2218–2229
    [Google Scholar]
  26. Handa N., Nakayama Y., Sadykov M., Kobayashi I.. 2001; Experimental genome evolution: large-scale genome rearrangements associated with resistance to replacement of a chromosomal restriction-modification gene complex. Mol Microbiol40:932–940
    [Google Scholar]
  27. Handa N., Bianco P. R., Baskin R. J., Kowalczykowski S. C.. 2005; Direct visualization of RecBCD movement reveals cotranslocation of the RecD motor after χ recognition. Mol Cell17:745–750
    [Google Scholar]
  28. Handa N., Morimatsu K., Lovett S. T., Kowalczykowski S. C.. 2009; Reconstitution of initial steps of dsDNA break repair by the RecF pathway of. E. coli. Genes Dev23:1234–1245
    [Google Scholar]
  29. Harmon F. G., Kowalczykowski S. C.. 1998; RecQ helicase, in concert with RecA and SSB proteins, initiates and disrupts DNA recombination. Genes Dev12:1134–1144
    [Google Scholar]
  30. Hashimoto-Gotoh T., Franklin F. C., Nordheim A., Timmis K. N.. 1981; Specific-purpose plasmid cloning vectors. I. Low copy number, temperature-sensitive, mobilization-defective pSC101-derived containment vectors. Gene16:227–235
    [Google Scholar]
  31. Hill S. A., Woodward T., Reger A., Baker R., Dinse T.. 2007; Role for the RecBCD recombination pathway for pilE gene variation in repair-proficient Neisseria gonorrhoeae. J Bacteriol189:7983–7990
    [Google Scholar]
  32. Holbeck S. L., Smith G. R.. 1992; Chi enhances heteroduplex DNA levels during recombination. Genetics132:879–891
    [Google Scholar]
  33. Horii Z., Clark A. J.. 1973; Genetic analysis of the recF pathway to genetic recombination in Escherichia coli K12: isolation and characterization of mutants. J Mol Biol80:327–344
    [Google Scholar]
  34. Ivancic-Bace I., Peharec P., Moslavac S., Skrobot N., Salaj-Smic E., Brcic-Kostic K.. 2003; RecFOR function is required for DNA repair and recombination in a RecA loading-deficient recB mutant of Escherichia coli. Genetics163:485–494
    [Google Scholar]
  35. Ivancic-Bace I., Salaj-Smic E., Brcic-Kostic K.. 2005; Effects of recJ, recQ, and recFOR mutations on recombination in nuclease-deficient recB recD double mutants of Escherichia coli. J Bacteriol187:1350–1356
    [Google Scholar]
  36. Jockovich M. E., Myers R. S.. 2001; Nuclease activity is essential for RecBCD recombination in Escherichia coli. Mol Microbiol41:949–962
    [Google Scholar]
  37. Karyagina A., Shilov I., Tashlitskii V., Khodoun M., Vasil'ev S., Lau P. C., Nikolskaya I.. 1997; Specific binding of SsoII DNA methyltransferase to its promoter region provides the regulation of SsoII restriction–modification gene expression. Nucleic Acids Res25:2114–2120
    [Google Scholar]
  38. Kobayashi I.. 2001; Behavior of restriction–modification systems as selfish mobile elements and their impact on genome evolution. Nucleic Acids Res29:3742–3756
    [Google Scholar]
  39. Kobayashi I.. 2002; Towards a new paradigm?. In Genome Science pp191–202 Edited by Yoshikawa H., Ogasawara N., Satoh N.. Amsterdam: Elsevier;
    [Google Scholar]
  40. Kobayashi I.. 2004a; Genetic addiction – a principle in symbiosis of genes in a genome. In Plasmid Biology pp105–144 Edited by Phillips G., Funnell B.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  41. Kobayashi I.. 2004b; Restriction–modification systems as minimal forms of life. In Restriction Endonucleases pp19–62 Edited by Pingoud A.. Berlin/Heidelberg: Springer;
    [Google Scholar]
  42. Kowalczykowski S. C., Dixon D. A., Eggleston A. K., Lauder S. D., Rehrauer W. M.. 1994; Biochemistry of homologous recombination in Escherichia coli. Microbiol Rev58:401–465
    [Google Scholar]
  43. Kusano K., Naito T., Handa N., Kobayashi I.. 1995; Restriction-modification systems as genomic parasites in competition for specific sequences. Proc Natl Acad Sci U S A92:11095–11099
