Regulation of potassium uptake in <i>Caulobacter crescentus</i>

Potassium (K⁺) is an essential physiological element determining membrane potential, intracellular pH, osmotic/turgor pressure, and protein synthesis in cells. Here, we describe the regulation of potassium uptake systems in the oligotrophic α-proteobacterium <i>Caulobacter crescentus</i> known as a model for asymmetric cell division. We show that <i>C. crescentus</i> can grow in concentrations from the micromolar to the millimolar range by mainly using two K⁺ transporters to maintain potassium homeostasis, the low-affinity Kup and the high-affinity Kdp uptake systems. When K⁺ is not limiting, we found that the <i>kup</i> gene is essential while <i>kdp</i> inactivation does not impact the growth. In contrast, <i>kdp</i> becomes critical but not essential and <i>kup</i> dispensable for growth in K⁺-limited environments. However, in the absence of <i>kdp</i>, mutations in <i>kup</i> were selected to improve growth in K⁺-depleted conditions, likely by increasing the affinity of Kup for K⁺. In addition, mutations in the KdpDE two-component system, which regulates <i>kdpABCDE</i> expression, suggest that the inner membrane sensor regulatory component KdpD mainly works as a phosphatase to limit the growth when cells reach late exponential phase. Our data therefore suggest that KdpE is phosphorylated by another non-cognate histidine kinase. On top of this, we determined the KdpE-dependent and independent K⁺ transcriptome. Together, our work illustrates how an oligotrophic bacterium responds to fluctuation in K⁺ availability.IMPORTANCEPotassium (K⁺) is a key metal ion involved in many essential cellular processes. Here, we show that the oligotroph <i>Caulobacter crescentus</i> can support growth at micromolar concentrations of K⁺ by mainly using two K⁺ uptake systems, the low-affinity Kup and the high-affinity Kdp. Using genome-wide approaches, we also determined the entire set of genes required for <i>C. crescentus</i> to survive at low K⁺ concentration as well as the full K⁺-dependent regulon. Finally, we found that the transcriptional regulation mediated by the KdpDE two-component system is unconventional since unlike <i>Escherichia coli</i>, the inner membrane sensor regulatory component KdpD seems to work rather as a phosphatase on the phosphorylated response regulator KdpE~P.