1887

Abstract

In prokaryotes, homologous recombination is essential for the repair of genomic DNA damage and for the integration of DNA taken up during horizontal gene transfer. In , the exonucleases RecJ (specific for 5′ single-stranded DNA) and RecBCD (degrades duplex DNA) play important roles in recombination and recombinational double-strand break (DSB) repair by the RecF and RecBCD pathways, respectively. The cloned of partially complemented an mutant, suggesting functional similarity of the enzymes. A Δ mutant of was only slightly altered in transformability and was not affected in UV survival. In contrast, a Δ mutant was UV-sensitive, and had a low viability and altered transformation. Compared to wild-type, transformation with large chromosomal DNA fragments was decreased about 5-fold, while transformation with 1.5 kbp DNA fragments was increased 3.3- to 7-fold. A Δ mutation did not affect transformation, viability or UV resistance. However, double mutants and were non-viable, suggesting that the RecJ DNase or the RecBCD DNase (presumably absent in ) becomes essential for the recombinational repair of spontaneously inactivated replication forks if the other DNase is absent. A model of recombination during genetic transformation is discussed in which the two ends of the single-stranded donor DNA present in the cytoplasm frequently integrate separately and often with a time difference. If replication runs through that genomic region before both ends of the donor DNA are ligated to recipient DNA, a double-strand break (DSB) is formed. In these cases, transformation becomes dependent on DSB repair.

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2007-07-01
2024-12-08
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References

  1. Alonso J. C., Stiege A. C., Lüder G. 1993; Genetic recombination in Bacillus subtilis 168: effect of recN, recF, recH and addAB mutations on DNA repair and recombination. Mol Gen Genet 239:129–136
    [Google Scholar]
  2. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410 [CrossRef]
    [Google Scholar]
  3. Amundsen S. K., Taylor A. F., Chaudhury A. M., Smith G. R. 1986; recD : the gene for an essential third subunit of exonuclease V. Proc Natl Acad Sci U S A 83:5558–5562 [CrossRef]
    [Google Scholar]
  4. Anderson D. G., Kowalczykowski S. C. 1997; The translocating RecBCD enzyme stimulates recombination by directing RecA protein onto ssDNA in a chi-regulated manner. Cell 90:77–86 [CrossRef]
    [Google Scholar]
  5. Aravind L., Koonin E. V. 1998; A novel family of predicted phosphoesterases includes Drosophila prune protein and bacterial RecJ exonuclease. Trends Biochem Sci 23:17–19 [CrossRef]
    [Google Scholar]
  6. Arber W. 2000; Genetic variation: molecular mechanisms and impact on microbial evolution. FEMS Microbiol Rev 24:1–7 [CrossRef]
    [Google Scholar]
  7. Barbe V., Vallenet D., Fonknechten N., Kreimeyer A., Oztas S., Labarre L., Cruveiller S., Robert C., Duprat S. other authors 2004; Unique features revealed by the genome sequence of Acinetobacter sp. ADP1, a versatile and naturally transformation competent bacterium. Nucleic Acids Res 32:5766–5779 [CrossRef]
    [Google Scholar]
  8. Biek D. P., Cohen S. N. 1986; Identification and characterization of recD , a gene affecting plasmid maintenance and recombination in Escherichia coli. J Bacteriol 167:594–603
    [Google Scholar]
