Abstract
Precise management of the spatiotemporal position of subcellular components is critical to a number of essential processes in the bacterial cell. The bacterial nucleoid is a highly structured yet dynamic object that undergoes significant reorganization during the relatively short cell cycle, e.g. during gene expression, chromosome replication, and segregation. Although the nucleoid takes up a large fraction of the volume of the cell, the mobility of macromolecules within these dense regions is relatively high and recent results suggest that the nucleoid plays an integral role of dynamic localization in a host of seemingly disparate cellular processes. Here, we review a number of recent reports of nucleoid-mediated positioning and transport in the model bacteria Escherichia coli. These results viewed as a whole suggest that the dynamic, cellular-scale structure of the nucleoid may be a key driver of positioning and transport within the cell. This model of a global, default positioning and transport system may help resolve many unanswered questions about the mechanisms of partitioning and segregation in bacteria.
Similar content being viewed by others
References
Adams DW, Errington J (2009) Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nat Rev Microbiol 7(9):642
Adler H, Fisher W, Cohen A, Hardigree AA (1967) Miniature Escherichia coli cells deficient in DNA. Proc Nat Acad Sci 57(2):321
Bailey MW, Bisicchia P, Warren BT, Sherratt DJ, Männik J (2014) Evidence for divisome localization mechanisms independent of the Min system and SlmA in Escherichia coli. PLOS Gen 10(8):e1004504
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(6):899–911
Bernhardt TG, de Boer PA (2005) SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over chromosomes in E. coli. Mol Cell 18(5):555–564
Bharat TA, Murshudov GN, Sachse C, Lӧwe J (2015) Structures of actin-like ParM filaments show architecture of plasmid-segregating spindles. Nature 523(7558):106
Bi E, Lutkenhaus J (1991) FtsZ ring structure associated with division in Escherichia coli. Nature 354(6349):161
Bisson-Filho AW, Hsu YP, Squyres GR, Kuru E, Wu F, Jukes C, Sun Y, Dekker C, Holden S, VanNieuwenhze MS, Brun YV (2017) Treadmilling by FtsZ filaments drives peptidoglycan synthesis and bacterial cell division. Science 355(6326):739–743
Bonny M, Fischer-Friedrich E, Loose M, Schwille P, Kruse K (2013) Membrane binding of MinE allows for a comprehensive description of Min-protein pattern formation. PLOS Comput Bio 9(12):e1003347
Brézellec P, Hoebeke M, Hiet MS, Pasek S, Ferat JL (2006) Domainsieve: a protein domain-based screen that led to the identification of dam-associated genes with potential link to DNA maintenance. Bioinformatics 22(16):1935–1941
Bryant JA, Sellars LE, Busby SJ, Lee DJ (2014) Chromosome position effects on gene expression in Escherichia coli K-12. Nucleic Acids Res 42(18):11383–11392
Campbell CS, Mullins RD (2007) In vivo visualization of type II plasmid segregation: bacterial actin filaments pushing plasmids. J Cell Biol 179(5):1059–1066
Cass JA, Kuwada NJ, Traxler B, Wiggins PA (2016) Escherichia coli chromosomal loci segregate from midcell with universal dynamics. Biophys J 110(12):2597–2609
Charbon G, Riber L, Løbner-Olesen A (2018) Countermeasures to survive excessive chromosome replication in Escherichia coli. Curr Genet 64(1):71–79
Cho H, McManus HR, Dove SL, Bernhardt TG (2011) Nucleoid occlusion factor SlmA is a DNA-activated FtsZ polymerization antagonist. Proc Nat Acad Sci 108(9):3773–3778
Cooper S, Helmstetter CE (1968) Chromosome replication and the division cycle of Escherichia coli. J Mol Biol 31(3):519–540
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(6):1485–1492
de Boer PA, Crossley RE, Rothfield LI (1989) A division inhibitor and a topological specificity factor coded for by the minicell locus determine proper placement of the division septum in E. coli. Cell 56(4):641–649
Donachie WD, Begg KJ (1989) Chromosome partition in Escherichia coli requires postreplication protein synthesis. J Bacteriol 171(10):5405–5409