    [Google Scholar]
  44. Kushner S. R., Nagaishi H., Templin A., Clark A. J.. 1971; Genetic recombination in Escherichia coli: the role of exonuclease I. Proc Natl Acad Sci U S A68:824–827
    [Google Scholar]
  45. Kuzminov A.. 1999; Recombinational repair of DNA damage in Escherichia coli and bacteriophage λ. Microbiol Mol Biol Rev63:751–813
    [Google Scholar]
  46. Lam S. T., Stahl M. M., McMilin K. D., Stahl F. W.. 1974; Rec-mediated recombinational hot spot activity in bacteriophage lambda. II. A mutation which causes hot spot activity. Genetics77:425–433
    [Google Scholar]
  47. Lloyd R. G., Buckman C.. 1985; Identification and genetic analysis of sbcC mutations in commonly used recBC sbcB strains of Escherichia coli K-12. J Bacteriol164:836–844
    [Google Scholar]
  48. Lloyd R. G., Low B.. 1996; In Escherichia coli and Salmonella: Cellular and Molecular Biology. , 2nd edn. pp2236–2255 Edited by Neidhardt F. C. Washington, DC: American Society for Microbiology;
  49. Lloyd R. G., Porton M. C., Buckman C.. 1988; Effect of recF, recJ, recN, recO and ruv mutations on ultraviolet survival and genetic recombination in a recD strain of Escherichia coli K12. Mol Gen Genet212:317–324
    [Google Scholar]
  50. Lovett S. T., Clark A. J.. 1984; Genetic analysis of the recJ gene of Escherichia coli K-12. J Bacteriol157:190–196
    [Google Scholar]
  51. Lovett S. T., Sutera V. A. Jr. 1995; Suppression of recJ exonuclease mutants of Escherichia coli by alterations in DNA helicasesII ( uvrD) and IV ( helD). Genetics 140:27–45
    [Google Scholar]
  52. Lovett S. T., Luisi-DeLuca C., Kolodner R. D.. 1988; The genetic dependence of recombination in recD mutants of Escherichia coli. Genetics120:37–45
    [Google Scholar]
  53. Mendonca V. M., Kaiser-Rogers K., Matson S. W.. 1993; Double helicase II ( uvrD)-helicase IV ( helD)deletion mutants are defective in the recombination pathways of Escherichia coli. J Bacteriol175:4641–4651
    [Google Scholar]
  54. Miller J.. 1992; A Short Course in Bacterial Genetics: a Laboratory Manual and Handbook for Escherichia coli and Related Bacteria Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  55. Mimitou E. P., Symington L. S.. 2008; Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature455:770–774
    [Google Scholar]
  56. Mochizuki A., Yahara K., Kobayashi I., Iwasa Y.. 2006; Genetic addiction: selfish gene's strategy for symbiosis in the genome. Genetics172:1309–1323
    [Google Scholar]
  57. Morimatsu K., Kowalczykowski S. C.. 2003; RecFOR proteins load RecA protein onto gapped DNA to accelerate DNA strand exchange: a universal step of recombinational repair. Mol Cell11:1337–1347
    [Google Scholar]
  58. Muir R. S., Flores H., Zinder N. D., Model P., Soberon X., Heitman J.. 1997; Temperature-sensitive mutants of the EcoRI endonuclease. J Mol Biol274:722–737
    [Google Scholar]
  59. Naito T., Kusano K., Kobayashi I.. 1995; Selfish behavior of restriction-modification systems. Science267:897–899
    [Google Scholar]
  60. Nakayama Y., Kobayashi I.. 1998; Restriction-modification gene complexes as selfish gene entities: roles of a regulatory system in their establishment, maintenance, and apoptotic mutual exclusion. Proc Natl Acad Sci U S A95:6442–6447
    [Google Scholar]
  61. Nakayama H., Nakayama K., Nakayama R., Irino N., Nakayama Y., Hanawalt P. C.. 1984; Isolation and genetic characterization of a thymineless death-resistant mutant of Escherichia coli K12: identification of a new mutation ( recQ1) that blocks the RecF recombination pathway. Mol Gen Genet195:474–480
    [Google Scholar]
  62. Nimonkar A. V., Ozsoy A. Z., Genschel J., Modrich P., Kowalczykowski S. C.. 2008; Human exonuclease 1 and BLM helicase interact to resect DNA and initiate DNA repair. Proc Natl Acad Sci U S A105:16906–16911
