Long range chromosome organization in Escherichia coli: The position of the replication origin defines the non-structured regions and the Right and Left macrodomains

The Escherichia coli chromosome is organized into four macrodomains (Ori, Ter, Right and Left) and two non-structured regions.This organization influences the segregation of sister chromatids, the mobility of chromosomal DNA, and the cellular localization of the chromosome.The organization of the Ter and Ori macrodomains relies on two specific systems, MatP/matS for the Ter domain and MaoP/maoS for the Ori domain, respectively.Here by constructing strains with chromosome rearrangements to reshuffle the distribution of chromosomal segments, we reveal that the difference between the non-structured regions and the Right and Left lateral macrodomains relies on their position on the chromosome.A change in the genetic location of oriC generated either by an inversion within the Ori macrodomain or by the insertion of a second oriC modifies the position of Right and Left macrodomains, as the chromosome region the closest to oriC are always non-structured while the regions further away behave as macrodomain regardless of their DNA sequence.Using fluorescent microscopy we estimated that loci belonging to a non-structured region are significantly closer to the Ori MD than loci belonging to a lateral MD.Altogether, our results suggest that the origin of replication plays a prominent role in chromosome organization in E. coli, as it determines structuring and localization of macrodomains in growing cell. Author summaryChromosomes allow the genetic information to be stored, transmitted and organized inside the cell.In bacteria, chromosomes are generally circular and they are shaped and organized by several mechanisms allowing simultaneous transcription, replication and segregation.The way such fundamental processes are managed is still unclear, but in the Gram negative bacteria Escherichia coli, one level of chromosome organization relies on a large scale structuring of the chromosome in macrodomains and non-structured regions.Macrodomains have been defined as chromosomal domains of megabase (Mb) sized genetically isolated from each other.E. coli chromosome is divided in 4 macrodomains