Dupaigne P, Tonthat NK, Espéli O, Whitfill T, Boccard F, Schumacher MA (2012) Molecular basis for a protein-mediated DNA-bridging mechanism that functions in condensation of the E. coli chromosome. Mol Cell. 48(4):560–571
Ebersbach G, Gerdes K (2004) Bacterial mitosis: partitioning protein ParA oscillates in spiral-shaped structures and positions plasmids at mid-cell. Mol Micrbiol 52(2):385–398
Ebersbach G, Briegel A, Jensen GJ, Jacobs-Wagner C (2008) A self-associating protein critical for chromosome attachment, division, and polar organization in Caulobacter. Cell 134(6):956–968
Espéli O, Mercier R, Boccard F (2008) Dna dynamics vary according to macrodomain topography in the E. coli chromosome. Mol Microbiol 68(6):1418–1427
Espéli 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(14):3198–3211
Garner EC, Campbell CS, Weibel DB, Mullins RD (2007) Reconstitution of DNA segregation driven by assembly of a prokaryotic actin homolog. Science 315(5816):1270–1274
Gayathri P, Fujii T, Møller-Jensen J, van Den Ent F, Namba K, Lӧwe J (2012) A bipolar spindle of antiparallel ParM filaments drives bacterial plasmid segregation. Science 338(6112):1334–1337
Gerdes K, Møller-Jensen J, Jensen RB (2000) Plasmid and chromosome partitioning: surprises from phylogeny. Mol Microbiol 37(3):455–466
Gray WT, Govers SK, Xiang Y, Parry BR, Campos M, Kim S, Jacobs-Wagner C (2019) Nucleoid size scaling and intracellular organization of translation across bacteria. Cell 177(6):1632–1648
Hadizadeh Yazdi N, Guet CC, Johnson RC, Marko JF (2012) Variation of the folding and dynamics of the Escherichia coli chromosome with growth conditions. Mol Microbiol 86(6):1318–1333
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(5):2730–2743
Hiraga S, Niki H, Ogura T, Ichinose C, Mori H, Ezaki B, Jaffe A (1989) Chromosome partitioning in Escherichia coli: novel mutants producing anucleate cells. J Bacteriol 171(3):1496–1505
Hiraga S, Ogura T, Niki H, Ichinose C, Mori H (1990) Positioning of replicated chromosomes in Escherichia coli. J Bacteriol 172(1):31–39
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(5):327–341
Hirano T (2016) Condensin-based chromosome organization from bacteria to vertebr. Cell 164(5):847–857
Hofmann A, Mäkelä J, Sherratt DJ, Heermann D, Murray SM (2019) Self-organised segregation of bacterial chromosomal origins. elife 8:e46564
Hu Z, Mukherjee A, Pichoff S, Lutkenhaus J (1999) The MinC component of the division site selection system in Escherichia coli interacts with FtsZ to prevent polymerization. Proc Nat Acad Sci 96(26):14819–14824
Hu L, Vecchiarelli AG, Mizuuchi K, Neuman KC, Liu J (2015) Directed and persistent movement arises from mechanochemistry of the ParA/ParB system. Proc Nat Acad Sci 112(51):E7055–E7064
Jacob F, Brenner S, Cuzin F (1963) On the regulation of DNA replication in bacteria. Cold Spring Harbor Symp Quant Biol 28:329–348
Jensen RB, Gerdes K (1997) Partitioning of plasmid R1. The ParM protein exhibits ATPase activity and interacts with the centromere-like ParR-parC complex. J Mol Biol 269(4):505–513
Joshi MC, Bourniquel A, Fisher J, Ho BT, Magnan D, Kleckner N, Bates D (2011) Escherichia coli sister chromosome separation includes an abrupt global transition with concomitant release of late-splitting intersister snaps. Proc Nat Acad Sci 108(7):2765–2770
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(8):e1003673
Krogh TJ, Møller-Jensen JJ, Kaleta CC (2019) Impact of chromosomal architecture on the function and evolution of bacterial genomes. Front Microbiol 9:2019
Kuwada NJ, Cheveralls KC, Traxler B, Wiggins PA (2013) Mapping the driving forces of chromosome structure and segregation in Escherichia coli. Nucleic Acids Res 41(15):7370–7377
Kuwada NJ, Traxler B, Wiggins PA (2015) Genome-scale quantitative characterization of bacterial protein localization dynamics throughout the cell cycle. Mol Microbiol 95(1):64–79
