Multiple Regulatory Systems Coordinate DNA Replication with Cell Growth in

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DNA replication must be coordinated with cellular physiology to ensure proper genome inheritance. Model bacteria such as the soil-dwelling Bacillus subtilis can achieve a wide range of growth rates in response to nutritional and chemical signals. In order to match the rate of DNA synthesis to the rate of nutrient-mediated cell growth, bacteria regulate the initiation frequency of DNA replication. This control of bacterial DNA replication initiation was first observed over forty years ago, however the molecular basis for this regulation has remained hotly debated. In this paper we test one of the leading models for nutrient-mediated growth rate regulation in bacteria, namely that the abundance of the master DNA replication initiation protein DnaA dictates the frequency of DNA replication events. Critically, our results show that changes in DnaA protein level are not sufficient to account for nutrient-mediated growth rate regulation of DNA replication initiation in B. subtilis. We then go on to show that there are strong connections between DNA replication and several essential cellular activities, which unexpectedly indicates that there is likely more than one single regulatory pathway involved in coordinating DNA replication with cell physiology. We believe that our work changes thinking regarding this long-standing biological question and reinvigorates the search for the molecular basis of these critical regulatory systems.

Vyšlo v časopise: Multiple Regulatory Systems Coordinate DNA Replication with Cell Growth in. PLoS Genet 10(10): e32767. doi:10.1371/journal.pgen.1004731
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004731

Souhrn

Zdroje

1. CooperS, HelmstetterCE (1968) Chromosome replication and the division cycle of Escherichia coli B/r. J Mol Biol 31: 519–540.

2. HelmstetterCE, CooperS (1968) DNA synthesis during the division cycle of rapidly growing Escherichia coli B/r. J Mol Biol 31: 507–518.

3. SchaechterM, MaaloeO, KjelgaardNO (1958) Dependency on medium and temperature on cell size and chemical coposition during balanced growth of Salmonella typhimurium. J Gen Microbiol 19: 592–606.

4. DonachieWD (1968) Relationship between cell size and time of initiation of DNA replication. Nature 219: 1077–1079.

5. WoldS, SkarstadK, SteenHB, StokkeT, BoyeE (1994) The initiation mass for DNA replication in Escherichia coli K-12 is dependent on growth rate. EMBO J 13: 2097–2102.

6. LeonardAC, GrimwadeJE (2011) Regulation of DnaA Assembly and Activity: Taking Directions from the Genome. Annu Rev Microbiol 65: 19–35.

7. DuderstadtKE, ChuangK, BergerJM (2011) DNA stretching by bacterial initiators promotes replication origin opening. Nature 478: 209–213.

8. AtlungT, Lobner-OlesenA, HansenFG (1987) Overproduction of DnaA protein stimulates initiation of chromosome and minichromosome replication in Escherichia coli. Mol Gen Genet 206: 51–59.

9. Lobner-OlesenA, SkarstadK, HansenFG, von MeyenburgK, BoyeE (1989) The DnaA protein determines the initiation mass of Escherichia coli K-12. Cell 57: 881–889.

10. HillNS, KadoyaR, ChattorajDK, LevinPA (2012) Cell size and the initiation of DNA replication in bacteria. PLoS Genetics 8: e1002549.

11. BoyeE, NordstromK (2003) Coupling the cell cycle to cell growth. EMBO Rep 4: 757–760.

12. OguraY, ImaiY, OgasawaraN, MoriyaS (2001) Autoregulation of the dnaAzdnaN operon and effects of DnaA protein levels on replication initiation in Bacillus subtilis. J Bacteriol 183: 3833–3841.

13. GoranovAI, BreierAM, MerrikhH, GrossmanAD (2009) YabA of Bacillus subtilis controls DnaA-mediated replication initiation but not the transcriptional response to replication stress. Mol Microbiol 74: 454–466.

14. SharpeME, HauserPM, SharpeRG, ErringtonJ (1998) Bacillus subtilis cell cycle as studied by fluorescence microscopy: constancy of the cell length at initiation of DNA replication and evidence for active nucleoid partitioning. J Bacteriol 180: 547–555.

15. LarkKG, MaaloeO (1956) Nucleic acid synthesis and the division cycle of Salmonella typhimurium. Biochim Biophys Acta 21: 448–458.

16. LarkKG, MaaloeO, RostockO (1955) Cytological studies of nuclear division in Salmonella typhimurium. J Gen Microbiol 13: 318–326.

17. WeartRB, LevinPA (2003) Growth rate-dependent regulation of medial FtsZ ring formation. J Bacteriol 185: 2826–2834.

18. MuntelJ, FromionV, GoelzerA, MaabetaS, MaderU, et al. (2014) Comprehensive absolute quantification of the cytosolic proteome of Bacillus subtilis by data independent, parallel fragmentation in liquid chromatography/mass spectrometry (LC/MS(E)). Mol Cell Proteomics 13: 1008–1019.

19. HassanAK, MoriyaS, OguraM, TanakaT, KawamuraF, et al. (1997) Suppression of initiation defects of chromosome replication in Bacillus subtilis dnaA and oriC-deleted mutants by integration of a plasmid replicon into the chromosomes. J Bacteriol 179: 2494–2502.

