Cell Size and the Initiation of DNA Replication in Bacteria

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In eukaryotes, DNA replication is coupled to the cell cycle through the actions of cyclin-dependent kinases and associated factors. In bacteria, the prevailing view, based primarily from work in Escherichia coli, is that growth-dependent accumulation of the highly conserved initiator, DnaA, triggers initiation. However, the timing of initiation is unchanged in Bacillus subtilis mutants that are ∼30% smaller than wild-type cells, indicating that achievement of a particular cell size is not obligatory for initiation. Prompted by this finding, we re-examined the link between cell size and initiation in both E. coli and B. subtilis. Although changes in DNA replication have been shown to alter both E. coli and B. subtilis cell size, the converse (the effect of cell size on DNA replication) has not been explored. Here, we report that the mechanisms responsible for coordinating DNA replication with cell size vary between these two model organisms. In contrast to B. subtilis, small E. coli mutants delayed replication initiation until they achieved the size at which wild-type cells initiate. Modest increases in DnaA alleviated the delay, supporting the view that growth-dependent accumulation of DnaA is the trigger for replication initiation in E. coli. Significantly, although small E. coli and B. subtilis cells both maintained wild-type concentration of DnaA, only the E. coli mutants failed to initiate on time. Thus, rather than the concentration, the total amount of DnaA appears to be more important for initiation timing in E. coli. The difference in behavior of the two bacteria appears to lie in the mechanisms that control the activity of DnaA.

Vyšlo v časopise: Cell Size and the Initiation of DNA Replication in Bacteria. PLoS Genet 8(3): e32767. doi:10.1371/journal.pgen.1002549
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002549

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Zdroje

1. SclafaniRAHolzenTM 2007 Cell cycle regulation of DNA replication. Annu Rev Genet 41 237 280

2. DonachieWD 1968 Relationship between cell size and time of initiation of DNA replication. Nature 219 1077 1079

3. KatayamaTOzakiSKeyamuraKFujimitsuK 2010 Regulation of the replication cycle: conserved and diverse regulatory systems for DnaA and oriC. Nat Rev Microbiol 8 163 170

4. SchaechterMMaaløeOKjeldgaardNO 1958 Dependency on medium and temperature of cell size and chemical composition during balanced grown of Salmonella typhimurium. J Gen Microbiol 19 592 606

5. CooperSHelmstetterCE 1968 Chromosome replication and the division cycle of Escherichia coli B/r. J Mol Biol 31 519 540

6. Løbner-OlesenASkarstadKHansenFGvon MeyenburgKBoyeE 1989 The DnaA protein determines the initiation mass of Escherichia coli K-12. Cell 57 881 889

7. LeonardACGrimwadeJE 2010 Regulating DnaA complex assembly: it is time to fill the gaps. Curr Opin Microbiol 13 766 772

8. BramhillDKornbergA 1988 Duplex opening by dnaA protein at novel sequences in initiation of replication at the origin of the E. coli chromosome. Cell 52 743 755

9. DuderstadtKEChuangKBergerJM 2011 DNA stretching by bacterial initiators promotes replication origin opening. Nature 478 209 213

10. CampbellJLKlecknerN 1990 E. coli oriC and the dnaA gene promoter are sequestered from dam methyltransferase following passage of the chromosomal replication fork. Cell 62 967 979

11. KatoJKatayamaT 2001 Hda, a novel DnaA-related protein, regulates the replication cycle in Escherichia coli. EMBO J 20 4253 4262

12. CamaraJEBreierAMBrendlerTAustinSCozzarelliNR 2005 Hda inactivation of DnaA is the predominant mechanism preventing hyperinitiation of Escherichia coli DNA replication. EMBO Rep 6 736 741

13. KitagawaRMitsukiHOkazakiTOgawaT 1996 A novel DnaA protein-binding site at 94.7 min on the Escherichia coli chromosome. Mol Microbiol 19 1137 1147

14. NishidaSFujimitsuKSekimizuKOhmuraTUedaT 2002 A nucleotide switch in the Escherichia coli DnaA protein initiates chromosomal replication: evidnece from a mutant DnaA protein defective in regulatory ATP hydrolysis in vitro and in vivo. J Biol Chem 277 14986 14995

15. SimmonsLABreierAMCozzarelliNRKaguniJM 2004 Hyperinitiation of DNA replication in Escherichia coli leads to replication fork collapse and inviability. Mol Microbiol 51 349 358

16. RiberLLøbner-OlesenA 2005 Coordinated replication and sequestration of oriC and dnaA are required for maintaining controlled once-per-cell-cycle initiation in Escherichia coli. J Bacteriol 187 5605 5613

17. GorbatyukBMarczynskiGT 2001 Physiological consequences of blocked Caulobacter crescentus dnaA expression, an essential DNA replication gene. Mol Microbiol 40 485 497

18. CollierJShapiroL 2009 Feedback control of DnaA-mediated replication initiation by replisome-associated HdaA protein in Caulobacter. J Bacteriol 191 5706 5716