Le Gall A, Cattoni DI, Guilhas B, Mathieu-Demaziere C, Oudjedi L, Fiche JB, Rech J, Abrahamsson S, Murray H, Bouet JY et al (2016) Bacterial partition complexes segregate within the volume of the nucleoid. Nat Commun 7:12107
Leighton RB, Sands ML (1965) The Feynman lectures on physics: mainly mechanics, radiation and heat. Addison-Wesley, Boston
Lim HC, Surovtsev IV, Beltran BG, Huang F, Bewersdorf J, Jacobs-Wagner C (2014) Evidence for a DNA-relay mechanism in ParABS-mediated chromosome segregation. eLife 3:e02758
Lioy VS, Cournac A, Marbouty M, Duigou S, Mozziconacci J, Espéli O, Boccard F, Koszul R (2018) Multiscale structuring of the E. coli chromosome by nucleoid-associated and condensin proteins. Cell 172(4):771–783
Llopis PM, Jackson AF, Sliusarenko O, Surovtsev I, Heinritz J, Emonet T, Jacobs-Wagner C (2010) Spatial organization of the flow of genetic information in bacteria. Nature 466(7302):77
Løbner-Olesen A, Skovgaard O, Marinus MG (2005) Dam methylation: coordinating cellular processes. Curr Opin Microbiol 8(2):154–160
Lu M, Campbell JL, Boye E, Kleckner N (1994) Seqa: a negative modulator of replication initiation in E. coli. Cell 77(3):413–426
Lutkenhaus J (2012) The ParA/MinD family puts things in their place. Trends Microbiol 20(9):411–418
Ma X, Ehrhardt DW, Margolin W (1996) Colocalization of cell division proteins FtsZ and FtsA to cytoskeletal structures in living Escherichia coli cells by using green fluorescent protein. Proc Nat Acad Sci 93(23):12998–13003
Mai J, Sokolov I, Blumen A (2001) Directed particle diffusion under “burnt bridges” conditions. Phys Rev E 64(1):011102
Mangiameli SM, Cass JA, Merrikh H, Wiggins PA (2018) The bacterial replisome has factory-like localization. Curr Genet 64(5):1029–1036
Männik J, Bailey MW (2015) Spatial coordination between chromosomes and cell division proteins in Escherichia coli. Front Microbiol 6:306
Melby T, Ciampaglio C, Briscoe G, Erickson H (1998) The symmetrical structure of structural maintenance of chromosomes (SMC) and MukB proteins: long antiparallel coiled coils, folded at a flexible hinge. J Cell Biol 142(6):1595–1604
Mercier R, Petit MA, Schbath S, Robin S, El Karoui M, Boccard F, Espéli O (2008) The MatP/matS site-specific system organizes the terminus region of the E. coli chromosome into a macrodomain. Cell 135(3):475–485
Meyer S, Reverchon S, Nasser W, Muskhelishvili G (2018) Chromosomal organization of transcription: in a nutshell. Curr Genet 64(3):555–565
Moffitt JR, Pandey S, Boettiger AN, Wang S, Zhuang X (2016) Spatial organization shapes the turnover of a bacterial transcriptome. elife 5:e13065
Mohl DA, Easter J Jr, Gober JW (2001) The chromosome partitioning protein, ParB, is required for cytokinesis in Caulobacter crescentus. Mol Microbiol 42(3):741–755
Møller-Jensen J, Jensen RB, Lӧwe J, Gerdes K (2002) Prokaryotic DNA segregation by an actin-like filament. EMBO J 21(12):3119–3127
Møller-Jensen J, Borch J, Dam M, Jensen RB, Roepstorff P, Gerdes K (2003) Bacterial mitosis: parM of plasmid R1 moves plasmid DNA by an actin-like insertional polymerization mechanism. Mol Cell 12(6):1477–1487
Murray SM, Sourjik V (2017) Self-organization and positioning of bacterial protein clusters. Nat Phys 13(10):1006
Nielsen HJ, Li Y, Youngren B, Hansen FG, Austin S (2006a) Progressive segregation of the Escherichia coli chromosome. Mol Microbiol 61(2):383–393
Nielsen HJ, Ottesen JR, Youngren B, Austin SJ, Hansen FG (2006b) The Escherichia coli chromosome is organized with the left and right chromosome arms in separate cell halves. Mol Microbiol 62(2):331–338
Niki H, Jaffe A, Imamura R, Ogura T, Hiraga S (1991) The new gene mukb codes for a 177 kd protein with coiled-coil domains involved in chromosome partitioning of E. coli. EMBO J 10(1):183–193
Niki H, Yamaichi Y, Hiraga S (2000) Dynamic organization of chromosomal DNA in Escherichia coli. Genes Dev 14(2):212–223
Nolivos S, Upton AL, Badrinarayanan A, Müller J, Zawadzka K, Wiktor J, Gill A, Arciszewska L, Nicolas E, Sherratt D (2016) Matp regulates the coordinated action of topoisomerase IV and MukBEF in chromosome segregation. Nat Commun 7:10466
