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

Andreas Kirsten, Martin Herzberg, Alexander Voigt, Javier Seravalli, Gregor Grass, Judith Scherer, Dietrich H. Nies

Research output: Contribution to journalArticle

33 Citations (Scopus)

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 corA1 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, CorA1 as the main secondary magnesium uptake system, and CorA2 and CorA3 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.

Original languageEnglish (US)
Pages (from-to)4652-4663
Number of pages12
JournalJournal of bacteriology
Volume193
Issue number18
DOIs
StatePublished - Sep 1 2011

Fingerprint

Cupriavidus
Homeostasis
Metals
Cations
Zinc
Phosphates
Magnesium
Starvation
Toxic Actions
Gene Expression
Gene Fusion
Coordination Complexes
Divalent Cations
Reporter Genes

ASJC Scopus subject areas

  • Microbiology
  • Molecular Biology

Cite this

Contributions of five secondary metal uptake systems to metal homeostasis of Cupriavidus metallidurans CH34. / Kirsten, Andreas; Herzberg, Martin; Voigt, Alexander; Seravalli, Javier; Grass, Gregor; Scherer, Judith; Nies, Dietrich H.

In: Journal of bacteriology, Vol. 193, No. 18, 01.09.2011, p. 4652-4663.

Research output: Contribution to journalArticle

Kirsten, Andreas ; Herzberg, Martin ; Voigt, Alexander ; Seravalli, Javier ; Grass, Gregor ; Scherer, Judith ; Nies, Dietrich H. / Contributions of five secondary metal uptake systems to metal homeostasis of Cupriavidus metallidurans CH34. In: Journal of bacteriology. 2011 ; Vol. 193, No. 18. pp. 4652-4663.
@article{542c8bc263434daa8b935893d14e439b,
title = "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 corA1 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, CorA1 as the main secondary magnesium uptake system, and CorA2 and CorA3 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.",
author = "Andreas Kirsten and Martin Herzberg and Alexander Voigt and Javier Seravalli and Gregor Grass and Judith Scherer and Nies, {Dietrich H.}",
year = "2011",
month = "9",
day = "1",
doi = "10.1128/JB.05293-11",
language = "English (US)",
volume = "193",
pages = "4652--4663",
journal = "Journal of Bacteriology",
issn = "0021-9193",
publisher = "American Society for Microbiology",
number = "18",

}

TY - JOUR

T1 - Contributions of five secondary metal uptake systems to metal homeostasis of Cupriavidus metallidurans CH34

AU - Kirsten, Andreas

AU - Herzberg, Martin

AU - Voigt, Alexander

AU - Seravalli, Javier

AU - Grass, Gregor

AU - Scherer, Judith

AU - Nies, Dietrich H.

PY - 2011/9/1

Y1 - 2011/9/1

N2 - 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 corA1 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, CorA1 as the main secondary magnesium uptake system, and CorA2 and CorA3 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.

AB - 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 corA1 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, CorA1 as the main secondary magnesium uptake system, and CorA2 and CorA3 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.

UR - http://www.scopus.com/inward/record.url?scp=80052541464&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=80052541464&partnerID=8YFLogxK

U2 - 10.1128/JB.05293-11

DO - 10.1128/JB.05293-11

M3 - Article

VL - 193

SP - 4652

EP - 4663

JO - Journal of Bacteriology

JF - Journal of Bacteriology

SN - 0021-9193

IS - 18

ER -