  9. Bruand C., Farache M., McGovern S., Ehrlich S. D., Polard P. 2001; DnaB, DnaD and DnaI proteins are components of the Bacillus subtilis replication restart primosome. Mol Microbiol 42:245–255
    [Google Scholar]
  10. Campbell E. A., Choi S. Y., Masure H. R. 1998; A competence regulon in Streptococcus pneumoniae revealed by genomic analysis. Mol Microbiol 27:929–939 [CrossRef]
    [Google Scholar]
  11. Chen I., Dubnau D. 2004; DNA uptake during bacterial transformation. Nat Rev Microbiol 2:241–249 [CrossRef]
    [Google Scholar]
  12. Churchill J. J., Anderson D. G., Kowalczykowski S. C. 1999; The RecBC enzyme loads RecA protein onto ssDNA asymmetrically and independently of chi, resulting in constitutive recombination activation. Genes Dev 13:901–911 [CrossRef]
    [Google Scholar]
  13. Clark A. J., Low K. B. 1988; Pathways and systems of homologous recombination in Escherichia coli . In The Recombination of Genetic Material pp 155–215 Edited by Low K. B. San Diego: Academic Press;
    [Google Scholar]
  14. Claverys J.-P., Lacks S. A. 1986; Heteroduplex deoxyribonucleic acid base mismatch repair in bacteria. Microbiol Rev 50:133–165
    [Google Scholar]
  15. Courcelle J., Hanawalt P. C. 1999; RecQ and RecJ process blocked replication forks prior to the resumption of replication in UV-irradiated Escherichia coli. Mol Gen Genet 262:543–551 [CrossRef]
    [Google Scholar]
  16. Courcelle J., Hanawalt P. C. 2003; RecA-dependent recovery of arrested DNA replication forks. Annu Rev Genet 37:611–646 [CrossRef]
    [Google Scholar]
  17. de Boer H. A., Constock L. J., Vasse M. 1983; The tac promoter: a functional hybrid derived from the trp and lac promoters. Proc Natl Acad Sci U S A 80:21–25 [CrossRef]
    [Google Scholar]
  18. de Vries J., Wackernagel W. 1998; Detection of nptII (kanamycin resistance) genes in genomes of transgenic plants by marker rescue transformation. Mol Gen Genet 257:606–613 [CrossRef]
    [Google Scholar]
  19. de Vries J., Wackernagel W. 2002; Integration of foreign DNA during natural transformation of Acinetobacter sp. by homology-facilitated illegitimate recombination. Proc Natl Acad Sci U S A 99:2094–2099 [CrossRef]
    [Google Scholar]
  20. de Vries J., Heine M., Harms K., Wackernagel W. 2003; Spread of recombinant DNA by roots and pollen of transgenic potato plants, identified by highly specific biomonitoring using natural transformation of Acinetobacter sp. Appl Environ Microbiol 69:4455–4462 [CrossRef]
    [Google Scholar]
  21. de Vries J., Herzfeld T., Wackernagel W. 2004; Transfer of plastid DNA from tobacco to the soil bacterium Acinetobacter sp. by natural transformation. Mol Microbiol 53:323–334 [CrossRef]
    [Google Scholar]
  22. Dedonder R. 1966; Levansucrase from Bacillus subtilis. Methods Enzymol 8:500–505
    [Google Scholar]
  23. Dermic D. 2006; Functions of multiple exonucleases are essential for cell viability, DNA repair and homologous recombination in recD mutants of Escherichia coli. Genetics 172:2057–2069
    [Google Scholar]
  24. Dubnau D. 1999; DNA uptake in bacteria. Annu Rev Microbiol 53:217–244 [CrossRef]
    [Google Scholar]
  25. Dubnau D., Davidoff-Abelson R., Scher B., Cirigliano C. 1973; Fate of transforming deoxyribonucleic acid after uptake by competent Bacillus subtilis : phenotypic characterization of radiation-sensitive recombination-deficient mutants. J Bacteriol 114:273–286
    [Google Scholar]
  26. Fernández S., Ayora S., Alonso J. C. 2000; Bacillus subtilis homologous recombination: genes and products. Res Microbiol 151:481–486 [CrossRef]
