Cited by 74Bacterial Genetics and BiotechnologyMicrotubule and mitosis dynamicsGenomics and Chromatin Dynamics

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Chromosome segregation by the Escherichia coli Min system

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Abstract

The mechanisms underlying chromosome segregation in prokaryotes remain a subject of debate and no unifying view has yet emerged. Given that the initial disentanglement of duplicated chromosomes could be achieved by purely entropic forces, even the requirement of an active prokaryotic segregation machinery has been questioned. Using computer simulations, we show that entropic forces alone are not sufficient to achieve and maintain full separation of chromosomes. This is, however, possible by assuming repeated binding of chromosomes along a gradient of membrane-associated tethering sites toward the poles. We propose that, in Escherichia coli, such a gradient of membrane tethering sites may be provided by the oscillatory Min system, otherwise known for its role in selecting the cell division site. Consistent with this hypothesis, we demonstrate that MinD binds to DNA and tethers it to the membrane in an ATP-dependent manner. Taken together, our combined theoretical and experimental results suggest the existence of a novel mechanism of chromosome segregation based on the Min system, further highlighting the importance of active segregation of chromosomes in prokaryotic cell biology.

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Crossref · 10.1038/msb.2013.44

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  • The Min system aids in chromosome partitioning through MinD mediated transient DNA-membrane tethering events.

    “and the Min system aids in chromosome partitioning through MinD mediated transient DNA-membrane tethering events,56”

    From Bringing the genetically minimal cell to life on a computer in 4D (2026) · cites this paper as [56]

    The Results section reports ATP-dependent recruitment of DNA to membrane-like liposomes by MinD, and the Discussion describes an alternating ‘catch-and-release’ mechanism. But the paper proposes that this mechanism aids chromosome segregation in E. coli; it does not establish that the transient tethering events do so in cells. No page numbers were provided in our copy. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

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Research works printed but not linked: 54

