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Abstract
Bacterial plasmids are extrachromosomal DNA that provides selective advantages for bacterial survival. Plasmid partitioning can be remarkably robust. For high-copy-number plasmids, diffusion ensures that both daughter cells inherit plasmids after cell division. In contrast, most low-copy-number plasmids need to be actively partitioned by a conserved tripartite ParA-type system. ParA is an ATPase that binds to chromosomal DNA; ParB is the stimulator of the ParA ATPase and specifically binds to the plasmid at a centromere-like site, parS. ParB stimulation of the ParA ATPase releases ParA from the bacterial chromosome, after which it takes a long time to reset its DNA-binding affinity. We previously demonstrated in vitro that the ParA system can exploit this biochemical asymmetry for directed cargo transport. Multiple ParA-ParB bonds can bridge a parS-coated cargo to a DNA carpet, and they can work collectively as a Brownian ratchet that directs persistent cargo movement with a ParA-depletion zone trailing behind. By extending this model, we suggest that a similar Brownian ratchet mechanism recapitulates the full range of actively segregated plasmid motilities observed in vivo. We demonstrate that plasmid motility is tuned as the replenishment rate of the ParA-depletion zone progressively increases relative to the cargo speed, evolving from diffusion to pole-to-pole oscillation, local excursions, and, finally, immobility. When the plasmid replicates, the daughters largely display motilities similar to that of their mother, except that when the single-focus progenitor is locally excursive, the daughter foci undergo directed segregation. We show that directed segregation maximizes the fidelity of plasmid partition. Given that local excursion and directed segregation are the most commonly observed modes of plasmid motility in vivo, we suggest that the operation of the ParA-type partition system has been shaped by evolution for high fidelity of plasmid segregation.
Highlights
Bacterial plasmids are extrachromosomal DNA that undergoes horizontal gene transfer within a population of microbes [1]
To discern the underlying mechanism of partition complexes (PCs) movement, we start with the simplest case, in which there is a single PC on the nucleoid
Our simulation begins with the following initial conditions: 1) the PC is positioned at the center of the nucleoid; 2) ParA$ATP dimers are randomly distributed on the nucleoid and are in equilibrium with the cytosolic counterpart; and 3) the plasmid-bound ParB dimers have not yet established any bonds with ParA$ATP
Summary
Bacterial plasmids are extrachromosomal DNA that undergoes horizontal gene transfer within a population of microbes [1]. The maintenance of bacterial plasmids during the cell cycle can endow the cells with selective advantages [1]. For low-copy plasmids, such as the P1 or F plasmids, active segregation machinery is needed for stable plasmid maintenance within a bacterial cell population [3,4]. These plasmids encode their own partitioning (or par) genes to assure that the plasmid copies are segregated, transported, and positioned along the nucleoid—a rod-like structure consisting primarily of condensed chromosomal DNA [3].
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