Regulation of potassium uptake in Caulobacter crescentus. Potassium homeostasis in C. crescentus

Alex Armando Quintero Yanes, Loic Leger, Madeline Collignon, Julien Mignon, Aurelie Mayard, Catherine Michaux, Regis Hallez

Research output: Contribution to journalArticlepeer-review

53 Downloads (Pure)

Abstract

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 Caulobacter crescentus known as a model for asymmetric cell division. We show that C. crescentus 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 kup gene is essential while kdp inactivation does not impact the growth. In contrast, kdp becomes critical but not essential and kup dispensable for growth in K +-limited environments. However, in the absence of kdp, mutations in kup 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 kdpABCDE 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.

Original languageEnglish
Article numbere0010724
Pages (from-to)e0010724
JournalJournal of Bacteriology
Volume206
Issue number9
Early online date12 Aug 2024
DOIs
Publication statusPublished - 19 Sept 2024

Funding

We thank the members of the Hallez lab for critical reading of the manuscript and helpful discussions. The authors are also grateful to the PTCI high-performance computing resource of the University of Namur. The present research benefited from computational resources made available on Lucia, the Tier-1 supercomputer of the Walloon Region, infrastructure funded by the Walloon Region under the grant agreement no. 1910247. This work was supported by the Fonds de la Recherche Scientifique \u2013 FNRS (F.R.S. \u2013 FNRS) with a Welbio Starting Grant (WELBIO-CR-2019S-05) to R.H. A.Q.-Y. was supported by a postdoctoral fellowship from the University of Namur (UNamur). L.L. and J.M. are both supported by the F.R.S. \u2013 FNRS, as a postdoctoral researcher for L.L. and a research fellow for J.M. C.M and R.H. are senior research associates of the F.R.S. \u2013 FNRS. Funder Grant(s) Author(s) Walloon excellence in life sciences and WELBIO-CR-2019S-05 R\u00E9gis Hallez biotechnology (WELBIO) AUL | Universit\u00E9 de Namur (UNamur) FSR Postdoctoral Quintero-Yanes Fellowship Alex Waalse Gewest (Walloon Region) 1910247 Catherine Michaux

FundersFunder number
PTCI
WELBIO-CR-2019S-05 Régis Hallez biotechnology
FSR Postdoctoral Quintero-Yanes Fellowship Alex Waalse Gewest
University of Namur
Région Wallonne1910247
Fonds De La Recherche Scientifique - FNRSWELBIO-CR-2019S-05

    Keywords

    • Potassium transport
    • Two-component system
    • Kup
    • KdpE
    • KdpD
    • potassium transport
    • two-component system

    Fingerprint

    Dive into the research topics of 'Regulation of potassium uptake in Caulobacter crescentus. Potassium homeostasis in C. crescentus'. Together they form a unique fingerprint.

    Cite this