Coupling of cell growth modulation to asymmetric division and cell cycle regulation in Caulobacter crescentus

In proliferating bacteria, growth rate is often assumed to be similar between daughter cells. However, most of our knowledge of cell growth derives from studies on symmetrically dividing bacteria. In many α-proteobacteria, asymmetric division is a normal part of the life cycle, with each division producing daughter cells with different sizes and fates. Here, we demonstrate that the functionally distinct swarmer and stalked daughter cells produced by the model α-proteobacterium Caulobacter crescentus can have different average growth rates under nutrient-replete conditions despite sharing an identical genome and environment. The discrepancy in growth rate is due to a growth slowdown associated with the cell cycle stage preceding DNA replication (the G1 phase), which initiates in the late predivisional mother cell before daughter cell separation. Both progenies experience a G1-associated growth slowdown, but the effect is more severe in swarmer cells because they have a longer G1 phase. Activity of SpoT, which produces the (p)ppGpp alarmone and extends the G1 phase, accentuates the cell cycle-dependent growth slowdown. Collectively, our data identify a coupling between cell growth, the G1 phase, and asymmetric division that C. crescentus may exploit for environmental adaptation through SpoT activity. This coupling differentially modulates the growth rate of functionally distinct daughter cells, thereby altering the relative abundance of ecologically important G1-specific traits within the population.