Chromosome choreography during the non-binary cell cycle of a predatory bacterium

Abstract

In bacteria, the dynamics of chromosome replication and segregation are tightly coordinated with cell-cycle progression and largely rely on specific spatiotemporal arrangement of the chromosome. Whereas these key processes are mostly investigated in species that divide by binary fission, they remain mysterious in bacteria producing larger number of descendants. Here, we establish the predatory bacterium Bdellovibrio bacteriovorus as a model to investigate the non-binary processing of a circular chromosome. We found that its single chromosome is highly compacted in a polarized nucleoid that excludes freely diffusing proteins during the non-proliferative stage of the cell cycle. A binary-like cycle of DNA replication and asymmetric segregation is followed by multiple asynchronous rounds of replication and progressive ParABS-dependent partitioning, uncoupled from cell division. Finally, we provide the first evidence for an on-off behavior of the ParB protein, which localizes at the centromere in a cell-cycle-regulated manner. Altogether, our findings support a model of complex chromosome choreography leading to the generation of variable, odd, or even numbers of offspring and highlight the adaptation of conserved mechanisms to achieve non-binary reproduction.

Keywords: Bdellovibrio bacteriovorus; ParB; bacterial cell cycle; bacterial predation; chromosome replication; chromosome segregation; non-binary division; spatiotemporal organization.