Abstract

The 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.

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