Imperfect coordination chemistry facilitates metal ion release in the Psa permease

Couñago, Rafael M., Ween, Miranda P., Begg, Stephanie L., Bajaj, Megha, Zuegg, Johannes, O'Mara, Megan L., Cooper, Matthew A., McEwan, Alastair G., Paton, James C., Kobe, Bostjan and McDevitt, Christopher A. (2014) Imperfect coordination chemistry facilitates metal ion release in the Psa permease. Nature Chemical Biology, 10 1: 35-41. doi:10.1038/nCHeMBIO.1382

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Author Couñago, Rafael M.
Ween, Miranda P.
Begg, Stephanie L.
Bajaj, Megha
Zuegg, Johannes
O'Mara, Megan L.
Cooper, Matthew A.
McEwan, Alastair G.
Paton, James C.
Kobe, Bostjan
McDevitt, Christopher A.
Title Imperfect coordination chemistry facilitates metal ion release in the Psa permease
Journal name Nature Chemical Biology   Check publisher's open access policy
ISSN 1552-4450
1552-4469
Publication date 2014-01-01
Year available 2013
Sub-type Article (original research)
DOI 10.1038/nCHeMBIO.1382
Open Access Status
Volume 10
Issue 1
Start page 35
End page 41
Total pages 7
Place of publication London, United Kingdom
Publisher Nature
Language eng
Abstract The relative stability of divalent first-row transition metal ion complexes, as defined by the Irving-Williams series, poses a fundamental chemical challenge for selectivity in bacterial metal ion acquisition. Here we show that although the substratebinding protein of Streptococcus pneumoniae, PsaA, is finely attuned to bind its physiological substrate manganese, it can also bind a broad range of other divalent transition metal cations. By combining high-resolution structural data, metal-binding assays and mutational analyses, we show that the inability of open-state PsaA to satisfy the preferred coordination chemistry of manganese enables the protein to undergo the conformational changes required for cargo release to the Psa permease. This is specific for manganese ions, whereas zinc ions remain bound to PsaA. Collectively, these findings suggest a new ligand binding and release mechanism for PsaA and related substrate-binding proteins that facilitate specificity for divalent cations during competition from zinc ions, which are more abundant in biological systems.
Formatted abstract
The relative stability of divalent first-row transition metal ion complexes, as defined by the Irving-Williams series, poses a fundamental chemical challenge for selectivity in bacterial metal ion acquisition. Here we show that although the substrate-binding protein of Streptococcus pneumoniae, PsaA, is finely attuned to bind its physiological substrate manganese, it can also bind a broad range of other divalent transition metal cations. By combining high-resolution structural data, metal-binding assays and mutational analyses, we show that the inability of open-state PsaA to satisfy the preferred coordination chemistry of manganese enables the protein to undergo the conformational changes required for cargo release to the Psa permease. This is specific for manganese ions, whereas zinc ions remain bound to PsaA. Collectively, these findings suggest a new ligand binding and release mechanism for PsaA and related substrate-binding proteins that facilitate specificity for divalent cations during competition from zinc ions, which are more abundant in biological systems.
Keyword Biochemistry & Molecular Biology
Biochemistry & Molecular Biology
BIOCHEMISTRY & MOLECULAR BIOLOGY
Q-Index Code C1
Q-Index Status Confirmed Code
Grant ID DP0986578
1022240
Institutional Status UQ
Additional Notes Published online: 10 November 2013.

 
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Created: Fri, 15 Nov 2013, 23:54:42 EST by Mrs Louise Nimwegen on behalf of School of Chemistry & Molecular Biosciences