Abstract
Structural Maintenance of Chromosomes (SMC) complexes have ubiquitous roles in compacting DNA linearly, thereby promoting chromosome organization-segregation. Interaction between the Escherichia coli SMC complex, MukBEF, and matS-bound MatP in the chromosome replication termination region, ter, results in depletion of MukBEF from ter, a process essential for efficient daughter chromosome individualization and for preferential association of MukBEF with the replication origin region. Chromosome-associated MukBEF complexes also interact with topoisomerase IV (ParC2E2), so that their chromosome distribution mirrors that of MukBEF. We demonstrate that MatP and ParC have an overlapping binding interface on the MukB hinge, leading to their mutually exclusive binding, which occurs with the same dimer to dimer stoichiometry. Furthermore, we show that matS DNA competes with the MukB hinge for MatP binding. Cells expressing MukBEF complexes that are mutated at the ParC/MatP binding interface are impaired in ParC binding and have a mild defect in MukBEF function. These data highlight competitive binding as a means of globally regulating MukBEF-topoisomerase IV activity in space and time.
Highlights
Structural Maintenance of Chromosomes (SMC) complexes play central roles in chromosome organization and segregation in all domains of life
The Escherichia coli SMC complex, MukBEF, is required for normal chromosome dynamics and its absence leads to temperature-sensitive growth in rich medium, under conditions of overlapping replication cycles, and anucleate cell formation during permissive growth [1, 2]
We propose that combined topoisomerase IV (topoIV) and MukBEF action may help coordinate chromosome unlinking with establishing the organization of newly replicated sister chromosomes
Summary
Structural Maintenance of Chromosomes (SMC) complexes play central roles in chromosome organization and segregation in all domains of life. The Escherichia coli SMC complex, MukBEF, is required for normal chromosome dynamics and its absence leads to temperature-sensitive growth in rich medium, under conditions of overlapping replication cycles, and anucleate cell formation during permissive growth [1, 2]. Wild type (WT) cells contain ~100 functional MukBEF complexes, with 40-50% associated with chromosomes [4]. These complexes are enriched in the replication origin (ori) region of the cell and act to position oris at either the midcell in new-born cells or the cell quarter position in cells undergoing replication [3,4,5,6]. MukBEF action in vivo, likely through extrusion of DNA loops, as demonstrated for a number of eukaryotic SMC complexes [7], leads to the formation of a MukBEF axial core to the chromosome, from which DNA loops of 15-
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