Dynamics of an Interactive Network Composed of a Bacterial Two-Component System, a Transporter and K+ as Mediator

Ralf Heermann, Katja Zigann, Stefan Gayer, Maria Rodriguez-Fernandez, Julio R Banga, Andreas Kremling and Kirsten Jung

PLOS ONE, 2014, vol. 9, issue 2, 1-15

Abstract: KdpD and KdpE form a histidine kinase/response regulator system that senses K+ limitation and induces the kdpFABC operon, which encodes a high-affinity K+ uptake complex. To define the primary stimulus perceived by KdpD we focused in this study on the dynamics of the Kdp response. Escherichia coli cells were subjected to severe K+ limitation, and all relevant parameters of the Kdp response, i.e., levels of kdpFABC transcripts and KdpFABC proteins, as well as extra- and intracellular K+ concentrations, were quantitatively analysed over time (0 to 180 min). Unexpectedly, induction of kdpFABC was found to follow a non-monotonic time-course. To interpret this unusual behaviour, a mathematical model that adequately captures the dynamics of the Kdp system was established and used for simulations. We found a strong correlation between KdpD/KdpE activation and the intracellular K+ concentration, which is influenced by the uptake of K+ via the KdpFABC complex. Based on these results a model is proposed in which KdpD/KdpE phosphorylation is inversely correlated with the intracellular K+ concentration. To corroborate this hypothesis an isogenic mutant that produces a defective KdpFABC complex, and the trans-complemented mutant that expresses the KtrAB high-affinity K+ uptake system of Vibrio alginolyticus were quantitatively analysed. Experimental data and simulations for the mutants consistently support the tight correlation between KdpD/KdpE activation and the intracellular K+ concentration. This study presents a striking example of the non-intuitive dynamics of a functional unit comprising signalling proteins and a transporter with K+ as mediator.

Date: 2014
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Persistent link: https://EconPapers.repec.org/RePEc:plo:pone00:0089671

DOI: 10.1371/journal.pone.0089671

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