Regulation of potassium homeostasis inCaulobacter crescentus

Abstract

Potassium (K+) is an essential physiological element determining membrane potential, intracellular pH, osmotic/turgor pressure, and protein synthesis in cells. Nevertheless, K+homeostasis remains poorly studied in bacteria. Here we describe the regulation of potassium uptake systems in the oligotrophic α-proteobacteriumCaulobacter crescentusknown as a model for asymmetric cell division. We show that C. crescentus can grow in concentrations from the micromolar to the millimolar range by essentially 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 thekupgene is essential whilekdpinactivation does not impact the growth. In contrast,kdpbecomes critical but not essential andkupdispensable for growth in K+-limited environments. However, in the absence ofkdp, mutations inkupwere selected to improve growth in K+-depleted conditions, likely by improving the affinity of Kup for K+. In addition, mutations in the KdpDE two-component system, which regulateskdpABCexpression, suggest that the inner membrane sensor regulatory component KdpD works as a kinase in early stages of growth and as a phosphatase to regulate transition into stationary phase. Our data also show that KdpE is not only phosphorylated by KdpD but also by another non-cognate histidine kinase. On top of this, we determined the KdpE-dependent and independent K+transcriptome as well as the direct targets of KdpE. Together, our work illustrates how an oligotrophic bacterium responds to fluctuation in K+availability.