  1. Akerlund T, Bernander R, Nordstrom K (1992) Cell division in Escherichia coli minB mutants. Mol Microbiol 6: 2073–2083 · DOI
  2. Akerlund T, Gullbrand B, Nordstrom K (2002) Effects of the Min system on nucleoid segregation in Escherichia coli. Microbiology 148: 3213–3222 · DOI
  3. Arnold A, Jun S (2007) Time scale of entropic segregation of flexible polymers in confinement: implications for chromosome segregation in filamentous bacteria. Phys Rev E, Stat Nonlin Soft Matter Phys 76: 031901 · DOI
  4. Badrinarayanan A, Reyes‐Lamothe R, Uphoff S, Leake MC, Sherratt DJ (2012) In vivo architecture and action of bacterial structural maintenance of chromosome proteins. Science 338: 528–531 · DOI
  5. Binder K, Heermann DW (2002) Monte Carlo Simulation in Statistical Physics: An Introduction. Springer‐Verlag , Berlin, Heidelberg, New York · DOI
  6. Bohn M, Heermann DW (2010) Topological interactions between ring polymers: Implications for chromatin loops. J Chem Phys 132: 044904 · DOI
  7. Bohn M, Heermann DW (2011) Repulsive forces between looping chromosomes induce entropy‐driven segregation. PLoS One 6: e14428 · DOI
  8. Castaing JP, Bouet JY, Lane D (2008) F plasmid partition depends on interaction of SopA with non‐specific DNA. Mol Microbiol 70: 1000–1011 · DOI
  9. Danilova O, Reyes‐Lamothe R, Pinskaya M, Sherratt D, Possoz C (2007) MukB colocalizes with the oriC region and is required for organization of the two Escherichia coli chromosome arms into separate cell halves. Mol Microbiol 65: 1485–1492 · DOI
  10. de Boer PA (2010) Advances in understanding E. coli cell fission. Curr Opin Microbiol 13: 730–737 · DOI
  11. Erickson HP, Anderson DE, Osawa M (2010) FtsZ in bacterial cytokinesis: cytoskeleton and force generator all in one. Microbiol Mol Biol Rev 74: 504–528 · DOI
  12. Espeli O, Borne R, Dupaigne P, Thiel A, Gigant E, Mercier R, Boccard F (2012) A MatP‐divisome interaction coordinates chromosome segregation with cell division in E. coli. EMBO J 31: 3198–3211 · DOI
  13. Fisher JK, Bourniquel A, Witz G, Weiner B, Prentiss M, Kleckner N (2013) Four‐dimensional imaging of E. coli nucleoid organization and dynamics in living cells. Cell 153: 882–895 · DOI
  14. Fogel MA, Waldor MK (2006) A dynamic, mitotic‐like mechanism for bacterial chromosome segregation. Genes Dev 20: 3269–3282 · DOI
  15. Fritsche M, Li S, Heermann DW, Wiggins PA (2012) A model for Escherichia coli chromosome packaging supports transcription factor‐induced DNA domain formation. Nucleic Acids Res 40: 972–980 · DOI
  16. Gerdes K, Howard M, Szardenings F (2010) Pushing and pulling in prokaryotic DNA segregation. Cell 141: 927–942 · DOI
  17. Grainge I, Bregu M, Vazquez M, Sivanathan V, Ip SC, Sherratt DJ (2007) Unlinking chromosome catenanes in vivo by site‐specific recombination. EMBO J 26: 4228–4238 · DOI
  18. Hayes F, Barilla D (2006) The bacterial segrosome: a dynamic nucleoprotein machine for DNA trafficking and segregation. Nat Rev Microbiol 4: 133–143 · DOI
  19. Hester CM, Lutkenhaus J (2007) Soj (ParA) DNA binding is mediated by conserved arginines and is essential for plasmid segregation. Proc Natl Acad Sci USA 104: 20326–20331 · DOI
  20. Hu Z, Gogol EP, Lutkenhaus J (2002) Dynamic assembly of MinD on phospholipid vesicles regulated by ATP and MinE. Proc Natl Acad Sci USA 99: 6761–6766 · DOI
  21. Hu Z, Lutkenhaus J (2003) A conserved sequence at the C‐terminus of MinD is required for binding to the membrane and targeting MinC to the septum. Mol Microbiol 47: 345–355 · DOI
  22. Jun S, Mulder B (2006) Entropy‐driven spatial organization of highly confined polymers: lessons for the bacterial chromosome. Proc Natl Acad Sci USA 103: 12388–12393 · DOI
  23. Jun S, Wright A (2010) Entropy as the driver of chromosome segregation. Nat Rev Microbiol 8: 600–607 · DOI
  24. Kruse K, Howard M, Margolin W (2007) An experimentalist's guide to computational modelling of the Min system. Mol Microbiol 63: 1279–1284 · DOI
  25. Lackner LL, Raskin DM, de Boer PA (2003) ATP‐dependent interactions between Escherichia coli Min proteins and the phospholipid membrane in vitro. J Bacteriol 185: 735–749 · DOI
  26. Loose M, Fischer‐Friedrich E, Ries J, Kruse K, Schwille P (2008) Spatial regulators for bacterial cell division self‐organize into surface waves in vitro. Science 320: 789–792 · DOI
  27. Lutkenhaus J (2007) Assembly dynamics of the bacterial MinCDE system and spatial regulation of the Z ring. Annu Rev Biochem 76: 539–562 · DOI
  28. Lutkenhaus J (2012) The ParA/MinD family puts things in their place. Trends Microbiol 20: 411–418 · DOI
  29. Madabhushi R, Marians KJ (2009) Actin homolog MreB affects chromosome segregation by regulating topoisomerase IV in Escherichia coli. Mol Cell 33: 171–180 · DOI
  30. Marston AL, Thomaides HB, Edwards DH, Sharpe ME, Errington J (1998) Polar localization of the MinD protein of Bacillus subtilis and its role in selection of the mid‐cell division site. Genes Dev 12: 3419–3430 · DOI
  31. Okuno T, Ohgita T, Sasa T, Nonaka A, Funasaki N, Kogure K (2010) Fluorescence polarization analysis for revealing molecular mechanism of nucleotide‐dependent phospholipid membrane binding of MinD adenosine 5′‐triphosphate, adenosine triphosphatase. Biol Pharm Bull 33: 1746–1750 · DOI
  32. Pogliano K, Pogliano J, Becker E (2003) Chromosome segregation in Eubacteria. Curr Opin Microbiol 6: 586–593 · DOI
  33. Possoz C, Filipe SR, Grainge I, Sherratt DJ (2006) Tracking of controlled Escherichia coli replication fork stalling and restart at repressor‐bound DNA in vivo. EMBO J 25: 2596–2604 · DOI
  34. Ptacin JL, Lee SF, Garner EC, Toro E, Eckart M, Comolli LR, Moerner WE, Shapiro L (2010) A spindle‐like apparatus guides bacterial chromosome segregation. Nat Cell Biol 12: 791–798 · DOI
  35. Raskin DM, de Boer PA (1999) MinDE‐dependent pole‐to‐pole oscillation of division inhibitor MinC in Escherichia coli. J Bacteriol 181: 6419–6424 · DOI
  36. Reyes‐Lamothe R, Nicolas E, Sherratt DJ (2012) Chromosome replication and segregation in bacteria. Annu Rev Genet 46: 121–143 · DOI
  37. Ringgaard S, van Zon J, Howard M, Gerdes K (2009) Movement and equipositioning of plasmids by ParA filament disassembly. Proc Natl Acad Sci USA 106: 19369–19374 · DOI
  38. Sawitzke J, Austin S (2001) An analysis of the factory model for chromosome replication and segregation in bacteria. Mol Microbiol 40: 786–794 · DOI
  39. Schofield WB, Lim HC, Jacobs‐Wagner C (2010) Cell cycle coordination and regulation of bacterial chromosome segregation dynamics by polarly localized proteins. EMBO J 29: 3068–3081 · DOI
  40. Scholefield G, Veening JW, Murray H (2011) DnaA and ORC: more than DNA replication initiators. Trends Cell Biol 21: 188–194 · DOI
  41. Shebelut CW, Guberman JM, van Teeffelen S, Yakhnina AA, Gitai Z (2010) Caulobacter chromosome segregation is an ordered multistep process. Proc Natl Acad Sci USA 107: 14194–14198 · DOI
  42. Steringer JP, Bleicken S, Andreas H, Zacherl S, Laussmann M, Temmerman K, Contreras FX, Bharat TA, Lechner J, Muller HM, Briggs JA, Garcia‐Saez AJ, Nickel W (2012) Phosphatidylinositol 4,5‐bisphosphate (PI(4,5)P2)‐dependent oligomerization of fibroblast growth factor 2 (FGF2) triggers the formation of a lipidic membrane pore implicated in unconventional secretion. J Biol Chem 287: 27659–27669 · DOI
  43. Szeto TH, Rowland SL, Habrukowich CL, King GF (2003) The MinD membrane targeting sequence is a transplantable lipid‐binding helix. J Biol Chem 278: 40050–40056 · DOI
  44. Szeto TH, Rowland SL, Rothfield LI, King GF (2002) Membrane localization of MinD is mediated by a C‐terminal motif that is conserved across eubacteria, archaea, and chloroplasts. Proc Natl Acad Sci USA 99: 15693–15698 · DOI
  45. Thanbichler M, Shapiro L (2008) Getting organized‐‐how bacterial cells move proteins and DNA. Nat Rev Microbiol 6: 28–40 · DOI
  46. Toro E, Shapiro L (2010) Bacterial chromosome organization and segregation. Cold Spring Harb Perspect Biol 2: a000349 · DOI
  47. Wang X, Liu X, Possoz C, Sherratt DJ (2006) The two Escherichia coli chromosome arms locate to separate cell halves. Genes Dev 20: 1727–1731 · DOI
  48. Wang X, Sherratt DJ (2010) Independent segregation of the two arms of the Escherichia coli ori region requires neither RNA synthesis nor MreB dynamics. J Bacteriol 192: 6143–6153 · DOI
  49. Weber T, Zemelman BV, McNew JA, Westermann B, Gmachl M, Parlati F, Sollner TH, Rothman JE (1998) SNAREpins: minimal machinery for membrane fusion. Cell 92: 759–772 · DOI
  50. White MA, Eykelenboom JK, Lopez‐Vernaza MA, Wilson E, Leach DR (2008) Non‐random segregation of sister chromosomes in Escherichia coli. Nature 455: 1248–1250 · DOI
  51. Woldringh CL (2002) The role of co‐transcriptional translation and protein translocation (transertion) in bacterial chromosome segregation. Mol Microbiol 45: 17–29 · DOI
  52. Wu W, Park KT, Holyoak T, Lutkenhaus J (2011) Determination of the structure of the MinD‐ATP complex reveals the orientation of MinD on the membrane and the relative location of the binding sites for MinE and MinC. Mol Microbiol 79: 1515–1528 · DOI
  53. Zhou H, Lutkenhaus J (2003) Membrane binding by MinD involves insertion of hydrophobic residues within the C‐terminal amphipathic helix into the bilayer. J Bacteriol 185: 4326–4335 · DOI
  54. Zhou H, Schulze R, Cox S, Saez C, Hu Z, Lutkenhaus J (2005) Analysis of MinD mutations reveals residues required for MinE stimulation of the MinD ATPase and residues required for MinC interaction. J Bacteriol 187: 629–638 · DOI

