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Current Genetics

, Volume 64, Issue 5, pp 1029–1036 | Cite as

The bacterial replisome has factory-like localization

  • Sarah M. Mangiameli
  • Julie A. Cass
  • Houra Merrikh
  • Paul A. Wiggins
Review

Abstract

DNA replication is essential to cellular proliferation. The cellular-scale organization of the replication machinery (replisome) and the replicating chromosome has remained controversial. Two competing models describe the replication process: In the track model, the replisomes translocate along the DNA like a train on a track. Alternately, in the factory model, the replisomes form a stationary complex through which the DNA is pulled. We summarize the evidence for each model and discuss a number of confounding aspects that complicate interpretation of the observations. We advocate a factory-like model for bacterial replication where the replisomes form a relatively stationary and weakly associated complex that can transiently separate.

Keywords

DNA replication Replication factory Cell biology Bacteria 

Notes

Acknowledgements

The authors are grateful to Colin LaMont for the helpful comments on the manuscript.

References

  1. Meselson M, Stahl FW (1958) The replication of DNA in Escherichia coli, Proceedings of the National Academy of Sciences of the United States of America, vol 44, pp 671–682. http://www.ncbi.nlm.nih.gov/pubmed/16590258, http://www.pubmedcentral.nih.gov/articlerender.fcgi? artid=PMC528642
  2. Zechner EL, Wu CA, Marians KJ (1992) Coordinated leading- and lagging-strand synthesis at the Escherichia coli DNA replication fork. II. Frequency of primer synthesis and efficiency of primer utilization control Okazaki fragment size. J Biol Chem 267:4045–4053. http://www.ncbi.nlm.nih.gov/pubmed/1740452
  3. Sanders GM, Dallmann HG, McHenry CS (2010) Reconstitution of the B. subtilis Replisome with 13 proteins including two distinct replicases. Mol Cell 37:273–281. http://www.ncbi.nlm.nih.gov/pubmed/20122408, http://linkinghub.elsevier.com/retrieve/pii/S1097276509009563 CrossRefPubMedCentralGoogle Scholar
  4. Mangiameli SM, Merrikh CN, Wiggins PA, Merrikh H (2017) Transcription leads to pervasive replisome instability in bacteria. eLife.  https://doi.org/10.7554/eLife.19848. http://www.ncbi.nlm.nih.gov/pubmed/28092263, http://www.pubmedcentral.nih.gov/articlerender.fcgi? artid=PMC5305214
  5. Frimodt-Møller J, Charbon G, Løbner-Olesen A (2017) Control of bacterial chromosome replication by non-coding regions outside the origin. Curr Genet 63:607–611.  https://doi.org/10.1007/s00294-016-0671-6. http://link.springer.com/ 10.1007/s00294-016-0671-6 CrossRefPubMedCentralGoogle Scholar
  6. Frouin I, Montecucco A, Spadari S, Maga G (2003) DNA replication: a complex matter. EMBO Rep 4:666–670.  https://doi.org/10.1038/sj.embor.embor886. http://embor.embopress.org/content/ 4/7/666 CrossRefPubMedCentralGoogle Scholar
  7. Dingman CW (1974) Bidirectional chromosome replication: some topological considerations. J Theor Biol 43:187–195CrossRefPubMedCentralGoogle Scholar
  8. Newport J, Yan H (1996) Organization of DNA into foci during replication. Curr Opinion Cell Biol 8:365–368.  https://doi.org/10.1016/S0955-0674(96)80011-1 CrossRefPubMedCentralGoogle Scholar
  9. Ma H, Samarabandu J, Devdhar RS, Acharya R, Cheng P-C, Meng C, Berezney R (1998) Spatial and temporal dynamics of DNA replication sites in mammalian cells. J Cell Biol 143:1415–1425.  https://doi.org/10.1083/jcb.143.6.1415 CrossRefPubMedCentralGoogle Scholar
