Organization of the Escherichia coli Chromosome by a MukBEF Axial Core

Mäkelä, Jarno; Sherratt, David J.

doi:10.1016/j.molcel.2020.02.003

Cited by 92 publications

(117 citation statements)

References 66 publications

(129 reference statements)

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“…Interestingly, in the absence of FIS, H-NS is capable of polymerising on the tightly bent loop connecting the bridged helices ( Fig.4d, Supplementary Fig.8), meaning that FIS hinders the spread of H-NS. Notably, recent studies demonstrated that the physiological B-form DNA can undergo structural changes resulting in non-canonical DNA forms under the influence of DNA supercoiling (61), spatial confinement (62) and DNA sequence (63,64), indicating that the DNA structure itself is highly heterogeneous.…”

Section: Discussionmentioning

confidence: 99%

DNA sequence-directed cooperation between nucleoid-associated proteins

Japaridze

Yang

Dekker

et al. 2020

Preprint

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Nucleoid associated proteins (NAPs) are a class of highly abundant DNA binding proteins in bacteria and archaea. While the composition and relative abundance of the NAPs change during the bacterial growth cycle, surprisingly little is known about their crosstalk in mutually binding to the bacterial chromosome and stabilising higher-order nucleoprotein complexes. Here, we use atomic force microscopy and solid-state nanopores to investigate longrange nucleoprotein structures formed by the binding of two major NAPs, FIS and H-NS, to DNA molecules with distinct binding-site arrangements. We find that spatial organisation of the protein binding sites can govern the higher-order architecture of the nucleoprotein complexes. Based on sequence arrangement the complexes differed in their global shape and compaction, as well as the extent of FIS and H-NS binding. Our observations highlight the important role the DNA sequence plays in driving structural differentiations within the bacterial chromosome.

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Section: Discussionmentioning

confidence: 99%

DNA sequence-directed cooperation between nucleoid-associated proteins

Japaridze

Yang

Dekker

et al. 2020

Preprint

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“…MukBEF complexes form axial cores that linearly organize the chromosome outside the 800 kb ter region, from where MatP bound to matS sites displaces MukBEF ( Fig. 2A) (Mäkelä and Sherratt, 2020). Complete axial cores were most easily visualized in cells in which MukBEF occupancy on the chromosome was increased ~3.5-fold, while cells with WT MukBEF abundance on chromosomes exhibited more granular structures (Mäkelä and Sherratt, 2020).…”

Section: Mukbef and Matp Direct Left-oric-right Chromosome Organizationmentioning

confidence: 99%

“…2A) (Mäkelä and Sherratt, 2020). Complete axial cores were most easily visualized in cells in which MukBEF occupancy on the chromosome was increased ~3.5-fold, while cells with WT MukBEF abundance on chromosomes exhibited more granular structures (Mäkelä and Sherratt, 2020). To characterize how MukBEF axial cores influence chromosome organization during the cell cycle, we used strains that allowed us to test the requirements for left and right chromosome arm organization in relation to oriC and ter in MatP + and ΔmatP cells with WT levels of MukBEF, and in ΔmukB cells (Fig.…”

Section: Mukbef and Matp Direct Left-oric-right Chromosome Organizationmentioning

confidence: 99%

“…Consistent with this, it has been proposed that large bacterial chromosomes can utilise repelling entropic effects to facilitate separation of bacterial chromosomes (Jun and Mulder, 2006), unlike much smaller low copy number plasmids that require a functional ParABS system for faithful segregation (Surovtsev and Jacobs-Wagner, 2018). Whatever roles entropic forces may play, studies in diverse bacterial species have demonstrated that chromosomal loci are not positioned randomly in cells (Fogel and Waldor, 2005;Umbarger et al, 2011;Vallet-Gely and Boccard, 2013;Wang et al, 2005Wang et al, , 2006Wang et al, , 2014, and that in E. coli, MukBEF complexes play an important role in correct positioning of replication origins and other loci by forming an axial core to the chromosome (Danilova et al, 2007;Mäkelä and Sherratt, 2020). Absence of MukBEF leads to formation of anucleate cells during growth and loss of viability at temperatures higher than 22 °C in rich media (Danilova et al, 2007;Niki and Jaffe, 1991).…”

