Water molecules mediate zinc mobility in the bacterial zinc diffusion channel ZIPB

Sayan Gupta, Chengfeng Merriman, Christopher J. Petzold, Corie Y. Ralston, Dax Fu

Research output: Contribution to journalArticle

Abstract

Regulated ion diffusion across biological membranes is vital for cell function. In a nanoscale ion channel, the active role of discrete water molecules in modulating hydrodynamic behaviors of individual ions is poorly understood because of the technical challenge of tracking water molecules through the channel. Here we report the results of a hydroxyl radical footprinting analysis of the zinc-selective channel ZIPB from the Gram-negative bacterium, Bordetella bronchiseptica. Irradiating ZIPB by microsecond X-ray pulses activated water molecules to form covalent hydroxyl radical adducts at nearby residues, which were identified by bottom-up proteomics to detect residues that interact either with zinc or water in response to zinc binding. We found a series of residues exhibiting reciprocal changes in water accessibility attributed to alternating zinc and water binding. Mapping these residues to the previously reported crystal structure of ZIPB, we identified a water-reactive pathway that superimposed on a zinc translocation pathway consisting of two binuclear metal centers and an interim zinc-binding site. The cotranslocation of zinc and water suggested that pore-lining residues undergo a mode switch between zinc coordination and water binding to confer zinc mobility. The unprecedented details of water-mediated zinc transport identified here highlight an essential role of solvated waters in driving zinc coordination dynamics and transmembrane crossing.

Original languageEnglish (US)
Pages (from-to)13327-13335
Number of pages9
JournalJournal of Biological Chemistry
Volume294
Issue number36
DOIs
StatePublished - Jan 1 2019

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Zinc
Molecules
Water
Hydroxyl Radical
Bordetella bronchiseptica
Ions
Biological membranes
Hydrodynamics
Gram-Negative Bacteria
Ion Channels
Linings
Proteomics
Bacteria
Crystal structure
Metals
Binding Sites
Switches
X-Rays
X rays
Membranes

ASJC Scopus subject areas

  • Biochemistry
  • Molecular Biology
  • Cell Biology

Cite this

Water molecules mediate zinc mobility in the bacterial zinc diffusion channel ZIPB. / Gupta, Sayan; Merriman, Chengfeng; Petzold, Christopher J.; Ralston, Corie Y.; Fu, Dax.

In: Journal of Biological Chemistry, Vol. 294, No. 36, 01.01.2019, p. 13327-13335.

Research output: Contribution to journalArticle

Gupta, Sayan ; Merriman, Chengfeng ; Petzold, Christopher J. ; Ralston, Corie Y. ; Fu, Dax. / Water molecules mediate zinc mobility in the bacterial zinc diffusion channel ZIPB. In: Journal of Biological Chemistry. 2019 ; Vol. 294, No. 36. pp. 13327-13335.
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