  10. Jackson DA, Pombo A (1998) Replicon clusters are stable units of chromosome structure: Evidence that nuclear organization contributes to the efficient activation and propagation of s phase in human cells. J Cell Biol 140:1285–1295.  https://doi.org/10.1083/jcb.140.6.1285. http://jcb.rupress.org/content/140/6/1285 CrossRefPubMedCentralGoogle Scholar
  11. Hozák P, Hassan AB, Jackson DA, Cook PR (1993) Visualization of replication factories attached to a nucleoskeleton. Cell.  https://doi.org/10.1016/0092-8674(93)90235-I CrossRefPubMedCentralGoogle Scholar
  12. Leonhardt H, Rahn H-P, Weinzierl P, Sporbert A, Cremer T, Zink D, Cardoso MC (2000) Dynamics of DNA replication factories in living cells. J Cell Biol 149:271–280.  https://doi.org/10.1083/jcb.149.2.271. http://jcb.rupress.org/content/149/2/271 CrossRefPubMedCentralGoogle Scholar
  13. Baker TA, Bell SP (1998) Polymerases and the replisome: machines within machines. Cell 92:295–305.  https://doi.org/10.1016/S0092-8674(00)80923-X CrossRefPubMedCentralGoogle Scholar
  14. Jensen RB, Wang SC, Shapiro L (2001) A moving dna replication factory in Caulobacter crescentus. EMBO J 20:4952–4963. http://emboj.embopress.org/content/20/17/4952 CrossRefPubMedCentralGoogle Scholar
  15. Lemon KP, Grossman AD (1998) Localization of bacterial DNA polymerase: evidence for a factory model of replication. Science 282:1516–1519CrossRefGoogle Scholar
  16. Lemon KP, Grossman AD (2000) Movement of replicating DNA through a stationary replisome. Mol Cell 6:1321–1330CrossRefPubMedCentralGoogle Scholar
  17. Berkmen MB, Grossman AD (2006) Spatial and temporal organization of the Bacillus subtilis replication cycle. Mol Microbiol 62:57–71.  https://doi.org/10.1111/j.1365-2958.2006.05356.x CrossRefPubMedCentralGoogle Scholar
  18. Mangiameli SM, Veit BT, Merrikh H, Wiggins PA (2017) The replisomes remain spatially proximal throughout the cell cycle in bacteria. PLoS Genet 13:1–17.  https://doi.org/10.1371/journal.pgen.1006582 CrossRefPubMedCentralGoogle Scholar
  19. Bates D, Kleckner N (2005) Chromosome and replisome dynamics in E. coli: loss of sister cohesion triggers global chromosome movement and mediates chromosome segregation. Cell 121:899–911CrossRefPubMedCentralGoogle Scholar
  20. Reyes-Lamothe R, Possoz C, Danilova O, Sherratt DJ (2008) Independent positioning and action of Escherichia coli replisomes in live cells. Cell 133:90–102CrossRefPubMedCentralGoogle Scholar
  21. Hiraga S, Ichinose C, Onogi T, Niki H, Yamazoe M (2000) Bidirectional migration of seqa-bound hemimethylated dna clusters and pairing of oric copies in Escherichia coli. Genes Cells 5:327–341.  https://doi.org/10.1046/j.1365-2443.2000.00334.x CrossRefPubMedCentralGoogle Scholar
  22. Kongsuwan K, Dalrymple BP, Wijffels G, Jennings PA (2002) Cellular localisation of the clamp protein during DNA replication. FEMS Microbiol Lett 216:255.  https://doi.org/10.1111/j.1574-6968.2002.tb11444.x CrossRefPubMedCentralGoogle Scholar
  23. Cass JA, Kuwada NJ, Traxler B, Wiggins PA (2016) Escherichia coli chromosomal loci segregate from midcell with universal dynamics. Biophys J 110:2597–2609CrossRefPubMedCentralGoogle Scholar
  24. Migocki MD, Lewis PJ, Wake RG, Harry EJ (2004) The midcell replication factory in Bacillus subtilis is highly mobile: implications for coordinating chromosome replication with other cell cycle events. Mol Microbiol 54:452–463.  https://doi.org/10.1111/j.1365-2958.2004.04267.x CrossRefPubMedCentralGoogle Scholar