    [Google Scholar]
  27. Friedman-Ohana R., Cohen A. 1998; Heteroduplex joint formation in Escherichia coli recombination is initiated by pairing of a 3′-ending strand. Proc Natl Acad Sci U S A 95:6909–6914 [CrossRef]
    [Google Scholar]
  28. Garzón A., Beuzón C. R., Mahan M. J., Casadesús J. 1996; recB recJ mutants of Salmonella typhimurium are deficient in transductional recombination, DNA repair and plasmid maintenance. Mol Gen Genet 250:570–580
    [Google Scholar]
  29. Goodgal S. H. 1982; DNA uptake in Haemophilus transformation. Annu Rev Genet 16:169–192 [CrossRef]
    [Google Scholar]
  30. Graupner S., Wackernagel W. 2000; A broad-host-range expression vector series including a P ta c test plasmid and its application in the expression of the dod gene of Serratia marcescens (coding for ribulose-5-phosphate 3-epimerase) in Pseudomonas stutzeri. Biomol Eng 17:11–16 [CrossRef]
    [Google Scholar]
  31. Haijema B. J., Noback M., Hesseling A., Kooistra J., Venema G., Meima R. 1996; Replacement of the lysine residue in the consensus ATP-binding sequence of the AddA subunit of AddAB drastically affects chromosomal recombination in transformation and transduction of Bacillus subtilis. Mol Microbiol 21:989–999 [CrossRef]
    [Google Scholar]
  32. Halpern D., Gruss A., Claverys J.-P., Karoui M. E. 2004; rexAB mutants in Streptococcus pneumoniae. Microbiology 150:2409–2414 [CrossRef]
    [Google Scholar]
  33. Harms K., Kickstein E., Wackernagel W., Schön V. 2007; The RecJ DNase strongly suppresses genomic integration of short but not long foreign DNA fragments by homology-facilitated illegitimate recombination during transformation of Acinetobacter baylyi. Mol Microbiol 64:691–702 [CrossRef]
    [Google Scholar]
  34. Ivančić-Baće I., Salaj-Šmic E., Brčić-Kostić K. 2005; Effects of recJ, recQ , and recFOR mutations on recombination in nuclease-deficient recB recD double mutants of Escherichia coli. J Bacteriol 187:1350–1356 [CrossRef]
    [Google Scholar]
  35. Keen N. T., Tamaki S., Kobayashi D., Trollinger D. 1988; Improved broad-host-range plasmids for DNA cloning in gram-negative bacteria. Gene 70:191–197 [CrossRef]
    [Google Scholar]
  36. Kooistra J., Venema G. 1976; Effect of adenosine 5′-triphosphate-dependent deoxyribonuclease deficiency on properties and transformation of Haemophilus influenzae strains. J Bacteriol 128:549–556
    [Google Scholar]
  37. Kowalczykowski S. C. 2000; Initiation of genetic recombination and recombination-dependent replication. Trends Biochem Sci 25:156–165 [CrossRef]
    [Google Scholar]
  38. Kowalczykowski S. C., Dixon D. A., Eggleston A. K., Lauder S. D., Rehrauer W. M. 1994; Biochemistry of homologous recombination in Escherichia coli. Microbiol Rev 58:401–465
    [Google Scholar]
  39. Kuzminov A. 1999; Recombinational repair of DNA damage in Escherichia coli and bacteriophage λ. Microbiol Mol Biol Rev 63:751–813
    [Google Scholar]
  40. Kuzminov A. 2001; Single-strand interruptions in replicating chromosomes cause double-strand breaks. Proc Natl Acad Sci U S A 98:8241–8246 [CrossRef]
    [Google Scholar]
  41. Lloyd R. G., Low K. B. 1996; Homologous recombination. In Escherichia coli and Salmonella pp 2236–2255 Edited by Neidhardt F. C. Washington, DC: American Society for Microbiology Press;
    [Google Scholar]
  42. Lloyd R. G., Buckman C., Benson F. E. 1987; Genetic analysis of conjugational recombination in Escherichia coli K12 strains deficient in RecBCD enzyme. J Gen Microbiol 133:2531–2538
