Modulation of prey size reveals adaptability and robustness in the cell cycle of an intracellular predator

Despite a remarkable diversity of lifestyles, bacterial replication has only been investigated in a few model species. In bacteria that do not rely on canonical binary division for proliferation, the coordination of major cellular processes is still largely mysterious. Moreover, the dynamics of bacterial growth and division remain unexplored within spatially confined niches where nutrients are limited. This includes the life cycle of the model endobiotic predatory bacterium Bdellovibrio bacteriovorus, which grows by filamentation within its prey and produces a variable number of daughter cells. Here, we examined the impact of the micro-compartment in which predators replicate (i.e., the prey bacterium) on their cell-cycle progression at the single-cell level. Using Escherichia coli with genetically encoded size differences, we show that the duration of the predator cell cycle scales with prey size. Consequently, prey size determines predator offspring numbers. We found that individual predators elongate exponentially, with a growth rate determined by the nutritional quality of the prey, irrespective of prey size. However, the size of newborn predator cells is remarkably stable across prey nutritional content and size variations. Tuning the predatory cell cycle by modulating prey dimensions also allowed us to reveal invariable temporal connections between key cellular processes. Altogether, our data imply adaptability and robustness shaping the enclosed cell-cycle progression of B. bacteriovorus, which might contribute to optimal exploitation of the finite resources and space in their prey. This study extends the characterization of cell cycle control strategies and growth patterns beyond canonical models and lifestyles. [Display omitted] •Bdellovibrio cell-cycle duration and number of offspring scale with prey size•Nutritional quality, but not the size of the prey, impacts predator growth rate•The size of newborn predators is not affected by growth rate or cell-cycle duration•The temporal connection between the last cell cycle steps is invariable Santin et al. investigate the proliferation of Bdellovibrio bacteriovorus inside other bacteria. They found that the size and content of the prey cell differentially modulate the predator cell cycle, offspring number, and growth rate. This study reveals new insights into bacterial growth patterns in confined environments and atypical lifestyles.