    [Google Scholar]
  63. 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 the methyltransferase activity. J Bacteriol190:2039–2049
    [Google Scholar]
  64. Orlowski J., Bujnicki J. M.. 2008; Structural and evolutionary classification of type II restriction enzymes based on theoretical and experimental analyses. Nucleic Acids Res36:3552–3569
    [Google Scholar]
  65. Roberts R. J., Vincze T., Posfai J., Macelis D.. 2007; rebase – enzymes and genes for DNA restriction and modification. Nucleic Acids Res35:D269–D270
    [Google Scholar]
  66. Rocha E. P., Cornet E., Michel B.. 2005; Comparative and evolutionary analysis of the bacterial homologous recombination systems. PLoS Genet1:e15
    [Google Scholar]
  67. Sadykov M., Asami Y., Niki H., Handa N., Itaya M., Tanokura M., Kobayashi I.. 2003; Multiplication of a restriction-modification gene complex. Mol Microbiol48:417–427
    [Google Scholar]
  68. Sambrook J., Fritsch E. F., Maniatis T.. 1989; Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  69. Schultz D. W., Taylor A. F., Smith G. R.. 1983; Escherichia coli RecBC pseudorevertants lacking chi recombinational hotspot activity. J Bacteriol155:664–680
    [Google Scholar]
  70. Seigneur M., Ehrlich S. D., Michel B.. 2000; RuvABC-dependent double-strand breaks in dnaBts mutants require RecA. Mol Microbiol38:565–574
    [Google Scholar]
  71. Simmon V. F., Lederberg S.. 1972; Degradation of bacteriophage lambda deoxyribonucleic acid after restriction by Escherichia coli K-12. J Bacteriol112:161–169
    [Google Scholar]
  72. Spies M., Kowalczykowski S. C.. 2006; The RecA binding locus of RecBCD is a general domain for recruitment of DNA strand exchange proteins. Mol Cell21:573–580
    [Google Scholar]
  73. Sung P., Klein H.. 2006; Mechanism of homologous recombination: mediators and helicases take on regulatory functions. Nat Rev Mol Cell Biol7:739–750
    [Google Scholar]
  74. Takahashi N., Kobayashi I.. 1990; Evidence for the double-strand break repair model of bacteriophage lambda recombination. Proc Natl Acad Sci U S A87:2790–2794
    [Google Scholar]
  75. Takahashi N. K., Yamamoto K., Kitamura Y., Luo S. Q., Yoshikura H., Kobayashi I.. 1992; Nonconservative recombination in Escherichia coli. Proc Natl Acad Sci U S A89:5912–5916
    [Google Scholar]
  76. Takahashi N., Kusano K., Yokochi T., Kitamura Y., Yoshikura H., Kobayashi I.. 1993; Genetic analysis of double-strand break repair in Escherichia coli. J Bacteriol175:5176–5185
    [Google Scholar]
  77. 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 Bacteriol184:6100–6108
    [Google Scholar]
  78. Tao T., Bourne J. C., Blumenthal R. M.. 1991; A family of regulatory genes associated with type II restriction-modification systems. J Bacteriol173:1367–1375
    [Google Scholar]
  79. Thoms B., Borchers I., Wackernagel W.. 2008; Effects of single-strand DNases ExoI, RecJ, ExoVII, and SbcCD on homologous recombination of recBCD + strains of Escherichia coli and roles of SbcB15 and XonA2 ExoI mutant enzymes. J Bacteriol190:179–192
    [Google Scholar]
  80. Tock M. R., Dryden D. T.. 2005; The biology of restriction and anti-restriction. Curr Opin Microbiol8:466–472
    [Google Scholar]
  81. Veaute X., Jeusset J., Soustelle C., Kowalczykowski S. C., Le Cam E., Fabre F.. 2003; The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature423:309–312
    [Google Scholar]
  82. Viswanathan M., Lovett S. T.. 1998; Single-strand DNA-specific exonucleases in Escherichia coli. Roles in repair and mutation avoidance. Genetics149:7–16
    [Google Scholar]
  83. Zhu Z., Chung W. H., Shim E. Y., Lee S. E., Ira G.. 2008; Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell134:981–994
    [Google Scholar]
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