Advertisement

The FtsK Family of DNA Pumps

  • Gaëlle Demarre
  • Elisa Galli
  • François-Xavier Barre
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 973)

Abstract

Interest for proteins of the FtsK family initially arose from their implication in many primordial processes in which DNA needs to be transported from one cell compartment to another in eubacteria. In the first section of this chapter, we address a list of the cellular functions of the different members of the FtsK family that have been so far studied. Soon after their discovery, interest for the FstK proteins spread because of their unique biochemical properties: most DNA transport systems rely on the assembly of complex multicomponent machines. In contrast, six FtsK proteins are sufficient to assemble into a fast and powerful DNA pump; the pump transports closed circular double stranded DNA molecules without any covalent-bond breakage nor topological alteration; transport is oriented despite the intrinsic symmetrical nature of the double stranded DNA helix and can occur across cell membranes. The different activities required for the oriented transport of DNA across cell compartments are achieved by three separate modules within the FtsK proteins: a DNA translocation module, an orientation module and an anchoring module. In the second part of this chapter, we review the structural and biochemical properties of these different modules.

Keywords

Chromosome Segregation Transmembrane Helix Conjugative Plasmid Septum Formation Cell Division Protein 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

We would like to acknowledge financial support from the Agence Nationale pour la Recherche [ANR-09-BLAN-0258] and from the European Research Council under the European Community’s Seventh Framework Programme [FP7/2007-2013 Grant Agreement no. 281590].

References

  1. 1.
    Mitchison TJ, Salmon ED. Mitosis: a history of division. Nat Cell Biol. 2001;3(1):E17–21.PubMedCrossRefGoogle Scholar
  2. 2.
    Bouet JY, Nordstrom K, Lane D. Plasmid partition and incompatibility–the focus shifts. Mol Microbiol. 2007;65(6):1405–14.PubMedCrossRefGoogle Scholar
  3. 3.
    Schumacher MA. Structural biology of plasmid partition: uncovering the molecular mechanisms of DNA segregation. Biochem J. 2008;412(1):1–18.PubMedCrossRefGoogle Scholar
  4. 4.
    Wu LJ, Lewis PJ, Allmansberger R, Hauser PM, Errington J. A conjugation-like mechanism for prespore chromosome partitioning during sporulation in Bacillus subtilis. Genes Dev. 1995;9(11):1316–26.PubMedCrossRefGoogle Scholar
  5. 5.
    Wu LJ, Errington J. Bacillus subtilis spoIIIE protein required for DNA segregation during asymmetric cell division. Science. 1994;264(5158):572–5.PubMedCrossRefGoogle Scholar
  6. 6.
    Barre FX, et al. FtsK functions in the processing of a Holliday junction intermediate during bacterial chromosome segregation. Genes Dev. 2000;14(23):2976–88.PubMedCrossRefGoogle Scholar
  7. 7.
    Steiner W, Liu G, Donachie WD, Kuempel P. The cytoplasmic domain of FtsK protein is required for resolution of chromosome dimers. Mol Microbiol. 1999;31(2):579–83.PubMedCrossRefGoogle Scholar
  8. 8.
    Possoz C, Ribard C, Gagnat J, Pernodet JL, Guerineau M. The integrative element pSAM2 from Streptomyces: kinetics and mode of conjugal transfer. Mol Microbiol. 2001;42(1):159–66.PubMedCrossRefGoogle Scholar
  9. 9.
    Vogelmann J, et al. Conjugal plasmid transfer in Streptomyces resembles bacterial chromosome segregation by FtsK/SpoIIIE. EMBO J. 2011;30(11):2246–54.PubMedCrossRefGoogle Scholar
  10. 10.
    Dubarry N, Barre FX. Fully efficient chromosome dimer resolution in Escherichia coli cells lacking the integral membrane domain of FtsK. EMBO J. 2010;29(3):597–605.PubMedCrossRefGoogle Scholar
  11. 11.
    Burton BM, Marquis KA, Sullivan NL, Rapoport TA, Rudner DZ. The ATPase SpoIIIE transports DNA across fused septal membranes during sporulation in Bacillus subtilis. Cell. 2007;131(7):1301–12.PubMedCrossRefGoogle Scholar
  12. 12.
