Abstract
The Ori region of bacterial genomes is segregated early in the replication cycle of bacterial chromosomes. Consequently, Ori region positioning plays a pivotal role in chromosome dynamics. The Ori region of the E. coli chromosome is organized as a macrodomain with specific properties concerning DNA mobility, segregation of loci and long distance DNA interactions. Here, by using strains with chromosome rearrangements and DNA mobility as a read-out, we have identified the MaoP/maoS system responsible for constraining DNA mobility in the Ori region and limiting long distance DNA interactions with other regions of the chromosome. MaoP belongs to a group of proteins conserved in the Enterobacteria that coevolved with Dam methylase including SeqA, MukBEF and MatP that are all involved in the control of chromosome conformation and segregation. Analysis of DNA rings excised from the chromosome demonstrated that the single maoS site is required in cis on the chromosome to exert its effect while MaoP can act both in cis and in trans. The position of markers in the Ori region was affected by inactivating maoP. However, the MaoP/maoS system was not sufficient for positioning the Ori region at the ¼–¾ regions of the cell. We also demonstrate that the replication and the resulting expansion of bulk DNA are localized centrally in the cell. Implications of these results for chromosome positioning and segregation in E. coli are discussed.
Highlights
The size of genomes with respect to cellular dimensions imposes the need for extensive chromosome condensation that is compatible with the genome replication and the expression of genetic information
The E. coli chromosome is divided into four macrodomains (MD) defined as large regions in which DNA interactions occurred preferentially
Enterobacteria that coevolved with the Dam DNA methylase and that includes the MatP protein structuring the Ter macrodomain and the SeqA and MukBEF proteins involved in the control of chromosome conformation and segregation. These results reveal the presence of a dedicated set of factors required in chromosome management in enterobacteria that might compensate, at least partially, for the absence of the ParABS system involved in the condensation and/or segregation of the Ori region in most bacteria
Summary
The size of genomes with respect to cellular dimensions imposes the need for extensive chromosome condensation that is compatible with the genome replication and the expression of genetic information. The bacterial chromosome is organized at multiple levels from the genome content (including the distribution of DNA motifs, genes and replication arms), to chromatin composition, supercoiling domains and large chromosomal domains [1,2]. The E. coli chromosome is divided into four large domains called macrodomains (MDs) [3,4]. MDs are defined as large regions in which DNA interactions occurred preferentially, whilst DNA interactions between different MDs are restricted. The Ori MD contains the origin of replication oriC, the opposite Ter MD contains the replication terminus and the chromosome dimer resolution dif site, whilst the Left and Right MDs flank the Ter MD. Two non-structured (NS) regions (NSRight and NSLeft) flank the Ori MD. DNA sites within the NS regions can interact with both flanking MDs [4]
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