Are Two Better Than One? Analysis of an FtsK/Xer Recombination System That Uses a Single Recombinase

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 2010 Jun 15

PMID 20542912

Citations 18

Authors

Sophie Nolivos

Carine Pages

Philippe Rousseau

Pascal Le Bourgeois

Francois Cornet

Affiliations

Soon will be listed here.

Abstract

Bacteria harbouring circular chromosomes have a Xer site-specific recombination system that resolves chromosome dimers at division. In Escherichia coli, the activity of the XerCD/dif system is controlled and coupled with cell division by the FtsK DNA translocase. Most Xer systems, as XerCD/dif, include two different recombinases. However, some, as the Lactococcus lactis XerS/dif(SL) system, include only one recombinase. We investigated the functional effects of this difference by studying the XerS/dif(SL) system. XerS bound and recombined dif(SL) sites in vitro, both activities displaying asymmetric characteristics. Resolution of chromosome dimers by XerS/dif(SL) required translocation by division septum-borne FtsK. The translocase domain of L. lactis FtsK supported recombination by XerCD/dif, just as E. coli FtsK supports recombination by XerS/dif(SL). Thus, the FtsK-dependent coupling of chromosome segregation with cell division extends to non-rod-shaped bacteria and outside the phylum Proteobacteria. Both the XerCD/dif and XerS/dif(SL) recombination systems require the control activities of the FtsKγ subdomain. However, FtsKγ activates recombination through different mechanisms in these two Xer systems. We show that FtsKγ alone activates XerCD/dif recombination. In contrast, both FtsKγ and the translocation motor are required to activate XerS/dif(SL) recombination. These findings have implications for the mechanisms by which FtsK activates recombination.

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References

Graham J, Sivanathan V, Sherratt D, Arciszewska L . FtsK translocation on DNA stops at XerCD-dif. Nucleic Acids Res. 2009; 38(1):72-81. PMC: 2800217. DOI: 10.1093/nar/gkp843. View

Lowe J, Ellonen A, Allen M, Atkinson C, Sherratt D, Grainge I . Molecular mechanism of sequence-directed DNA loading and translocation by FtsK. Mol Cell. 2008; 31(4):498-509. PMC: 2570039. DOI: 10.1016/j.molcel.2008.05.027. View

Kaimer C, Gonzalez-Pastor J, Graumann P . SpoIIIE and a novel type of DNA translocase, SftA, couple chromosome segregation with cell division in Bacillus subtilis. Mol Microbiol. 2009; 74(4):810-25. DOI: 10.1111/j.1365-2958.2009.06894.x. View

Bigot S, Corre J, Louarn J, Cornet F, Barre F . FtsK activities in Xer recombination, DNA mobilization and cell division involve overlapping and separate domains of the protein. Mol Microbiol. 2004; 54(4):876-86. DOI: 10.1111/j.1365-2958.2004.04335.x. View

Ptacin J, Nollmann M, Bustamante C, Cozzarelli N . Identification of the FtsK sequence-recognition domain. Nat Struct Mol Biol. 2006; 13(11):1023-5. DOI: 10.1038/nsmb1157. View

Possoz C, Ribard C, Gagnat J, Pernodet J, Guerineau M . The integrative element pSAM2 from Streptomyces: kinetics and mode of conjugal transfer. Mol Microbiol. 2001; 42(1):159-66. DOI: 10.1046/j.1365-2958.2001.02618.x. View

Steiner W, KUEMPEL P . Cell division is required for resolution of dimer chromosomes at the dif locus of Escherichia coli. Mol Microbiol. 1998; 27(2):257-68. DOI: 10.1046/j.1365-2958.1998.00651.x. View

Hallet B, Sherratt D . Transposition and site-specific recombination: adapting DNA cut-and-paste mechanisms to a variety of genetic rearrangements. FEMS Microbiol Rev. 1997; 21(2):157-78. DOI: 10.1111/j.1574-6976.1997.tb00349.x. View

Cornet F, Mortier I, PATTE J, Louarn J . 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; 176(11):3188-95. PMC: 205487. DOI: 10.1128/jb.176.11.3188-3195.1994. View

10.

Bregu M, Sherratt D, Colloms S . Accessory factors determine the order of strand exchange in Xer recombination at psi. EMBO J. 2002; 21(14):3888-97. PMC: 126124. DOI: 10.1093/emboj/cdf379. View

11.

Blakely G, May G, McCulloch R, Arciszewska L, Burke M, Lovett S . Two related recombinases are required for site-specific recombination at dif and cer in E. coli K12. Cell. 1993; 75(2):351-61. DOI: 10.1016/0092-8674(93)80076-q. View

12.

Arciszewska L, Sherratt D . Xer site-specific recombination in vitro. EMBO J. 1995; 14(9):2112-20. PMC: 398313. DOI: 10.1002/j.1460-2075.1995.tb07203.x. View

13.

Bigot S, Sivanathan V, Possoz C, Barre F, Cornet F . FtsK, a literate chromosome segregation machine. Mol Microbiol. 2007; 64(6):1434-41. DOI: 10.1111/j.1365-2958.2007.05755.x. View

14.

Sciochetti S, Piggot P, Blakely G . Identification and characterization of the dif Site from Bacillus subtilis. J Bacteriol. 2001; 183(3):1058-68. PMC: 94974. DOI: 10.1128/JB.183.3.1058-1068.2001. View

15.

Gonzalez M, Lichtensteiger C, Caughlan R, Vimr E . Conserved filamentous prophage in Escherichia coli O18:K1:H7 and Yersinia pestis biovar orientalis. J Bacteriol. 2002; 184(21):6050-5. PMC: 135385. DOI: 10.1128/JB.184.21.6050-6055.2002. View

16.

Yates J, Aroyo M, Sherratt D, Barre F . Species specificity in the activation of Xer recombination at dif by FtsK. Mol Microbiol. 2003; 49(1):241-9. DOI: 10.1046/j.1365-2958.2003.03574.x. View

17.

Perals K, Capiaux H, Vincourt J, Louarn J, Sherratt D, Cornet F . Interplay between recombination, cell division and chromosome structure during chromosome dimer resolution in Escherichia coli. Mol Microbiol. 2001; 39(4):904-13. DOI: 10.1046/j.1365-2958.2001.02277.x. View

18.

Levy O, Ptacin J, Pease P, Gore J, Eisen M, Bustamante C . Identification of oligonucleotide sequences that direct the movement of the Escherichia coli FtsK translocase. Proc Natl Acad Sci U S A. 2005; 102(49):17618-23. PMC: 1287487. DOI: 10.1073/pnas.0508932102. View

19.

Sherratt D, Soballe B, Barre F, Filipe S, Lau I, Massey T . Recombination and chromosome segregation. Philos Trans R Soc Lond B Biol Sci. 2004; 359(1441):61-9. PMC: 1693297. DOI: 10.1098/rstb.2003.1365. View

20.

Maguin E, Prevost H, Ehrlich S, Gruss A . Efficient insertional mutagenesis in lactococci and other gram-positive bacteria. J Bacteriol. 1996; 178(3):931-5. PMC: 177749. DOI: 10.1128/jb.178.3.931-935.1996. View