    Fleming TC, et al. Dynamic SpoIIIE assembly mediates septal membrane fission during Bacillus subtilis sporulation. Genes Dev. 2010;24(11):1160–72.PubMedCrossRefGoogle Scholar
  13. 13.
    Saleh OA, Bigot S, Barre FX, Allemand JF. Analysis of DNA supercoil induction by FtsK indicates translocation without groove-tracking. Nat Struct Mol Biol. 2005;12(5):436–40.PubMedCrossRefGoogle Scholar
  14. 14.
    Bigot S, et al. KOPS: DNA motifs that control E. coli chromosome segregation by orienting the FtsK translocase. EMBO J. 2005;24(21):3770–80.PubMedCrossRefGoogle Scholar
  15. 15.
    Ptacin JL, et al. Sequence-directed DNA export guides chromosome translocation during sporulation in Bacillus subtilis. Nat Struct Mol Biol. 2008;15(5):485–93.PubMedCrossRefGoogle Scholar
  16. 16.
    Levy O, et al. 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.PubMedCrossRefGoogle Scholar
  17. 17.
    Becker EC, Pogliano K. Cell-specific SpoIIIE assembly and DNA translocation polarity are dictated by chromosome orientation. Mol Microbiol. 2007;66(5):1066–79.PubMedCrossRefGoogle Scholar
  18. 18.
    Piggot PJ, Hilbert DW. Sporulation of Bacillus subtilis. Curr Opin Microbiol. 2004;7(6):579–86.PubMedCrossRefGoogle Scholar
  19. 19.
    Wu LJ, Errington J. Septal localization of the SpoIIIE chromosome partitioning protein in Bacillus subtilis. EMBO J. 1997;16(8):2161–9.PubMedCrossRefGoogle Scholar
  20. 20.
    Bath J, Wu LJ, Errington J, Wang JC. Role of bacillus subtilis SpoIIIE in DNA transport across the mother cell-prespore division septum. Science. 2000;290(5493):995–7.PubMedCrossRefGoogle Scholar
  21. 21.
    Ben-Yehuda S, Rudner DZ, Losick R. Assembly of the SpoIIIE DNA translocase depends on chromosome trapping in Bacillus subtilis. Curr Biol. 2003;13(24):2196–200.PubMedGoogle Scholar
  22. 22.
    Sharp MD, Pogliano K. Role of cell-specific SpoIIIE assembly in polarity of DNA transfer. Science. 2002;295(5552):137–9.PubMedCrossRefGoogle Scholar
  23. 23.
    Sharp MD, Pogliano K. MinCD-dependent regulation of the polarity of SpoIIIE assembly and DNA transfer. EMBO J. 2002;21(22):6267–74.PubMedCrossRefGoogle Scholar
  24. 24.
    Sharp MD, Pogliano K. An in vivo membrane fusion assay implicates SpoIIIE in the final stages of engulfment during Bacillus subtilis sporulation. Proc Natl Acad Sci U S A. 1999;96(25):14553–8.PubMedCrossRefGoogle Scholar
  25. 25.
    Sharp MD, Pogliano K. The membrane domain of SpoIIIE is required for membrane fusion during Bacillus subtilis sporulation. J Bacteriol. 2003;185(6):2005–8.PubMedCrossRefGoogle Scholar
  26. 26.
    Liu NJ, Dutton RJ, Pogliano K. Evidence that the SpoIIIE DNA translocase participates in membrane fusion during cytokinesis and engulfment. Mol Microbiol. 2006;59(4):1097–113.PubMedCrossRefGoogle Scholar
  27. 27.
    Reuther J, Gekeler C, Tiffert Y, Wohlleben W, Muth G. Unique conjugation mechanism in mycelial streptomycetes: a DNA-binding ATPase translocates unprocessed plasmid DNA at the hyphal tip. Mol Microbiol. 2006;61(2):436–46.PubMedCrossRefGoogle Scholar
  28. 28.
    Val M-E, et al. FtsK-dependent dimer resolution on multiple chromosomes in the pathogen Vibrio cholerae. PLoS Genet. 2008;4(9):e1000201.PubMedCrossRefGoogle Scholar
  29. 29.
    Kono N, Arakawa K, Tomita M. Comprehensive prediction of chromosome dimer resolution sites in bacterial genomes. BMC Genomics. 2011;12(1):19.PubMedCrossRefGoogle Scholar
  30. 30.
