Spatial control over near-critical-point operation ensures fidelity of ParABS-mediated bacterial genome segregation

Abstract

In bacteria, most low-copy-number plasmid and chromosomally encoded partition systems belong to the tripartite ParABS partition machinery. Despite the importance in genetic inheritance, the mechanisms of ParABS-mediated genome partition are not well understood. Combining theory and experiment, we provided evidences that the ParABS system - partitioning via the ParA gradient-based Brownian ratcheting - operates near a critical point in vivo. This near-critical-point operation adapts the segregation distance of replicated plasmids to the half-length of the elongating nucleoid, ensuring both cell halves to inherit one copy of the plasmids. Further, we demonstrated that the plasmid localizes the cytoplasmic ParA to buffer the partition fidelity against the large cell-to-cell fluctuations in ParA level. Thus, the spatial control over the near-critical-point operation not only ensures both sensitive adaption and robust execution of partitioning, but sheds light on the fundamental question in cell biology: How do cells faithfully measure cellular-scale distance by only using molecular-scale interactions?