  25. Reyes-Lamothe R, Sherratt DJ, Leake MC (2010) Stoichiometry and architecture of active DNA replication machinery in Escherichia coli. Science 328:498–501.  https://doi.org/10.1126/science.1185757. http://science.sciencemag.org/content/328/ 5977/498 CrossRefPubMedCentralGoogle Scholar
  26. Swulius MT, Jensen GJ (2012) The helical MreB cytoskeleton in Escherichia coli MC1000/pLE7 is an artifact of the N-Terminal yellow fluorescent protein tag. J Bacteriol 194:6382–6386.  https://doi.org/10.1128/JB.00505-12. http://www.ncbi.nlm.nih.gov/pubmed/22904287, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC3497537 CrossRefPubMedCentralGoogle Scholar
  27. Landgraf D, Okumus B, Chien P, Baker TA, Paulsson J (2012) Segregation of molecules at cell division reveals native protein localization. Nat Methods 9:480–482.  https://doi.org/10.1038/nmeth.1955. http://www.ncbi.nlm.nih.gov/pubmed/22484850www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC3779060, http://www.nature.com/doifinder/10.1038/nmeth.1955 CrossRefPubMedCentralGoogle Scholar
  28. Koppes LJ, Woldringh CL, Nanninga N (1999) Escherichia coli contains a DNA replication compartment in the cell center. Biochimie 81:803–810.  https://doi.org/10.1016/S0300-9084(99)00217-5 CrossRefPubMedCentralGoogle Scholar
  29. Molina F, Skarstad K (2004) Replication fork and SeqA focus distributions in Escherichia coli suggest a replication hyperstructure dependent on nucleotide metabolism. Mol Microbiol 52:1597–1612.  https://doi.org/10.1111/j.1365-2958.2004.04097.x CrossRefPubMedCentralGoogle Scholar
  30. Adachi S, Kohiyama M, Onogi T, Hiraga S (2005) Localization of replication forks in wild-type and mukB mutant cells of Escherichia coli. Mol Genet Genomics 274:264–271CrossRefPubMedCentralGoogle Scholar
  31. Den Blaauwen T, Aarsman MEG, Wheeler LJ, Nanninga N (2006) Pre-replication assembly of E. coli replisome components. Mol Microbiol 62:695–708CrossRefGoogle Scholar
  32. Wallden M, Fange D, Lundius EG, Baltekin O, Elf J (2016) The synchronization of replication and division cycles in individual E. coli cells. Cell 166:729–739.  https://doi.org/10.1016/j.cell.2016.06.052 CrossRefPubMedCentralGoogle Scholar
  33. Cass JA, Stylianidou S, Kuwada NJ, Traxler B, Wiggins PA (2017) Probing bacterial cell biology using image cytometry. Mol Microbiol 103:818–828.  https://doi.org/10.1111/mmi.13591 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Yamazoe M, Adachi S, Kanaya S, Ohsumi K, Hiraga S (2004).  https://doi.org/10.1111/j.1365-2958.2004.04389.x CrossRefGoogle Scholar
  35. Onogi T, Ohsumi K, Katayama T, Hiraga S (2002) Replication-dependent recruitment of the beta-subunit of DNA polymerase III from cytosolic spaces to replication forks in Escherichia coli. J Bacteriol 184:867–870.  https://doi.org/10.1128/jb.184.3.867-870.2002. http://www.ncbi.nlm.nih.gov/pubmed/11790763, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC139520 CrossRefPubMedCentralGoogle Scholar
  36. Sunako Y, Onogi T, Hiraga S (2002) Sister chromosome cohesion of Escherichia coli. Mol Microbiol 42:1233–1241.  https://doi.org/10.1046/j.1365-2958.2001.02680.x CrossRefGoogle Scholar
  37. Breier AM, Weier H-UG, Cozzarelli NR (2005) Independence of replisomes in Escherichia coli chromosomal replication. Proc Nat Acad Sci 102:3942–3947.  https://doi.org/10.1073/pnas.0500812102. http://www.ncbi.nlm.nih.gov/pubmed/15738384, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC552787, http://www.pnas.org/cgi/doi/10. 1073/pnas.0500812102 CrossRefGoogle Scholar