Pedersen IB, Helgesen E, Flåtten I, Fossum-Raunehaug S, Skarstad K (2017) SeqA structures behind Escherichia coli replication forks affect replication elongation and restart mechanisms. Nucleic Acids Res 45(11):6471–6485
Pogliano J, Pogliano K, Weiss DS, Losick R, Beckwith J (1997) Inactivation of FtsI inhibits constriction of the FtsZ cytokinetic ring and delays the assembly of FtsZ rings at potential division sites. Proc Nat Acad Sci 94(2):559–564
Proenca AM, Rang CU, Buetz C, Shi C, Chao L (2018) Age structure landscapes emerge from the equilibrium between aging and rejuvenation in bacterial populations. Nat Commun 9(1):3722
Ptacin JL, Shapiro L (2013) Chromosome architecture is a key element of bacterial cellular organization. Cell Microbiol 15(1):45–52
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(8):791
Raskin DM, de Boer PA (1999) Rapid pole-to- pole oscillation of a protein required for directing division to the middle of Escherichia coli. Proc Nat Acad Sci 96(9):4971–4976
Reyes-Lamothe R, Wang X, Sherratt D (2008a) Escherichia coli and its chromosome. Trends Microbiol 16(5):238–245
Reyes-Lamothe R, Possoz C, Danilova O, Sherratt DJ (2008b) Independent positioning and action of Escherichia coli replisomes in live cells. Cell 133(1):90–102
Rothfield L, Tagh-Balout A, Shih YL (2005) Spatial control of bacterial division-site placement. Nat Rev Microbiol 3(12):959
Shaevitz JW, Gitai Z (2010) The structure and function of bacterial actin homologs. Cold Spring Harbor Perspect Biol 2(9):a000364
Shebelut CW, Guberman JM, Van Teeffelen S, Yakhnina AA, Gitai Z (2010) Caulobacter chromosome segregation is an ordered multistep process. Proc Nat Acad Sci 107(32):14194–14198
Sinha AK, Possoz C, Durand A, Desfontaines JM, Barre FX, Leach DR, Michel B (2018) Broken replication forks trigger heritable DNA breaks in the terminus of a circular chromosome. PLoS Genet 14(3):e1007256
Slater S, Wold S, Lu M, Boye E, Skarstad K, Kleckner N (1995) E. coli SeqA protein binds oriC in two different methyl-modulated reactions appropriate to its roles in DNA replication initiation and origin sequestration. Cell 82(6):927–936
Smoluchowski M (1912) Experimental proof of regular thermodynamic conflicting molecular phenomenons. Phys Z 13:1069–1080
Soppa J (2001) Prokaryotic structural maintenance of chromosomes (SMC) proteins: distribution, phylogeny, and comparison with MukBs and additional prokaryotic and eukaryotic coiled-coil proteins. Gene 278(1–2):253–264
Stewart EJ, Madden R, Paul G, Taddei F (2005) Aging and death in an organism that reproduces by morphologically symmetric division. PLoS Biol 3(2):e45
Stouf M, Meile JC, Cornet F (2013) FtsK actively segregates sister chromosomes in Escherichia coli. Proc Nat Acad Sci. 110(27):11157–11162
Stracy M, Lesterlin C, De Leon FG, Uphoff S, Zawadzki P, Kapanidis AN (2015) Live-cell superresolution microscopy reveals the organization of RNA polymerase in the bacterial nucleoid. Proc Nat Acad Sci 112(32):E4390–E4399
Stylianidou S, Kuwada NJ, Wiggins PA (2014) Cytoplasmic dynamics reveals two modes of nucleoid-dependent mobility. Biophys J 107(11):2684–2692
Sugawara T, Kaneko K (2011) Chemophoresis as a driving force for intracellular organization: theory and application to plasmid partitioning. Biophysics 7:77–88
Surovtsev IV, Jacobs-Wagner C (2018) Subcellular organization: a critical feature of bacterial cell replication. Cell 172(6):1271–1293
Surovtsev IV, Campos M, Jacobs-Wagner C (2016) DNA-relay mechanism is sufficient to explain ParA-dependent intracellular transport and patterning of single and multiple cargos. Proc Nat Acad Sci 113(46):E7268–E7276
Thiel A, Valens M, Vallet-Gely I, Espéli O, Boccard F (2012) Long-range chromosome organization in E. coli: a site-specific system isolates the Ter macrodomain. PLoS Gen 8(4):e1002672
Trueba FJ (1982) On the precision and accuracy achieved by Escherichia coli cells at fission about their middle. Arch Microbiol 131(1):55–59
