Abstract
The Escherichia coli SMC complex, MukBEF, forms clusters of molecules that interact with the decatenase topisomerase IV and which are normally associated with the chromosome replication origin region (ori). Here we demonstrate an additional ATP-hydrolysis-dependent association of MukBEF with the replication termination region (ter). Consistent with this, MukBEF interacts with MatP, which binds matS sites in ter. MatP displaces wild-type MukBEF complexes from ter, thereby facilitating their association with ori, and limiting the availability of topoisomerase IV (TopoIV) at ter. Displacement of MukBEF is impaired when MukB ATP hydrolysis is compromised and when MatP is absent, leading to a stable association of ter and MukBEF. Impairing the TopoIV-MukBEF interaction delays sister ter segregation in cells lacking MatP. We propose that the interplay between MukBEF and MatP directs chromosome organization in relation to MukBEF clusters and associated topisomerase IV, thereby ensuring timely chromosome unlinking and segregation.
Highlights
The Escherichia coli structural maintenance of chromosomes (SMC) complex, MukBEF, forms clusters of molecules that interact with the decatenase topisomerase IV and which are normally associated with the chromosome replication origin region
We propose that the interplay between MukBEF and MatP directs the positioning of the chromosome with respect to MukBEF clusters and their associated topoisomerase IV (TopoIV), thereby ensuring normal chromosome organization, and timely unlinking and segregation
By using an interdisciplinary approach, we have revealed how MatP regulates the position and action of E. coli TopoIV and MukBEF, complexes that play sequential roles in chromosome unlinking and segregation
Summary
The Escherichia coli SMC complex, MukBEF, forms clusters of molecules that interact with the decatenase topisomerase IV and which are normally associated with the chromosome replication origin region (ori). Functional fluorescent derivatives of MukBEF form foci that are normally associated with the replication origin region (ori) of the E. coli chromosome, and which have been proposed to position oris before and after their replication, as well as recruiting TopoIV4,11,12 These foci contain on average eight dimers of dimer MukBEF complexes, hereafter termed MukBEF clusters, which adopt an ellipsoidal shape, with a mean diameter of B400 nm, irrespective of whether MukB, MukE or MukF was labelled[13]. Cells lacking MatP show a stable association of both ori and ter with positioned MukBEF clusters, consistent with MatP directing the displacement of wild-type MukBEF complexes from ter This dispacement, which is impaired when MukB ATP hydrolysis is compromised, thereby facilitates MukBEF cluster association with ori. We propose that the interplay between MukBEF and MatP directs the positioning of the chromosome with respect to MukBEF clusters and their associated TopoIV, thereby ensuring normal chromosome organization, and timely unlinking and segregation
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