    Begg KJ, Dewar SJ, Donachie WD. A new Escherichia coli cell division gene, ftsK. J Bacteriol. 1995;177(21):6211–22.PubMedGoogle Scholar
  31. 31.
    Di Lallo G, Fagioli M, Barionovi D, Ghelardini P, Paolozzi L. Use of a two-hybrid assay to study the assembly of a complex multicomponent protein machinery: bacterial septosome differentiation. Microbiology. 2003;149(Pt 12):3353–9.PubMedCrossRefGoogle Scholar
  32. 32.
    Yu XC, Tran AH, Sun Q, Margolin W. Localization of cell division protein FtsK to the Escherichia coli septum and identification of a potential N-terminal targeting domain. J Bacteriol. 1998;180(5):1296–304.PubMedGoogle Scholar
  33. 33.
    Wang L, Lutkenhaus J. FtsK is an essential cell division protein that is localized to the septum and induced as part of the SOS response. Mol Microbiol. 1998;29(3):731–40.PubMedCrossRefGoogle Scholar
  34. 34.
    Liu G, Draper GC, Donachie WD. FtsK is a bifunctional protein involved in cell division and chromosome localization in Escherichia coli. Mol Microbiol. 1998;29(3):893–903.PubMedCrossRefGoogle Scholar
  35. 35.
    Draper GC, McLennan N, Begg K, Masters M, Donachie WD. Only the N-terminal domain of FtsK functions in cell division. J Bacteriol. 1998;180(17):4621–7.PubMedGoogle Scholar
  36. 36.
    Chen JC, Beckwith J. FtsQ, FtsL and FtsI require FtsK, but not FtsN, for co-localization with FtsZ during Escherichia coli cell division. Mol Microbiol. 2001;42(2):395–413.PubMedCrossRefGoogle Scholar
  37. 37.
    Geissler B, Margolin W. Evidence for functional overlap among multiple bacterial cell division proteins: compensating for the loss of FtsK. Mol Microbiol. 2005;58(2):596–612.PubMedCrossRefGoogle Scholar
  38. 38.
    Dubarry N, Possoz C, Barre FX. Multiple regions along the Escherichia coli FtsK protein are implicated in cell division. Mol Microbiol. 2010;78(1088–1100):1088–100.PubMedCrossRefGoogle Scholar
  39. 39.
    Lesterlin C, Pages C, Dubarry N, Dasgupta S, Cornet F. Asymmetry of chromosome Replichores renders the DNA translocase activity of FtsK essential for cell division and cell shape maintenance in Escherichia coli. PLoS Genet. 2008;4(12):e1000288.PubMedCrossRefGoogle Scholar
  40. 40.
    Yu XC, Weihe EK, Margolin W. Role of the C terminus of FtsK in Escherichia coli chromosome segregation. J Bacteriol. 1998;180(23):6424–8.PubMedGoogle Scholar
  41. 41.
    Bigot S, Corre J, Louarn J, Cornet F, Barre FX. 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.PubMedCrossRefGoogle Scholar
  42. 42.
    Recchia GD, Aroyo M, Wolf D, Blakely G, Sherratt DJ. FtsK-dependent and -independent pathways of Xer site-specific recombination. EMBO J. 1999;18(20):5724–34.PubMedCrossRefGoogle Scholar
  43. 43.
    Deghorain M, et al. A defined terminal region of the E. coli chromosome shows late segregation and high FtsK activity. PLoS One. 2011;6(7):e22164.PubMedCrossRefGoogle Scholar
  44. 44.
    Capiaux H, Lesterlin C, Perals K, Louarn JM, Cornet F. A dual role for the FtsK protein in Escherichia coli chromosome segregation. EMBO Rep. 2002;3(6):532–6.PubMedCrossRefGoogle Scholar
  45. 45.
    Perals K, Cornet F, Merlet Y, Delon I, Louarn JM. Functional polarization of the Escherichia coli chromosome terminus: the dif site acts in chromosome dimer resolution only when located between long stretches of opposite polarity. Mol Microbiol. 2000;36(1):33–43.PubMedCrossRefGoogle Scholar
  46. 46.
    Bigot S, Saleh OA, Cornet F, Allemand JF, Barre FX. Oriented loading of FtsK on KOPS. Nat Struct Mol Biol. 2006;13(11):1026–8.PubMedCrossRefGoogle Scholar
  47. 47.