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Metadata

Authors
Di Ventura, B., Knecht, B., Andreas, H., Godinez, W. J., Fritsche, M., Rohr, K., Nickel, W., Heermann, D. W., & Sourjik, V.
Affiliations
  • Heidelberg University (DE)
  • German Cancer Research Center (DE)
Corresponding author
Sourjik, Victor
Venue
Molecular Systems Biology
Published
2013-09-10
Volume
9
Issue
1
Pages
686-686
ISSN
1744-4292 (ISSN-L)
OpenAlex
W2025055246
Cited by
74
References
1
Citations by year
2026: 1 · 2025: 4 · 2024: 3 · 2023: 3 · 2022: 5 · 2021: 5 · 2020: 6 · 2019: 7 · 2018: 6 · 2017: 3 · 2016: 6 · 2015: 11 · 2014: 12 · 2013: 2
FWCI
6.86
Type
journal article
Language
en
Open access
Locations
  • Molecular Systems Biology (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
  • CHS Stiftung
  • Deutsche Forschungsgemeinschaft (TRR 83)
  • Bundesministerium für Bildung und Forschung
  • Heidelberg Graduate School of Mathematical and Computational Methods for the Sciences, University of Heidelberg
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Keywords
chromosome segregation, Escherichia coli, Min system, mind, entropic force, cell division site selection, DNA binding, ATP-dependent DNA binding
MeSH terms
Adenosine Triphosphatases, Adenosine Triphosphate, Cell Division, Cell Membrane, Chromosomes, Bacterial, Computer Simulation, DNA, Bacterial, Escherichia coli, Models, Molecular, Thermodynamics, Gene Expression Regulation, Bacterial, Cell Cycle Proteins, Chromosome Segregation, Escherichia coli Proteins

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