Abstract
The propensity of the terminus of the Escherichia coli chromosome for recombination has been further explored, using a test based on the selectable loss of a λ prophage inserted between repeated sequences from Tn10. Terminal recombination appears region-specific and unrelated to replication termination in a strain harboring a major chromosomal rearrangement. It requires RecBC(D) activity and must therefore occur between sister chromosomes, to conserve genomic integrity in spite of DNA degradation by RecBCD. Terminal recombination is maximal in the dif region and its intensity on either side of this recombination site depends on the orientation of the repeated sequences, probably because of the single χ site present in each repeat. Additional observations support the model that the crossover is initiated by single-strand invasion between sister chromosomes followed by RecBCD action as a consequence of DNA breakage due to the initial invasion event. Crossover location within repeats inserted at dif position supports the possibility that sister chromosomes are tightly paired in the centre of the terminal recombination zone. These data reinforce the model that postreplicative reconstruction of nucleoid organization creates a localized synapsis between the termini of sister chromosomes.
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- Adams D. E., Shekhtman E. M., Zechiedrich E. L., Schmid M. B., Cozzarelli N. R. The role of topoisomerase IV in partitioning bacterial replicons and the structure of catenated intermediates in DNA replication. Cell. 1992 Oct 16;71(2):277–288. doi: 10.1016/0092-8674(92)90356-h. [DOI] [PubMed] [Google Scholar]
- Bennett R. J., West S. C. RuvC protein resolves Holliday junctions via cleavage of the continuous (noncrossover) strands. Proc Natl Acad Sci U S A. 1995 Jun 6;92(12):5635–5639. doi: 10.1073/pnas.92.12.5635. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bird R. E., Louarn J., Martuscelli J., Caro L. Origin and sequence of chromosome replication in Escherichia coli. J Mol Biol. 1972 Oct 14;70(3):549–566. doi: 10.1016/0022-2836(72)90559-1. [DOI] [PubMed] [Google Scholar]
- Blakely G., Colloms S., May G., Burke M., Sherratt D. Escherichia coli XerC recombinase is required for chromosomal segregation at cell division. New Biol. 1991 Aug;3(8):789–798. [PubMed] [Google Scholar]
- Bouché J. P. Physical map of a 470 x 10(3) base-pair region flanking the terminus of DNA replication in the Escherichia coli K12 genome. J Mol Biol. 1982 Jan 5;154(1):1–20. doi: 10.1016/0022-2836(82)90413-2. [DOI] [PubMed] [Google Scholar]
- Béjar S., Bouché J. P. Molecular cloning of the region of the terminus of Escherichia coli K-12 DNA replication. J Bacteriol. 1983 Feb;153(2):604–609. doi: 10.1128/jb.153.2.604-609.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Capaldo-Kimball F., Barbour S. D. Involvement of recombination genes in growth and viability of Escherichia coli K-12. J Bacteriol. 1971 Apr;106(1):204–212. doi: 10.1128/jb.106.1.204-212.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cheng K. C., Smith G. R. Cutting of chi-like sequences by the RecBCD enzyme of Escherichia coli. J Mol Biol. 1987 Apr 20;194(4):747–750. doi: 10.1016/0022-2836(87)90252-x. [DOI] [PubMed] [Google Scholar]
- Cornet F., Louarn J., Patte J., Louarn J. M. Restriction of the activity of the recombination site dif to a small zone of the Escherichia coli chromosome. Genes Dev. 1996 May 1;10(9):1152–1161. doi: 10.1101/gad.10.9.1152. [DOI] [PubMed] [Google Scholar]
- Cornet F., Mortier I., Patte J., Louarn J. M. Plasmid pSC101 harbors a recombination site, psi, which is able to resolve plasmid multimers and to substitute for the analogous chromosomal Escherichia coli site dif. J Bacteriol. 1994 Jun;176(11):3188–3195. doi: 10.1128/jb.176.11.3188-3195.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DiGate R. J., Marians K. J. Molecular cloning and DNA sequence analysis of Escherichia coli topB, the gene encoding topoisomerase III. J Biol Chem. 1989 Oct 25;264(30):17924–17930. [PubMed] [Google Scholar]