  38. Lemon KP, Grossman AD (2001) The extrusion-capture model for chromosome partitioning in bacteria. Genes Dev 15:2031–2041.  https://doi.org/10.1101/gad.913301. http://www.ncbi.nlm.nih.gov/pubmed/11511534 CrossRefGoogle Scholar
  39. Sawitzke J, Austin S (2001) An analysis of the factory model for chromosome replication and segregation in bacteria. Mol Microbiol 40:786–794. http://www.ncbi.nlm.nih.gov/pubmed/11401686 CrossRefPubMedCentralGoogle Scholar
  40. Cebrián J, Castán A, Martínez V, Kadomatsu-Hermosa MJ, Parra C, Fernández-Nestosa MJ, Schaerer C, Hernández P, Krimer DB, Schvartzman JB (2015) Direct Evidence for the Formation of Precatenanes during DNA Replication. J Biol Chem 290:13725–13735.  https://doi.org/10.1074/jbc.M115.642272. http://www.ncbi.nlm.nih.gov/pubmed/25829493, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC4447951, http://www.jbc.org/lookup/doi/10.1074/jbc.M115.642272 CrossRefPubMedCentralGoogle Scholar
  41. Bermejo R, Branzei D, Foiani M (2008) Cohesion by topology: sister chromatids interlocked by DNA. Genes Dev 22:2297–2301.  https://doi.org/10.1101/gad.1719308. http://www.ncbi.nlm.nih.gov/pubmed/18765785, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC2749673 CrossRefGoogle Scholar
  42. Joshi MC, Magnan D, Montminy TP, Lies M, Stepankiw N, Bates D (2013) Regulation of sister chromosome cohesion by the replication fork tracking protein SeqA. PLoS Genet 9:e1003673.  https://doi.org/10.1371/journal.pgen.1003673. http://www.ncbi.nlm.nih.gov/pubmed/23990792, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC3749930 CrossRefPubMedCentralGoogle Scholar
  43. Lesterlin C, Gigant E, Boccard F, Espéli O (2012) Sister chromatid interactions in bacteria revealed by a site-specific recombination assay. EMBO J 31:3468–3479.  https://doi.org/10.1038/emboj.2012.194. http://www.ncbi.nlm.nih.gov/pubmed/22820946, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC3419930, http://emboj.embopress.org/cgi/doi/10.1038/emboj.2012.194 CrossRefPubMedCentralGoogle Scholar
  44. Wang X, Reyes-Lamothe R, Sherratt DJ (2008) Modulation of Escherichia coli sister chromosome cohesion by topoisomerase IV. Genes Dev 22:2426–2433.  https://doi.org/10.1101/gad.487508. http://www.ncbi.nlm.nih.gov/pubmed/18765793, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC2532930 CrossRefGoogle Scholar
  45. Fossum-Raunehaug S, Helgesen E, Stokke C, Skarstad K (2014) Escherichia coli SeqA structures relocalize abruptly upon termination of origin sequestration during multifork DNA replication. PLoS One 9:e110575.  https://doi.org/10.1371/journal.pone.0110575. http://www.ncbi.nlm.nih.gov/pubmed/25333813, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC4204900 CrossRefPubMedCentralGoogle Scholar
  46. Helgesen E, Fossum-Raunehaug S, Sætre F, Schink KO, Skarstad K (2015) Dynamic Escherichia coli SeqA complexes organize the newly replicated DNA at a considerable distance from the replisome. Nucleic Acids Res 43:2730–2743.  https://doi.org/10.1093/nar/gkv146. http://academic.oup.com/nar/article/43/5/2730/2453293/Dynamic-Escherichia-coli-SeqA-complexes-organize, http://www.ncbi.nlm.nih.gov/pubmed/25722374, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC4357733 CrossRefPubMedCentralGoogle Scholar