19. MuraiNKurokawaKIchihashiNMatsuoMSekimizuK 2006 Isolation of a temperature-sensitive dnaA mutant of Staphylococcus aureus. FEMS Microbiol Lett 254 19 26

20. SharpeMEHauserPMSharpeRGErringtonJ 1998 Bacillus subtilis cell cycle as studied by fluorescence microscopy: constancy of cell length at initiation of DNA replication and evidence for active nucleoid partitioning. J Bacteriol 180 547 555

21. MoriyaSKatoKYoshikawaHOgasawaraN 1990 Isolation of a dnaA mutant of Bacillus subtilis defective in initiation of replication: amount of DnaA protein determines cells initiation potential. EMBO J 9 2905 2910

22. OguraYImaiYOgasawaraNMoriyaS 2001 Autoregulation of the dnaA-dnaN operon and effects of DnaA protein levels on replication initiation in Bacillus subtilis. J Bacteriol 183 3833 3841

23. OgasawaraNMoriyaSvon MeyenburgKHansenFGYoshikawaH 1985 Conservation of genes and their organization in the chromosomal replication origin region of Bacillus subtilis and Escherichia coli. EMBO J 4 3345 3350

24. ChoEOgasawaraNIshikawaS 2008 The functional analysis of YabA, which interacts with DnaA and regulates initiation of chromosome replication in Bacillus subtilis. Genes Genet Syst 83 111 125

25. GoranovAIBreierAMMerrikhHGrossmanAD 2009 YabA of Bacillus subtilis controls DnaA-mediated replication initiation but not the transcriptional response to replication stress. Mol Microbiol 74 454 466

26. Noirot-GrosMFDervynEWuLJMerveletPErringtonJ 2002 An expanded view of bacterial DNA replication. Proc Natl Acad Sci U S A 99 8342 8347

27. Noirot-GrosMFVeltenMYoshimuraMMcGovernSMorimotoT 2006 Functional dissection of YabA, a negative regulator of DNA replication initiation in Bacillus subtilis. Proc Natl Acad Sci U S A 103 2368 2373

28. SoufoCDSoufoHJNoirot-GrosMFSteindorfANoirotP 2008 Cell-cycle-dependent spatial sequestration of the DnaA replication initiator protein in Bacillus subtilis. Dev Cell 15 935 941

29. HayashiMOguraYHarryEJOgasawaraNMoriyaS 2005 Bacillus subtilis YabA is involved in determining the timing and synchrony of replication initiation. FEMS Microbiol Lett 247 73 79

30. MerrikhHGrossmanAD 2011 Control of the replication initiator DnaA by an anti-cooperativity factor. Mol Microbiol 82 434 446

31. MurrayHErringtonJ 2008 Dynamic control of the DNA replication initiation protein DnaA by Soj/ParA. Cell 135 74 84

32. ScholefieldGWhitingRErringtonJMurrayH 2011 Spo0J regulates the oligomeric state of Soj to trigger its switch from an activator to an inhibitor of DNA replication initiation. Mol Microbiol 79 1089 1100

33. IshikawaSOguraYYoshimuraMOkumuraHChoE 2007 Distribution of stable DnaA-binding sites on the Bacillus subtilis genome detected using a modified ChIP-chip method. DNA Res 14 155 168

34. WeartRBLeeAHChienACHaeusserDPHillNS 2007 A metabolic sensor governing cell size in bacteria. Cell 130 335 347

35. LuMKlecknerN 1994 Molecular cloning and characterization of the pgm gene encoding phosphoglucomutase of Escherichia coli. J Bacteriol 176 5847 5851

36. GeisslerBShiomiDMargolinW 2007 The ftsA* gain-of-function allele of Escherichia coli and its effects on the stability and dynamics of the Z ring. Microbiology 153 814 825

37. GeisslerBElrahebDMargolinW 2003 A gain-of-function mutation in ftsA bypasses the requirement for the essential cell division gene zipA in Escherichia coli. Proc Natl Acad Sci U S A 100 4197 4202

38. BoyeEStokkeTKlecknerNSkarstadK 1996 Coordinating DNA replication initiation with cell growth: differential roles for DnaA and SeqA proteins. Proc Natl Acad Sci USA 93 12206 12211

39. AtlungTHansenFG 1993 Three distinct chromosome replication states are induced by increasing concentrations of DnaA protein in Escherichia coli. J Bacteriol 175 6537 6545

40. BremerHChurchwardG 1977 An examination of the Cooper-Helmstetter theory of DNA replication in bacteria and its underlying assumptions. J Theor Biol 69 645 654

41. MichelsenOTeixeira de MattosMJJensenPRHansenFG 2003 Precise determinations of C and D periods by flow cytometry in Escherichia coli K-12 and B/r. Microbiology 149 1001 1010

42. GordonGSSitnikovDWebbCDTelemanAStraightA 1997 Chromosome and low copy plasmid segregation in E. coli: visual evidence for distinct mechanisms. Cell 90 1 20