    [Google Scholar]
  43. 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 Genet 212:317–324 [CrossRef]
    [Google Scholar]
  44. Lorenz M. G., Wackernagel W. 1994; Bacterial gene transfer by natural genetic transformation in the environment. Microbiol Rev 58:563–602
    [Google Scholar]
  45. Lovett S. T., Clark A. J. 1984; Genetic analysis of the recJ gene of Escherichia coli K-12. J Bacteriol 157:190–196
    [Google Scholar]
  46. Lovett S. T., Kolodner R. D. 1989; Identification and purification of a single-stranded DNA-specific exonuclease encoded by the recJ gene of Escherichia coli. Proc Natl Acad Sci U S A 86:2627–2631 [CrossRef]
    [Google Scholar]
  47. Lovett S. T., Luisi-DeLuca C., Kolodner R. D. 1988; The genetic dependence of recombination in recD mutants of Escherichia coli. Genetics 120:37–45
    [Google Scholar]
  48. Majewski J., Cohan F. M. 1998; The effect of mismatch repair and heteroduplex formation on sexual isolation in Bacillus. Genetics 148:13–18
    [Google Scholar]
  49. Majewski J., Cohan F. M. 1999; DNA sequence similarity requirements for interspecific recombination in Bacillus. Genetics 153:1525–1533
    [Google Scholar]
  50. Maloy S. R., Nunn W. D. 1981; Selection for loss of tetracycline resistance by Escherichia coli. J Bacteriol 145:1110–1112
    [Google Scholar]
  51. McIlwraith M. J., West S. C. 2001; The efficiency of strand invasion by Escherichia coli RecA is dependent upon the length and polarity of ssDNA tails. J Mol Biol 305:23–31 [CrossRef]
    [Google Scholar]
  52. Mehr I. J., Seifert H. S. 1998; Differential roles of homologous recombination pathways in Neisseria gonorrhoeae pilin antigenic variation, DNA transformation and DNA repair. Mol Microbiol 30:697–710 [CrossRef]
    [Google Scholar]
  53. Meier P., Wackernagel W. 2005; Impact of mutS inactivation on foreign DNA acquisition by natural transformation in Pseudomonas stutzeri. J Bacteriol 187:143–154 [CrossRef]
    [Google Scholar]
  54. Mendonca V. M., Klepin H. D., Matson S. W. 1995; DNA helicases in recombination and repair: construction of a Δ uvrD Δ helD Δ recQ mutant deficient in recombination and repair. J Bacteriol 177:1326–1335
    [Google Scholar]
  55. Michel B., Niaudet B., Ehrlich S. D. 1982; Intramolecular recombination during plasmid transformation of Bacillus subtilis competent cells. EMBO J 1:1565–1571
    [Google Scholar]
  56. Michel B., Flores M.-J., Viguera E., Grompone G., Seigneur M., Bidnenko V. 2001; Rescue of arrested replication forks by homologous recombination. Proc Natl Acad Sci U S A 98:8181–8188 [CrossRef]
    [Google Scholar]
  57. Michel B., Grompone G., Flores M.-J., Bidnenko V. 2004; Multiple pathways process stalled replication forks. Proc Natl Acad Sci U S A 101:12783–12788 [CrossRef]
    [Google Scholar]
  58. Miesel L., Roth J. R. 1996; Evidence that SbcB and RecF pathway functions contribute to RecBCD-dependent transductional recombination. J Bacteriol 178:3146–3155
    [Google Scholar]
  59. Miranda A., Kuzminov A. 2003; Chromosomal lesion suppression and removal in Escherichia coli via linear DNA degradation. Genetics 163:1255–1271
    [Google Scholar]
  60. Morrison D. A., Mannarelli B. 1979; Transformation in pneumococcus: nuclease resistance of deoxyribonucleic acid in eclipse complex. J Bacteriol 140:655–665
    [Google Scholar]
  61. Palmen R., Hellingwerf K. J. 1997; Uptake and processing of DNA by Acinetobacter calcoaceticus – a review. Gene 192:179–190 [CrossRef]
