Water molecules mediate zinc mobility in the bacterial zinc diffusion channel ZIPB
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 inmore »
- Authors:
-
[2]
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Johns Hopkins Univ., Baltimore, MD (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1582337
- Grant/Contract Number:
- AC02-05CH11231; 5R01DK108599
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Biological Chemistry
- Additional Journal Information:
- Journal Volume: 294; Journal Issue: 36; Journal ID: ISSN 0021-9258
- Publisher:
- American Society for Biochemistry and Molecular Biology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Gupta, Sayan, Merriman, Chengfeng, Petzold, Christopher J., Ralston, Corie Y., and Fu, Dax. Water molecules mediate zinc mobility in the bacterial zinc diffusion channel ZIPB. United States: N. p., 2019.
Web. doi:10.1074/jbc.ra119.009239.
Gupta, Sayan, Merriman, Chengfeng, Petzold, Christopher J., Ralston, Corie Y., & Fu, Dax. Water molecules mediate zinc mobility in the bacterial zinc diffusion channel ZIPB. United States. https://doi.org/10.1074/jbc.ra119.009239
Gupta, Sayan, Merriman, Chengfeng, Petzold, Christopher J., Ralston, Corie Y., and Fu, Dax. Thu .
"Water molecules mediate zinc mobility in the bacterial zinc diffusion channel ZIPB". United States. https://doi.org/10.1074/jbc.ra119.009239. https://www.osti.gov/servlets/purl/1582337.
@article{osti_1582337,
title = {Water molecules mediate zinc mobility in the bacterial zinc diffusion channel ZIPB},
author = {Gupta, Sayan and Merriman, Chengfeng and Petzold, Christopher J. and Ralston, Corie Y. and Fu, Dax},
abstractNote = {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.},
doi = {10.1074/jbc.ra119.009239},
journal = {Journal of Biological Chemistry},
number = 36,
volume = 294,
place = {United States},
year = {2019},
month = {7}
}
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Figures / Tables:
Table 1 : Part 1: The ratio of hydroxyl radical reactivity between Apo-ZIPB and Zn-ZIPB
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