43. Reyes-LamotheRPossozCDanilovaOSherrattDJ 2008 Independent positioning and action of Escherichia coli replisomes in live cells. Cell 133 90 102

44. FossumSCrookeESkarstadK 2007 Organization of sister origins and replisomes during multifork DNA replication in Escherichia coli. EMBO J 26 4514 4522

45. LemonKPGrossmanAD 1998 Localization of bacterial DNA polymerase: evidence for a factory model of replication. Science 282 1516 1519

46. LeePSLinDCMoriyaSGrossmanAD 2003 Effects of the chromosome partitioning protein Spo0J (ParB) on oriC positioning and replication initiation in Bacillus subtilis. J Bacteriol 185 1326 1337

47. Den BlaauwenTBuddelmeijerNAarsmanMEHameeteCMNanningaN 1999 Timing of FtsZ assembly in Escherichia coli. J Bacteriol 181 5167 5175

48. HwangDSKaguniJM 1988 Purification and characterization of the dnaA46 gene product. J Biol Chem 263 10625 10632

49. WeartRBLevinPA 2003 Growth rate-dependent regulation of medial FtsZ ring formation. J Bacteriol 185 2826 2834

50. HaeusserDPGarzaACBuscherAZLevinPA 2007 The division inhibitor EzrA contains a seven-residue patch required for maintaining the dynamic nature of the medial FtsZ ring. J Bacteriol 189 9001 9010

51. FukuokaTMoriyaSYoshikawaHOgasawaraN 1990 Purification and characterization of an initiation protein for chromosomal replication, DnaA, in Bacillus subtilis. J Biochem 107 732 739

52. SmitsWKMerrikhHBonillaCYGrossmanAD 2011 Primosomal proteins DnaD and DnaB are recruited to chromosomal regions bound by DnaA in Bacillus subtilis. J Bacteriol 193 640 648

53. ZaritskyAWangPVischerNO 2011 Instructive simulation of the bacterial cell division cycle. Microbiology 157 1876 1885

54. TorheimNKBoyeELøbner-OlesenAStokkeTSkarstadK 2000 The Escherichia coli SeqA protein destabilizes mutant DnaA204 protein. Mol Microbiol 37 629 638

55. AtlungTLøbner-OlesenAHansenFG 1987 Overproduction of DnaA protein stimulates initiation of chromosome and minichromosome replication in Escherichia coli. Mol Gen Genet 206 51 59

56. HelmstetterCE 1968 DNA synthesis during the division cycle of rapidly growing Escherichia coli B/r. J Mol Biol 31 507 518

57. Von FreieslebenURasmussenKVAtlungTHansenFG 2000 Rifampicin-resistant initiation of chromosome replication from oriC in ihf mutants. Mol Microbiol 37 1087 1093

58. AtlungTHansenFG 2002 Effect of different concentrations of H-NS protein on chromosome replication and the cell cycle in Escherichia coli. J Bacteriol 184 1843 1850

59. MorigenOdsbuISkarstadK 2009 Growth rate dependent numbers of SeqA structures organize the multiple replication forks in rapidly growing Escherichia coli. Genes Cells 14 643 657

60. HardyCDCozzarelliNR 2005 A genetic selection for supercoiling mutants of Escherichia coli reveals proteins implicated in chromosome structure. Mol Microbiol 57 1636 1652

61. PostowLCrisonaNJPeterBJHardyCDCozzarelliNR 2001 Topological challenges to DNA replication: conformations at the fork. Proc Natl Acad Sci U S A 98 8219 8226

62. ClarkDJMaaløeO 1967 DNA replication and the division cycle in Escherichia coli. J Mol Biol 23 99 112

63. JaacksKJHealyJLosickRGrossmanAD 1989 Identification and characterization of genes controlled by the sporulation-regulatory gene spo0H in Bacillus subtilis. J Bacteriol 171 4121 4129

64. PfafflMW 2001 A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29 e45

65. SetlowBSetlowP 1998 Heat killing of Bacillus subtilis spores in water is not due to oxidative damage. Appl Environ Microbiol 64 4109 4112

66. FerulloDJCooperDLMooreHRLovettST 2009 Cell cycle synchronization of Escherichia coli using the stringent response, with fluorescence labeling assays for DNA content and replication. Methods 48 8 13

67. KearnsDBChuFBrandaSSKolterRLosickR 2005 A master regulator for biofilm formation by Bacillus subtilis. Mol Microbiol 55 739 749

68. WoldSSkarstadKSteenHBStokkeTBoyeE 1994 The initiation mass for DNA replication in Escherichia coli K-12 is dependent on growth rate. EMBO J 13 2097 2102

69. SekimizuKYungBYKornbergA 1988 The dnaA protein of Escherichia coli. Abundance, improved purification, and membrane binding. J Biol Chem 263 7136 7140

70. HansenFGAtlungTBraunREWrightAHughesP 1991 Initiator (DnaA) protein concentration as a function of growth rate in Escherichia coli and Salmonella typhimurium. J Bacteriol 173 5194 5199