  47. Ozaki S, Matsuda Y, Keyamura K, Kawakami H, Noguchi Y, Kasho K, Nagata K, Masuda T, Sakiyama Y, Katayama T (2013) A replicase clamp-binding dynamin-like protein promotes colocalization of nascent DNA strands and equipartitioning of chromosomes in E. coli. Cell Rep 4:985–995.  https://doi.org/10.1016/j.celrep.2013.07.040. http://linkinghub.elsevier.com/retrieve/pii/S2211124713004026, http://www.ncbi.nlm.nih.gov/pubmed/23994470 CrossRefPubMedCentralGoogle Scholar
  48. Wang X, Brando HB, Le TBK, Laub MT, Rudner DZ (2017) Bacillus subtilis smc complexes juxtapose chromosome arms as they travel from origin to terminus. Science 355:524–527CrossRefPubMedCentralGoogle Scholar
  49. Helgesen E, Fossum-Raunehaug S, Skarstad K (2016) Lack of the H-NS protein results in extended and aberrantly positioned DNA during chromosome replication and segregation in Escherichia coli. J Bacteriol 198:1305–16.  https://doi.org/10.1128/JB.00919-15. http://jb.asm.org/lookup/doi/10.1128/JB.00919-15, http://www.ncbi.nlm.nih.gov/pubmed/26858102, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC4859577 CrossRefPubMedCentralGoogle Scholar
  50. Wang X, Montero Llopis P, Rudner DZ (2013) Organization and segregation of bacterial chromosomes. Nat Rev Genet 14:191–203.  https://doi.org/10.1038/nrg3375. http://www.ncbi.nlm.nih.gov/pubmed/23400100, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC3869393 CrossRefPubMedCentralGoogle Scholar
  51. Youngren B, Nielsen HJ, Jun S, Austin S (2014) The multifork Escherichia coli chromosome is a self-duplicating and self-segregating thermodynamic ring polymer. Genes Dev 28:71–84.  https://doi.org/10.1101/gad.231050.113. http://www.ncbi.nlm.nih.gov/pubmed/24395248, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC3894414, http://genesdev.cshlp.org/cgi/doi/10.1101/gad.231050.113 CrossRefGoogle Scholar
  52. Liao Y, Li Y, Schroeder JW, Simmons LA, Biteen JS (2016) Single-Molecule DNA Polymerase Dynamics at a Bacterial Replisome in Live Cells. Biophys J 111:2562–2569.  https://doi.org/10.1016/j.bpj.2016.11.006. http://www.ncbi.nlm.nih.gov/pubmed/28002733, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC5192695linkinghub.elsevier.com/retrieve/pii/S0006349516310335 CrossRefPubMedCentralGoogle Scholar
  53. Beattie TR, Kapadia N, Nicolas E, Uphoff S, Wollman AJ, Leake MC, Reyes-Lamothe R (2017) Frequent exchange of the DNA polymerase during bacterial chromosome replication. eLife.  https://doi.org/10.7554/eLife.21763. http://www.ncbi.nlm.nih.gov/pubmed/28362256, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC5403216, http://elifesciences.org/lookup/doi/10.7554/eLife.21763
  54. Lewis JS, Spenkelink LM, Jergic S, Wood EA, Monachino E, Horan NP, Duderstadt KE, Cox MM, Robinson A, Dixon NE, van Oijen AM (2017) Single-molecule visualization of fast polymerase turnover in the bacterial replisome. eLife.  https://doi.org/10.7554/eLife.23932. http://www.ncbi.nlm.nih.gov/pubmed/28432790, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC5419744
  55. Redder P (2016) How does sub-cellular localization affect the fate of bacterial mRNA? Curr Genet 62:687–690.  https://doi.org/10.1007/s00294-016-0587-1. http://www.ncbi.nlm.nih.gov/pubmed/26972734, http://link.springer.com/10.1007/s00294-016-0587-1 CrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Sarah M. Mangiameli
    • 1
  • Julie A. Cass
    • 2
  • Houra Merrikh
    • 3
  • Paul A. Wiggins
    • 1
  1. 1.Department of PhysicsUniversity of WashingtonSeattleUSA
  2. 2.Department of BiologyUniversity of WashingtonSeattleUSA
  3. 3.Department of MicrobiologyHealth Sciences BuildingSeattleUSA

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