    Grainge I, Lesterlin C, Sherratt DJ. Activation of XerCD-dif recombination by the FtsK DNA translocase. Nucleic Acids Res. 2011;39(12):5140–8.PubMedCrossRefGoogle Scholar
  48. 48.
    Yates J, et al. Dissection of a functional interaction between the DNA translocase, FtsK, and the XerD recombinase. Mol Microbiol. 2006;59(6):1754–66.PubMedCrossRefGoogle Scholar
  49. 49.
    Massey TH, Aussel L, Barre F-X, Sherratt DJ. Asymmetric activation of Xer site-specific recombination by FtsK. EMBO Rep. 2004;5(4):399–404.PubMedCrossRefGoogle Scholar
  50. 50.
    Yates J, Aroyo M, Sherratt DJ, Barre FX. Species specificity in the activation of Xer recombination at dif by FtsK. Mol Microbiol. 2003;49(1):241–9.PubMedCrossRefGoogle Scholar
  51. 51.
    Aussel L, et al. FtsK is a DNA motor protein that activates chromosome dimer resolution by switching the catalytic state of the XerC and XerD recombinases. Cell. 2002;108(2):195–205.PubMedCrossRefGoogle Scholar
  52. 52.
    Nolivos S, Pages C, Rousseau P, Le Bourgeois P, Cornet F. Are two better than one? Analysis of an FtsK/Xer recombination system that uses a single recombinase. Nucleic Acids Res. 2010;38(19):6477–89.PubMedCrossRefGoogle Scholar
  53. 53.
    Nolivos S, et al. Co-evolution of segregation guide DNA motifs and the FtsK translocase in bacteria: identification of the atypical Lactococcus lactis KOPS motif. Nucleic Acids Res. 2012;40:5535–45.PubMedCrossRefGoogle Scholar
  54. 54.
    Kaimer C, Gonzalez-Pastor JE, Graumann PL. 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.PubMedCrossRefGoogle Scholar
  55. 55.
    Biller SJ, Burkholder WF. The Bacillus subtilis SftA (YtpS) and SpoIIIE DNA translocases play distinct roles in growing cells to ensure faithful chromosome partitioning. Mol Microbiol. 2009;74(4):790–809.PubMedCrossRefGoogle Scholar
  56. 56.
    Kaimer C, Schenk K, Graumann PL. Two DNA translocases synergistically affect chromosome dimer resolution in Bacillus subtilis. J Bacteriol. 2011;193(6):1334–40.PubMedCrossRefGoogle Scholar
  57. 57.
    Grainge I, et al. Unlinking chromosome catenanes in vivo by site-specific recombination. EMBO J. 2007;26(19):4228–38.PubMedCrossRefGoogle Scholar
  58. 58.
    Ip SC, Bregu M, Barre FX, Sherratt DJ. Decatenation of DNA circles by FtsK-dependent Xer site-specific recombination. EMBO J. 2003;22(23):6399–407.PubMedCrossRefGoogle Scholar
  59. 59.
    Bigot S, Marians KJ. DNA chirality-dependent stimulation of topoisomerase IV activity by the C-terminal AAA+ domain of FtsK. Nucleic Acids Res. 2010;38(9):3031–40.PubMedCrossRefGoogle Scholar
  60. 60.
    Espeli O, Levine C, Hassing H, Marians KJ. Temporal regulation of topoisomerase IV activity in E. coli. Mol Cell. 2003;11(1):189–201.PubMedCrossRefGoogle Scholar
  61. 61.
    Espeli O, Lee C, Marians KJ. A physical and functional interaction between Escherichia coli FtsK and topoisomerase IV. J Biol Chem. 2003;278(45):44639–44.PubMedCrossRefGoogle Scholar
  62. 62.
    Wang SC, West L, Shapiro L. The bifunctional FtsK protein mediates chromosome partitioning and cell division in Caulobacter. J Bacteriol. 2006;188(4):1497–508.PubMedCrossRefGoogle Scholar
  63. 63.
    Sivanathan V, et al. The FtsK gamma domain directs oriented DNA translocation by interacting with KOPS. Nat Struct Mol Biol. 2006;13(11):965–72.PubMedCrossRefGoogle Scholar
  64. 64.
    Massey TH, Mercogliano CP, Yates J, Sherratt DJ, Lowe J. Double-stranded DNA translocation: structure and mechanism of hexameric FtsK. Mol Cell. 2006;23:457–69.PubMedCrossRefGoogle Scholar
  65. 65.
