Abstract
Cells closely coordinate cell division with chromosome replication and segregation; however, the mechanisms responsible for this coordination still remain largely unknown. Here, we analyzed the spatial arrangement and temporal dynamics of the 9.1 Mb circular chromosome in the rod-shaped cells of Myxococcus xanthus. For chromosome segregation, M. xanthus uses a parABS system, which is essential, and lack of ParB results in chromosome segregation defects as well as cell divisions over nucleoids and the formation of anucleate cells. From the determination of the dynamic subcellular location of six genetic loci, we conclude that in newborn cells ori, as monitored following the ParB/parS complex, and ter regions are localized in the subpolar regions of the old and new cell pole, respectively and each separated from the nearest pole by approximately 1 µm. The bulk of the chromosome is arranged between the two subpolar regions, thus leaving the two large subpolar regions devoid of DNA. Upon replication, one ori region remains in the original subpolar region while the second copy segregates unidirectionally to the opposite subpolar region followed by the rest of the chromosome. In parallel, the ter region of the mother chromosome relocates, most likely passively, to midcell, where it is replicated. Consequently, after completion of replication and segregation, the two chromosomes show an ori-ter-ter-ori arrangement with mirror symmetry about a transverse axis at midcell. Upon completion of segregation of the ParB/parS complex, ParA localizes in large patches in the DNA-free subpolar regions. Using an Ssb-YFP fusion as a proxy for replisome localization, we observed that the two replisomes track independently of each other from a subpolar region towards ter. We conclude that M. xanthus chromosome arrangement and dynamics combine features from previously described systems with new features leading to a novel spatiotemporal arrangement pattern.
Highlights
In all cells, chromosome replication and segregation are closely coordinated with cell division to ensure that daughter cells inherit the correct chromosome complement
Work on several model organisms has revealed that bacterial chromosomes are spatially highly arranged throughout the cell cycle in a dynamic yet reproducible manner
These analyses have demonstrated significant differences between chromosome arrangements and dynamics in different bacterial species
Summary
Chromosome replication and segregation are closely coordinated with cell division to ensure that daughter cells inherit the correct chromosome complement. Bacterial chromosomes are spatially precisely arranged with individual chromosomal loci reproducibly localizing to the same subcellular locations [3,4,5,6,7,8,9] and this spatial arrangement is established during the segregation process [3,4,7,10]. The mechanistic details underlying the linked processes of chromosome segregation and spatial arrangement in bacteria are much less understood than in the case of their eukaryotic counterparts and have only been studied in details in a few species. These analyses have revealed significant differences in chromosome arrangement as well as in the mechanisms of chromosome segregation in different bacterial species
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