20. GoranovAI, KatzL, BreierAM, BurgeCB, GrossmanAD (2005) A transcriptional response to replication status mediated by the conserved bacterial replication protein DnaA. Proc Natl Acad Sci U S A 102: 12932–12937.

21. MurrayH, ErringtonJ (2008) Dynamic control of the DNA replication initiation protein DnaA by Soj/ParA. Cell 135: 74–84.

22. ScholefieldG, ErringtonJ, MurrayH (2012) Soj/ParA stalls DNA replication by inhibiting helix formation of the initiator protein DnaA. EMBO J 31: 1542–1555.

23. OguraY, OgasawaraN, HarryEJ, MoriyaS (2003) Increasing the ratio of Soj to Spo0J promotes replication initiation in Bacillus subtilis. J Bacteriol 185: 6316–6324.

24. SoufoCD, SoufoHJ, Noirot-GrosMF, SteindorfA, NoirotP, et al. (2008) Cell-cycle-dependent spatial sequestration of the DnaA replication initiator protein in Bacillus subtilis. Dev Cell 15: 935–941.

25. MerrikhH, GrossmanAD (2011) Control of the replication initiator DnaA by an anti-cooperativity factor. Mol Microbiol 82: 434–446.

26. ScholefieldG, MurrayH (2013) YabA and DnaD inhibit helix assembly of the DNA replication initiation protein DnaA. Mol Microbiol 90: 147–159.

27. Noirot-GrosMF, DervynE, WuLJ, MerveletP, ErringtonJ, et al. (2002) An expanded view of bacterial DNA replication. Proc Natl Acad Sci USA 99: 8342–8347.

28. LeePS, GrossmanAD (2006) The Chromosome partitioning proteins Soj (ParA) and Spo0J (ParB) contribute to accurate chromosome partitioning, separation of replicated sister origins, and regulation of replication initiation in Bacillus subtilis. Mol Microbiol 60: 853–869.

29. WangX, TangOW, RileyEP, RudnerDZ (2014) The SMC Condensin Complex Is Required for Origin Segregation in Bacillus subtilis. Curr Biol 24: 287–292.

30. Wang X, Montero Llopis P, Rudner DZ (2014) Bacillus subtilis chromosome organization oscillates between two distinct patterns. Proc Natl Acad Sci USA 10.1073/pnas.1407461111.

31. KawakamiH, KeyamuraK, KatayamaT (2005) Formation of an ATP-DnaA-specific initiation complex requires DnaA Arginine 285, a conserved motif in the AAA+ protein family. J Biol Chem 280: 27420–27430.

32. JanniereL, CanceillD, SuskiC, KangaS, DalmaisB, et al. (2007) Genetic evidence for a link between glycolysis and DNA replication. PloS One 2: e447.

33. MaciagM, NowickiD, JanniereL, Szalewska-PalaszA, WegrzynG (2011) Genetic response to metabolic fluctuations: correlation between central carbon metabolism and DNA replication in Escherichia coli. Microb Cell Fact 10: 19.

34. SchneiderDA, GourseRL (2004) Relationship between growth rate and ATP concentration in Escherichia coli: a bioassay for available cellular ATP. J Biol Chem 279: 8262–8268.

35. PetersenC, MollerLB (2000) Invariance of the nucleoside triphosphate pools of Escherichia coli with growth rate. J Biol Chem 275: 3931–3935.

36. SaxenaR, FinglandN, PatilD, SharmaAK, CrookeE (2013) Crosstalk between DnaA protein, the initiator of Escherichia coli chromosomal replication, and acidic phospholipids present in bacterial membranes. Int J Mol Sci 14: 8517–8537.

37. SikoraAE, ZielkeR, WegrzynA, WegrzynG (2006) DNA replication defect in the Escherichia coli cgtA(ts) mutant arising from reduced DnaA levels. Arch Microbiol 185: 340–347.

38. MoriyaS, FukuokaT, OgasawaraN, YoshikawaH (1988) Regulation of initiation of the chromosomal replication by DnaA-boxes in the origin region of the Bacillus subtilis chromosome. EMBO J 7: 2911–2917.

39. LevineA, VannierF, DehbiM, HenckesG, SerorSJ (1991) The stringent response blocks DNA replication outside the ori region in Bacillus subtilis and at the origin in Escherichia coli. J Mol Biol 219: 605–613.

40. WangJD, SandersGM, GrossmanAD (2007) Nutritional control of elongation of DNA replication by (p)ppGpp. Cell 128: 865–875.

41. LesleyJA, ShapiroL (2008) SpoT regulates DnaA stability and initiation of DNA replication in carbon-starved Caulobacter crescentus. J Bacteriol 190: 6867–6880.

42. SchreiberG, RonEZ, GlaserG (1995) ppGpp-mediated regulation of DNA replication and cell division in Escherichia coli. Current Microbiol 30: 27–32.

43. SekimizuK, KornbergA (1988) Cardiolipin activation of DnaA protein, the initiation protein of replication in Escherichia coli. J Biol Chem 263: 7131–7135.

44. XiaW, DowhanW (1995) In vivo evidence for the involvement of anionic phospholipids in initiation of DNA replication in Escherichia coli. Proc Natl Acad Sci USA 92: 783–787.

45. BreierAM, GrossmanAD (2009) Dynamic association of the replication initiator and transcription factor DnaA with the Bacillus subtilis chromosome during replication stress. J Bacteriol 191: 486–493.