Valens M, Penaud S, Rossignol M, Cornet F, Boccard F (2004) Macrodomain organization of the Escherichia coli chromosome. EMBO J 23(21):4330–4341
Valens M, Thiel A, Boccard F (2016) The MaoP/maoS site-specific system organizes the Ori region of the E. coli chromosome into a macrodomain. PLOS Genet 12(9):e1006309
Vecchiarelli AG, Mizuuchi K, Funnell BE (2012) Surfing biological surfaces: exploiting the nucleoid for partition and transport in bacteria. Mol Microbiol 86(3):513–523
Vecchiarelli AG, Hwang LC, Mizuuchi K (2013) Cell-free study of F plasmid partition provides evidence for cargo transport by a diffusion-ratchet mechanism. Proc Nat Acad Sci 110(15):E1390–E1397
Vecchiarelli AG, Neuman KC, Mizuuchi K (2014) A propagating ATPase gradient drives transport of surface-confined cellular cargo. Proc Nat Acad Sci 111(13):4880–4885
Vecchiarelli AG, Li M, Mizuuchi M, Hwang LC, Seol Y, Neuman KC, Mizuuchi K (2016) Membrane-bound MinDE complex acts as a toggle switch that drives Min oscillation coupled to cytoplasmic depletion of MinD. Proc Nat Acad Sci 113(11):E1479–E1488
Volkmer B, Heinemann M (2011) Condition-dependent cell volume and concentration of Escherichia coli to facilitate data conversion for systems biology modeling. PLoS One 6(7):e23126
Waldminghaus T, Skarstad K (2009) The Escherichia coli SeqA protein. Plasmid 61(3):141–150
Wang X, Liu X, Possoz C, Sherratt DJ (2006) The two Escherichia coli chromosome arms locate to separate cell halves. Genes Dev 20(13):1727–1731
Wang X, Lesterlin C, Reyes-Lamothe R, Ball G, Sherratt DJ (2011) Replication and segregation of an Escherichia coli chromosome with two replication origins. Proc Nat Acad Sci 108(26):E243–E250
Weitao T, Nordstrӧm K, Dasgupta S (1999) Mutual suppression of mukB and seqA phenotypes might arise from their opposing influences on the Escherichia coli nucleoid structure. Mol Microbiol 34(1):157–168
White MA, Eykelenboom JK, Lopez-Vernaza MA, Wilson E, Leach DR (2008) Non-random segregation of sister chromosomes in Escherichia coli. Nature 455(7217):1248
Wiggins PA, Cheveralls KC, Martin JS, Lintner R, Kondev J (2010) Strong intranucleoid interactions organize the Escherichia coli chromosome into a nucleoid filament. Proc Nat Acad Sci 107(11):4991–4995
Woldringh C, Huls P, Pas E, Brakenhoff G, Nanninga N (1987) Topography of peptidoglycan synthesis during elongation and polar cap formation in a cell division mutant of Escherichia coli MC4100. Microbiology 133(3):575–586
Woldringh C, Mulder E, Huls P, Vischer N (1991) Toporegulation of bacterial division according to nucleoid occlusion model. Res Microbiol 142(2–3):309–320
Wu F, Japaridze A, Zheng X, Wiktor J, Kerssemakers JW, Dekker C (2019a) Direct imaging of the circular chromosome in a live bacterium. Nat Commun 10(1):2194
Wu F, Swain P, Kuijpers L, Zheng X, Felter K, Guurink M, Solari J, Jun S, Shimizu TS, Chaudhuri D, Mulder B (2019b) Cell boundary confinement sets the size and position of the E. coli chromosome. Curr Biol 29:2131–2144
Yang X, Lyu Z, Miguel A, McQuillen R, Huang KC, Xiao J (2017) GTPase activity-coupled treadmilling of the bacterial tubulin FtsZ organizes septal cell wall synthesis. Science 355(6326):744–747
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(1):71–84
Yu XC, Margolin W (1999) FtsZ ring clusters in min and partition mutants: role of both the Min system and the nucleoid in regulating FtsZ ring localization. Mol Microbiol 32(2):315–326
Acknowledgements
Special thanks to Austin Lott for early assistance in tracking down references. This work was supported by the Central Washington University College of the Sciences Faculty Early Career Grant.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M. Kupiec.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Kisner, J.R., Kuwada, N.J. Nucleoid-mediated positioning and transport in bacteria. Curr Genet 66, 279–291 (2020). https://doi.org/10.1007/s00294-019-01041-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00294-019-01041-2