Nonequilibrium polysome dynamics promote chromosome segregation and its coupling to cell growth in Escherichia coli

Chromosome segregation is essential for cellular proliferation. Unlike eukaryotes, bacteria lack cytoskeleton-based machinery to segregate their chromosomal DNA (nucleoid). The bacterial ParABS system segregates the duplicated chromosomal regions near the origin of replication. However, this function does not explain how bacterial cells partition the rest (bulk) of the chromosomal material. Furthermore, some bacteria, including Escherichia coli, lack a ParABS system. Yet, E. coli faithfully segregates nucleoids across various growth rates. Here, we provide theoretical and experimental evidence that polysome production during chromosomal gene expression helps compact, split, segregate, and position nucleoids in E. coli through nonequilibrium dynamics that depend on polysome synthesis, degradation (through mRNA decay), and exclusion from the DNA meshwork. These dynamics inherently couple chromosome segregation to biomass growth across nutritional conditions. Halting chromosomal gene expression and thus polysome production immediately stops sister nucleoid migration, while ensuing polysome depletion gradually reverses nucleoid segregation. Redirecting gene expression away from the chromosome and toward plasmids causes ectopic polysome accumulations that are sufficient to drive aberrant nucleoid dynamics. Cell width enlargement experiments suggest that limiting the exchange of polysomes across DNA-free regions ensures nucleoid segregation along the cell length. Our findings suggest a self-organizing mechanism for coupling nucleoid compaction and segregation to cell growth without the apparent requirement of regulatory molecules.