Cell cycle-dependent organization of a bacterial centromere through multi-layered regulation of the ParABS system

Abstract

The accurate distribution of genetic material is crucial for all organisms. In most bacteria, chromosome segregation is achieved by the ParABS system, in which the ParB-bound centromere parS is actively partitioned by ParA. While this system is highly conserved, its adaptation in organisms with unique lifestyles and its regulation between developmental stages remain unexplored. Bdellovibrio bacteriovorus is a predatory bacterium proliferating through polyploid replication and non-binary division inside other bacteria. Our study reveals the subcellular dynamics and multi-layered regulation of the ParABS system, coupled to the cell cycle of B. bacteriovorus. We found that ParA:ParB ratios fluctuate between predation stages, their balance being critical for cell cycle progression. Moreover, the parS chromosomal context in non-replicative cells, combined with ParB depletion at cell division, critically contribute to the unique cell cycle-dependent organization of the centromere in this bacterium, highlighting new levels of complexity in chromosome segregation and cell cycle control. Author summaryThe precise distribution of genetic material to the progeny is essential for all living organisms, and the ParABS system is critical for this process in bacteria. Our study provides novel insights into the regulation of this system in a predatory bacterium that exhibits a non-canonical cell cycle, in which the chromosome is copied and segregated multiple times during growth inside a prey bacterium. Our work reveals the subcellular dynamics and multi-level regulation of the ParABS system in this bacterium, which results in the unique cell-cycle dependent assembly of the segregation complex at the chromosomal centromere. Our findings provide a deeper understanding of the adaptation of the ParABS system across bacterial species and developmental stages.