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Contributions of five secondary metal uptake systems to metal homeostasis of Cupriavidus metallidurans CH34.

ABSTRACT: Cupriavidus metallidurans is adapted to high concentrations of transition metal cations and is a model system for studying metal homeostasis in difficult environments. The elemental composition of C. metallidurans cells cultivated under various conditions was determined, revealing the ability of the bacterium to shield homeostasis of one essential metal from the toxic action of another. The contribution of metal uptake systems to this ability was studied. C. metallidurans contains three CorA members of the metal inorganic transport (MIT) protein family of putative magnesium uptake systems, ZupT of the ZRT/IRT protein, or ZIP, family, and PitA, which imports metal phosphate complexes. Expression of the genes for all these transporters was regulated by zinc availability, as shown by reporter gene fusions. While expression of zupT was upregulated under conditions of zinc starvation, expression of the other genes was downregulated at high zinc concentrations. Only corA(1) expression was influenced by magnesium starvation. Deletion mutants were constructed to characterize the contribution of each system to transition metal import. This identified ZupT as the main zinc uptake system under conditions of low zinc availability, CorA(1) as the main secondary magnesium uptake system, and CorA(2) and CorA(3) as backup systems for metal cation import. PitA may function as a cation-phosphate uptake system, the main supplier of divalent metal cations and phosphate in phosphate-rich environments. Thus, metal homeostasis in C. metallidurans is achieved by highly redundant metal uptake systems, which have only minimal cation selectivity and are in combination with efflux systems that "worry later" about surplus cations.

SUBMITTER: Kirsten A

PROVIDER: S-EPMC3165648 | biostudies-literature | 2011 Sep

REPOSITORIES: biostudies-literature

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Contributions of five secondary metal uptake systems to metal homeostasis of Cupriavidus metallidurans CH34.

Kirsten Andreas A Herzberg Martin M Voigt Alexander A Seravalli Javier J Grass Gregor G Scherer Judith J Nies Dietrich H DH

Journal of bacteriology 20110708 18

Cupriavidus metallidurans is adapted to high concentrations of transition metal cations and is a model system for studying metal homeostasis in difficult environments. The elemental composition of C. metallidurans cells cultivated under various conditions was determined, revealing the ability of the bacterium to shield homeostasis of one essential metal from the toxic action of another. The contribution of metal uptake systems to this ability was studied. C. metallidurans contains three CorA mem ...[more]

PMID: 21742896

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Project description:Central to the ability of Cupriavidus metallidurans to maintain its metal homoeostasis is the metal transportome, composed of uptake and efflux systems. Seven secondary metal import systems, ZupT, PitA, CorA1, CorA2, CorA3, ZntB, and HoxN, interact and are at the core of the metal uptake transportome. The 7-fold deletion mutant ?7 (?zupT ?pitA ?corA1?corA2?corA3?zntB ?hoxN) of parent strain AE104 is still able to maintain its cellular metal content, although at the cost of reduced fitness (M. Herzberg, L. Bauer, A. Kirsten, and D. H. Nies, Metallomics, in press, http://dx.doi.org/10.1039/C5MT00295H). Strain ?7 does not express genes for backup importers, and so ?7 should use metal uptake systems also produced in the AE104 parent cells. These systems should be activated in ?7 by posttranscriptional regulatory processes. The decreased fitness of ?7 correlated with a zinc-dependent downregulation of the overall metabolic backbone of the cells even at nontoxic external zinc concentrations. Responsible for this decreased fitness of ?7 was a negative interference of the activity of two P-type ATPases, MgtA and MgtB, which, on the other hand, kept ?7 at a fitness level higher than that of the ?9 (?7 ?mgtA::kan ?mgtB) mutant strain. This revealed a complicated interplay of the metal uptake transportome of C. metallidurans, which is composed of the seven secondary uptake systems, MgtA, MgtB, and yet-unknown components, with cytoplasmic transition metal pools and posttranscriptional regulatory processes. IMPORTANCE Bacteria, including pathogenic strains, need to make use of the metal composition and speciation of their environment to fulfill the requirement of the cytoplasmic metal content and composition. This task is performed by the bacterial metal transportome, composed of uptake and efflux systems. Seven interacting secondary metal uptake systems are at the core of the metal transportome in C. metallidurans. This publication verifies that posttranscriptional events are responsible for activation of even more, yet-unknown, metal import systems in the 7-fold deletion mutant ?7. Two P-type ATPases were identified as new members of the metal uptake transportome. This publication demonstrates the complexity of the metal transportome and the regulatory processes involved.

Dataset Information

Contributions of five secondary metal uptake systems to metal homeostasis of Cupriavidus metallidurans CH34.

Publications

Contributions of five secondary metal uptake systems to metal homeostasis of Cupriavidus metallidurans CH34.

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