- Fellay R., Frey J., Krisch H. Interposon mutagenesis of soil and water bacteria: a family of DNA fragments designed for in vitro insertional mutagenesis of gram-negative bacteria. Gene. 1987;52(2-3):147–154. doi: 10.1016/0378-1119(87)90041-2. [DOI] [PubMed] [Google Scholar]
- Horiuchi T., Fujimura Y., Nishitani H., Kobayashi T., Hidaka M. The DNA replication fork blocked at the Ter site may be an entrance for the RecBCD enzyme into duplex DNA. J Bacteriol. 1994 Aug;176(15):4656–4663. doi: 10.1128/jb.176.15.4656-4663.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kato J., Nishimura Y., Imamura R., Niki H., Hiraga S., Suzuki H. New topoisomerase essential for chromosome segregation in E. coli. Cell. 1990 Oct 19;63(2):393–404. doi: 10.1016/0092-8674(90)90172-b. [DOI] [PubMed] [Google Scholar]
- Kohara Y., Akiyama K., Isono K. The physical map of the whole E. coli chromosome: application of a new strategy for rapid analysis and sorting of a large genomic library. Cell. 1987 Jul 31;50(3):495–508. doi: 10.1016/0092-8674(87)90503-4. [DOI] [PubMed] [Google Scholar]
- Kowalczykowski S. C., Dixon D. A., Eggleston A. K., Lauder S. D., Rehrauer W. M. Biochemistry of homologous recombination in Escherichia coli. Microbiol Rev. 1994 Sep;58(3):401–465. doi: 10.1128/mr.58.3.401-465.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kuempel P. L., Henson J. M., Dircks L., Tecklenburg M., Lim D. F. dif, a recA-independent recombination site in the terminus region of the chromosome of Escherichia coli. New Biol. 1991 Aug;3(8):799–811. [PubMed] [Google Scholar]
- Kuempel P., Høgaard A., Nielsen M., Nagappan O., Tecklenburg M. Use of a transposon (Tndif) to obtain suppressing and nonsuppressing insertions of the dif resolvase site of Escherichia coli. Genes Dev. 1996 May 1;10(9):1162–1171. doi: 10.1101/gad.10.9.1162. [DOI] [PubMed] [Google Scholar]
- Kuzminov A. Instability of inhibited replication forks in E. coli. Bioessays. 1995 Aug;17(8):733–741. doi: 10.1002/bies.950170810. [DOI] [PubMed] [Google Scholar]
- Louarn J. M., Bouché J. P., Legendre F., Louarn J., Patte J. Characterization and properties of very large inversions of the E. coli chromosome along the origin-to-terminus axis. Mol Gen Genet. 1985;201(3):467–476. doi: 10.1007/BF00331341. [DOI] [PubMed] [Google Scholar]
- Louarn J. M., Louarn J., François V., Patte J. Analysis and possible role of hyperrecombination in the termination region of the Escherichia coli chromosome. J Bacteriol. 1991 Aug;173(16):5097–5104. doi: 10.1128/jb.173.16.5097-5104.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Louarn J., Cornet F., François V., Patte J., Louarn J. M. Hyperrecombination in the terminus region of the Escherichia coli chromosome: possible relation to nucleoid organization. J Bacteriol. 1994 Dec;176(24):7524–7531. doi: 10.1128/jb.176.24.7524-7531.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mahan M. J., Roth J. R. Role of recBC function in formation of chromosomal rearrangements: a two-step model for recombination. Genetics. 1989 Mar;121(3):433–443. doi: 10.1093/genetics/121.3.433. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Martin B., Sharples G. J., Humbert O., Lloyd R. G., Claverys J. P. The mmsA locus of Streptococcus pneumoniae encodes a RecG-like protein involved in DNA repair and in three-strand recombination. Mol Microbiol. 1996 Mar;19(5):1035–1045. doi: 10.1046/j.1365-2958.1996.445975.x. [DOI] [PubMed] [Google Scholar]
- Rebollo J. E., François V., Louarn J. M. Detection and possible role of two large nondivisible zones on the Escherichia coli chromosome. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9391–9395. doi: 10.1073/pnas.85.24.9391. [DOI] [PMC free article] [PubMed] [Google Scholar]