    [Google Scholar]
  62. Palmen R., Vosman B., Buijsman P., Breek C. K., Hellingwerf K. J. 1993; Physiological characterization of natural transformation in Acinetobacter calcoaceticus. J Gen Microbiol 139:295–305 [CrossRef]
    [Google Scholar]
  63. Rajman L. A., Lovett S. T. 2000; A thermostable single-strand DNase from Methanococcus jannaschii related to the RecJ recombination and repair exonuclease from Escherichia coli. J Bacteriol 182:607–612 [CrossRef]
    [Google Scholar]
  64. Razavy H., Szigety S. K., Rosenberg S. M. 1996; Evidence for both 3′ and 5′ single-strand DNA ends in intermediates in Chi-stimulated recombination in vivo. Genetics 142:333–339
    [Google Scholar]
  65. Rinken R., Thoms B., Wackernagel W. 1992; Evidence that recBC -dependent degradation of duplex DNA in Escherichia coli recD mutants involves DNA unwinding. J Bacteriol 174:5424–5429
    [Google Scholar]
  66. 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]
  67. Scholz P., Haring V., Wittmann-Liebold B., Ashman K., Bagdasarian M., Scherzinger E. 1989; Complete nucleotide sequence and gene organization of the broad-host-range plasmid RSF1010. Gene 75:271–288 [CrossRef]
    [Google Scholar]
  68. Sutera V. A., Han E. S., Rajman L. A., Lovett S. T. 1999; Mutational analysis of the RecJ exonuclease of Escherichia coli : identification of phosphoesterase motifs. J Bacteriol 181:6098–6102
    [Google Scholar]
  69. te Riele H. P., Venema G. 1982; Molecular fate of heterologous bacterial DNA in competent Bacillus subtilis . I. Processing of B. pumilus and B.licheniformis DNA in B. subtilis. Genetics 101:179–188
    [Google Scholar]
  70. Thaler D. S., Sampson E., Siddiqi I., Rosenberg S. M., Thomason L. C., Stahl F. W., Stahl M. M. 1989; Recombination of bacteriophage lambda in recD mutants of Escherichia coli. Genome 31:53–67 [CrossRef]
    [Google Scholar]
  71. Thoms B., Wackernagel W. 1982; UV-induced alleviation of λ restriction in Escherichia coli K-12: kinetics of induction and specificity of this SOS function. Mol Gen Genet 186:111–117 [CrossRef]
    [Google Scholar]
  72. Vijayakumar M. N., Morrison D. A. 1986; Localization of competence-induced proteins of Streptococcus pneumoniae. J Bacteriol 165:689–695
    [Google Scholar]
  73. Viswanathan M., Lovett S. T. 1998; Single-strand DNA-specific exonucleases in Escherichia coli : roles in repair and mutation avoidance. Genetics 149:7–16
    [Google Scholar]
  74. Vovis G. F. 1973; Adenosine triphosphate-dependent deoxyribonuclease from Diplococcus pneumoniae : fate of transforming deoxyribonucleic acid in a strain deficient in the enzymatic activity. J Bacteriol 113:718–723
    [Google Scholar]
  75. Vovis G. F., Buttin G. 1970; An ATP-dependent deoxyribonuclease from Diplococcus pneumoniae . II. Evidence for its involvement in bacterial recombination. Biochim Biophys Acta 224:42–54 [CrossRef]
    [Google Scholar]
  76. Wilcox K. W., Smith H. O. 1975; Isolation and characterization of mutants of Haemophilus influenzae deficient in an adenosine 5′-triphosphate-dependent deoxyribonuclease activity. J Bacteriol 122:443–453
    [Google Scholar]
  77. Young D. M., Parke D., Ornston L. N. 2005; Opportunities for genetic investigation afforded by Acinetobacter baylyi , a nutritionally versatile bacterial species that is highly competent for natural transformation. Annu Rev Microbiol 59:519–551 [CrossRef]
    [Google Scholar]
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