Section: Introductionmentioning

confidence: 99%

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Non-random segregation of sister chromosomes by Escherichia coli MukBEF axial cores

Mäkelä

Uphoff

Sherratt

2020

Preprint

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SummaryThe Escherichia coli structural maintenance of chromosomes complex, MukBEF, forms axial cores to chromosomes that determine their spatio-temporal organization. Here, we show that axial cores direct chromosome arms to opposite poles and generate the translational symmetry between newly replicated sister chromosomes. MatP, a replication terminus (ter) binding protein, prevents chromosome rotation in the longitudinal cell axis by displacing MukBEF from ter, thereby maintaining the linear shape of axial cores. During DNA replication, MukBEF-MatP action directs lagging strands towards the cell center, marked by accumulation of DNA-bound β2-clamps in the wake of the replisome, in a process necessary for translational symmetry. Finally, the ancestral template DNA strand, propagated from previous generations, is preferentially inherited by the cell forming at the old pole, dependent on MukBEF-MatP. The work demonstrates how chromosome organization-segregation fosters non-random inheritance of genetic material and provides a framework for understanding how chromosome conformation and dynamics shape subcellular organization.HighlightsLinear MukBEF axial cores are required for left-oriC-right chromosome organizationMatP prevents longitudinal nucleoid rotation by linearizing the axial coresMukBEF axial cores direct lagging strands towards the cell centerThe ancestral DNA strand is preferentially segregated to the older pole cell

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“…Recently, using Chromosome Conformation Capture, we showed that MukBEF does not align E. coli chromosome arms but instead gives rise to long-range cis-contacts within replication arms. These contacts are absent in the 800-kb long Ter region, where MatP (the factor responsible for Ter structuring (Mercier et al, 2008)) prevents MukBEF activity (Lioy et al, 2018;Mäkelä and Sherratt, 2020;Nolivos et al, 2016). Interestingly, MukBEF and MatP both belong to a group of proteins that coevolved with the Dam methylase (Brézellec et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

Distinct activities of bacterial condensins for chromosome management in Pseudomonas aeruginosa

Lioy

Junier

Lagage

et al. 2020

Preprint

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Bacteria encompass three types of structurally related SMC complexes referred to as condensins. Smc-ScpAB is present in most bacteria while MukBEF is found in enterobacteria and MksBEF is scattered over the phylogenic tree. The contributions of these condensins to chromosome management were characterized in Pseudomonas aeruginosa that carries both Smc-ScpAB and MksBEF. In this bacterium, SMC-ScpAB controls chromosome disposition by juxtaposing chromosome arms. In contrast, MksBEF is critical for chromosome segregation in the absence of the main segregation system and affects the higher-order architecture of the chromosome by promoting DNA contacts in the megabase range.Strikingly, our results reveal a prevalence of Smc-ScpAB over MksBEF involving a coordination of their activities with the DNA replication process. They also show that E. coli MukBEF can substitute for MksBEF in P. aeruginosa while prevailing over Smc-ScpAB. Altogether, our results reveal a hierarchy between activities of bacterial condensins on the same chromosome.

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Organization of the Escherichia coli Chromosome by a MukBEF Axial Core

Abstract: Highlightsd MukBEF forms a chromosome axial core dependent on ATP hydrolysis d MukBEF compacts the chromosome lengthwise while avoiding links between replichores

Cited by 92 publications

References 66 publications

DNA sequence-directed cooperation between nucleoid-associated proteins

DNA sequence-directed cooperation between nucleoid-associated proteins

Non-random segregation of sister chromosomes by Escherichia coli MukBEF axial cores

Distinct activities of bacterial condensins for chromosome management in Pseudomonas aeruginosa

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