    Iyer LM, Makarova KS, Koonin EV, Aravind L. Comparative genomics of the FtsK-HerA superfamily of pumping ATPases: implications for the origins of chromosome segregation, cell division and viral capsid packaging. Nucleic Acids Res. 2004;32(17):5260–79.PubMedCrossRefGoogle Scholar
  66. 66.
    Gomis-Ruth FX, et al. The bacterial conjugation protein TrwB resembles ring helicases and F1-ATPase. Nature. 2001;409(6820):637–41.PubMedCrossRefGoogle Scholar
  67. 67.
    Saleh OA, Perals C, Barre FX, Allemand JF. Fast, DNA-sequence independent translocation by FtsK in a single-molecule experiment. EMBO J. 2004;23(12):2430–9.PubMedCrossRefGoogle Scholar
  68. 68.
    Pease PJ, et al. Sequence-directed DNA translocation by purified FtsK. Science. 2005;307(5709):586–90.PubMedCrossRefGoogle Scholar
  69. 69.
    Lee JY, Finkelstein IJ, Crozat E, Sherratt DJ, Greene EC. Single-molecule imaging of DNA curtains reveals mechanisms of KOPS sequence targeting by the DNA translocase FtsK. Proc Natl Acad Sci U S A. 2012;109(17):6531–6.PubMedCrossRefGoogle Scholar
  70. 70.
    Marquis KA, et al. SpoIIIE strips proteins off the DNA during chromosome translocation. Genes Dev. 2008;22(13):1786–95.PubMedCrossRefGoogle Scholar
  71. 71.
    Lau IF, et al. Spatial and temporal organization of replicating Escherichia coli chromosomes. Mol Microbiol. 2003;49(3):731–43.PubMedCrossRefGoogle Scholar
  72. 72.
    Bonne L, Bigot S, Chevalier F, Allemand JF, Barre FX. Asymmetric DNA requirements in Xer recombination activation by FtsK. Nucleic Acids Res. 2009;37(7):2371–80.PubMedCrossRefGoogle Scholar
  73. 73.
    Graham JE, Sherratt DJ, Szczelkun MD. Sequence-specific assembly of FtsK hexamers establishes directional translocation on DNA. Proc Natl Acad Sci U S A. 2010;107(47):20263–8.PubMedCrossRefGoogle Scholar
  74. 74.
    Crozat E, et al. Separating speed and ability to displace roadblocks during DNA translocation by FtsK. EMBO J. 2010;29(8):1423–33.PubMedCrossRefGoogle Scholar
  75. 75.
    Graham JE, Sivanathan V, Sherratt DJ, Arciszewska LK. FtsK translocation on DNA stops at XerCD-dif. Nucleic Acids Res. 2009;38(1):72–81.PubMedCrossRefGoogle Scholar
  76. 76.
    Lowe J, et al. Molecular mechanism of sequence-directed DNA loading and translocation by FtsK. Mol Cell. 2008;31(4):498–509.PubMedCrossRefGoogle Scholar
  77. 77.
    Kennedy SP, Chevalier F, Barre FX. Delayed activation of Xer recombination at dif by FtsK during septum assembly in Escherichia coli. Mol Microbiol. 2008;68(4):1018–28.PubMedCrossRefGoogle Scholar
  78. 78.
    Enemark EJ, Joshua-Tor L. Mechanism of DNA translocation in a replicative hexameric helicase. Nature. 2006;442(7100):270–5.PubMedCrossRefGoogle Scholar
  79. 79.
    Cornet F, Louarn J, Patte J, Louarn JM. Restriction of the activity of the recombination site dif to a small zone of the Escherichia coli chromosome. Genes Dev. 1996;10(9):1152–61.PubMedCrossRefGoogle Scholar
  80. 80.
    Mercier R, et al. The MatP/matS site-specific system organizes the terminus region of the E. coli chromosome into a macrodomain. Cell. 2008;135(3):475–85.PubMedCrossRefGoogle Scholar
  81. 81.
    Espeli O, Mercier R, Boccard F. DNA dynamics vary according to macrodomain topography in the E. coli chromosome. Mol Microbiol. 2008;68(6):1418–27.PubMedCrossRefGoogle Scholar
  82. 82.
