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The fluoride permeation pathway and anion recognition in Fluc family fluoride channels
Published version of a preprint
Abstract
Fluc family fluoride channels protect microbes against ambient environmental fluoride by undermining the cytoplasmic accumulation of this toxic halide. These proteins are structurally idiosyncratic, and thus the permeation pathway and mechanism have no analogy in other known ion channels. Although fluoride-binding sites were identified in previous structural studies, it was not evident how these ions access aqueous solution, and the molecular determinants of anion recognition and selectivity have not been elucidated. Using x-ray crystallography, planar bilayer electrophysiology, and liposome-based assays, we identified additional binding sites along the permeation pathway. We used this information to develop an oriented system for planar lipid bilayer electrophysiology and observed anion block at one of these sites, revealing insights into the mechanism of anion recognition. We propose a permeation mechanism involving alternating occupancy of anion-binding sites that are fully assembled only as the substrate approaches.
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Fluc proteins are small, homodimeric permeases, with extremely high specificity for fluoride anion (10,000-fold versus chloride).
“The Fluc proteins are small, homodimeric permeases (175), with extremely high specificity for the fluoride anion (10,000-fold versus chloride) (176).”
From Toward the development of a molecular toolkit for the microbial remediation of per-and polyfluoroalkyl substances (2024) · cites this paper as [175]
The induction of the membrane export protein CrcB is highly protective against fluoride.
“The induction of the membrane export protein-designated CrcB is shown to be highly protective against fluoride (9, 12, 13).”
From Recombinant Pseudomonas growing on non-natural fluorinated substrates shows stress but overall tolerance to cytoplasmically released fluoride anion (2024) · cites this paper as [13]
A knockout of the crcB gene, encoding a membrane protein that exports fluoride, makes P. putida KT2440 and other bacteria much more sensitive to fluoride.
“Previous studies had also shown that a knockout of the crcB gene, encoding a membrane protein that exports fluoride, makes P. putida KT2440 (46) and other bacteria (13) much more sensitive to fluoride.”
From Recombinant Pseudomonas growing on non-natural fluorinated substrates shows stress but overall tolerance to cytoplasmically released fluoride anion (2024) · cites this paper as [13]
Flucs have a rapid rate of F− efflux (10^6 ions/s) and extremely high selectivity for fluoride over other anions, exceeding 10,000-fold.
“The Flucs are notable for their rapid rate of F− efflux (106 ions/s) and extremely high selectivity for fluoride over other anions, which exceeds 10,000-fold81,82.”
From The link between ancient microbial fluoride resistance mechanisms and bioengineering organofluorine degradation or synthesis (2024) · cites this paper as [82]
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Cites
Crystal structures of a double-barrelled fluoride ion channel
Stockbridge, R. B., Kolmakova-Partensky, L., Shane, T., Koide, A., Koide, S., Miller, C., & Newstead, S. (2015) · Nature · doi:10.1038/nature14981 · Cited by 119
Self-citationBacterial fluoride resistance, Fluc channels, and the weak acid accumulation effect
Ji, C., Stockbridge, R. B., & Miller, C. (2014) · Journal of General Physiology · doi:10.1085/jgp.201411243 · Cited by 97
Self-citationMembrane exporters of fluoride ion
McIlwain, B. C., Ruprecht, M. T., & Stockbridge, R. B. (2021) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-071520-112507 · Cited by 69
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Cited by
Sorted by citations
Stockbridge, R. B., & Wackett, L. P. (2024) · Nature Communications · doi:10.1038/s41467-024-49018-1 · Cited by 80
Self-citationMembrane exporters of fluoride ion
McIlwain, B. C., Ruprecht, M. T., & Stockbridge, R. B. (2021) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-071520-112507 · Cited by 69
Self-citationHu, M., & Scott, C. (2024) · Applied and Environmental Microbiology · doi:10.1128/aem.00157-24 · Cited by 63
Dodge, A. G., Thoma, C. J., O’Connor, M. R., & Wackett, L. P. (2024) · mBio · doi:10.1128/mbio.02785-23 · Cited by 23
Metadata
- Authors
- McIlwain, B. C., Gundepudi, R., Koff, B. B., & Stockbridge, R. B.
- Affiliations
- Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, United States
- Program in Biophysics, University of Michigan, Ann Arbor, United States
- ORCID
- Stockbridge, Randy B
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2021-07-12
- Volume
- 10
- ISSN
- 2050-084X
- PMC
- PMC8315801
- Cited by
- 24
- References
- 3
- Language
- en
- Licence
- Funders
- National Institutes of Health (R35-GM128768)
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