    Lesterlin C, Mercier R, Boccard F, Barre FX, Cornet F. Roles for replichores and macrodomains in segregation of the Escherichia coli chromosome. EMBO Rep. 2005;6:557–62.PubMedCrossRefGoogle Scholar
  83. 83.
    Valens M, Penaud S, Rossignol M, Cornet F, Boccard F. Macrodomain organization of the Escherichia coli chromosome. EMBO J. 2004;23(21):4330–41.PubMedCrossRefGoogle Scholar
  84. 84.
    Meile JC, et al. The terminal region of the E. coli chromosome localises at the periphery of the nucleoid. BMC Microbiol. 2011;11(1):28.PubMedCrossRefGoogle Scholar
  85. 85.
    Corre J, Patte J, Louarn JM. Prophage lambda induces terminal recombination in Escherichia coli by inhibiting chromosome dimer resolution. An orientation-dependent cis-effect lending support to bipolarization of the terminus. Genetics. 2000;154(1):39–48.PubMedGoogle Scholar
  86. 86.
    Corre J, Louarn JM. Evidence from terminal recombination gradients that FtsK uses replichore polarity to control chromosome terminus positioning at division in Escherichia coli. J Bacteriol. 2002;184(14):3801–7.PubMedCrossRefGoogle Scholar
  87. 87.
    Ptacin JL, Nollmann M, Bustamante C, Cozzarelli NR. Identification of the FtsK sequence-recognition domain. Nat Struct Mol Biol. 2006;13(11):1023–5.PubMedCrossRefGoogle Scholar
  88. 88.
    Spies M, et al. A molecular throttle: the recombination hotspot chi controls DNA translocation by the RecBCD helicase. Cell. 2003;114(5):647–54.PubMedCrossRefGoogle Scholar
  89. 89.
    Taylor AF, Schultz DW, Ponticelli AS, Smith GR. RecBC enzyme nicking at Chi sites during DNA unwinding: location and orientation-dependence of the cutting. Cell. 1985;41(1):153–63.PubMedCrossRefGoogle Scholar
  90. 90.
    Sourice S, Biaudet V, El Karoui M, Ehrlich SD, Gruss A. Identification of the Chi site of Haemophilus influenzae as several sequences related to the Escherichia coli Chi site. Mol Microbiol. 1998;27(5):1021–9.PubMedCrossRefGoogle Scholar
  91. 91.
    El Karoui M, et al. Orientation specificity of the Lactococcus lactis chi site. Genes Cells. 2000;5(6):453–61.PubMedCrossRefGoogle Scholar
  92. 92.
    El Karoui M, Biaudet V, Schbath S, Gruss A. Characteristics of Chi distribution on different bacterial genomes. Res Microbiol. 1999;150(9–10):579–87.PubMedCrossRefGoogle Scholar
  93. 93.
    Dorazi R, Dewar SJ. Membrane topology of the N-terminus of the Escherichia coli FtsK division protein. FEBS Lett. 2000;478(1–2):13–8.PubMedCrossRefGoogle Scholar
  94. 94.
    Barre FX. FtsK and SpoIIIE: the tale of the conserved tails. Mol Microbiol. 2007;66(5):1051–5.PubMedCrossRefGoogle Scholar
  95. 95.
    Perals K, et al. Interplay between recombination, cell division and chromosome structure during chromosome dimer resolution in Escherichia coli. Mol Microbiol. 2001;39(4):904–13.PubMedCrossRefGoogle Scholar
  96. 96.
    Le Bourgeois P, et al. The unconventional Xer recombination machinery of Streptococci/Lactococci. PLoS Genet. 2007;3(7):e117.PubMedCrossRefGoogle Scholar
  97. 97.
    McCool JD, Sandler SJ. Effects of mutations involving cell division, recombination, and chromosome dimer resolution on a priA2::kan mutant. Proc Natl Acad Sci U S A. 2001;98(15):8203–10.PubMedCrossRefGoogle Scholar
  98. 98.
    Thanbichler M. Synchronization of chromosome dynamics and cell division in bacteria. Cold Spring Harb Perspect Biol. 2010;2(1):a000331.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Gaëlle Demarre
    • 1
  • Elisa Galli
    • 1
  • François-Xavier Barre
    • 1
  1. 1.Centre de Génétique Moléculaire, CNRSGif sur Yvette, CedexFrance

Personalised recommendations