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High-resolution mapping of metal ions reveals principles of surface layer assembly in Caulobacter crescentus cells

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Herdman, M., von Kügelgen, A., Kureisaite-Ciziene, D., Duman, R., El Omari, K., Garman, E. F., Kjaer, A., Kolokouris, D., Löwe, J., Wagner, A., Stansfeld, Phillip J. and Bharat, T. (2022) High-resolution mapping of metal ions reveals principles of surface layer assembly in Caulobacter crescentus cells. Structure, 30 (2). pp. 215-228. doi:10.1016/j.str.2021.10.012 ISSN 0969-2126.

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Official URL: https://doi.org/10.1016/j.str.2021.10.012

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Abstract

Surface layers (S-layers) are proteinaceous crystalline coats that constitute the outermost component of most prokaryotic cell envelopes. In this study, we have investigated the role of metal ions in the formation of the Caulobacter crescentus S-layer using high-resolution structural and cell biology techniques, as well as molecular simulations. Utilizing optical microscopy of fluorescently tagged S-layers, we show that calcium ions facilitate S-layer lattice formation and cell-surface binding. We report all-atom molecular dynamics simulations of the S-layer lattice, revealing the importance of bound metal ions. Finally, using electron cryomicroscopy and long-wavelength X-ray diffraction experiments, we mapped the positions of metal ions in the S-layer at near-atomic resolution, supporting our insights from the cellular and simulations data. Our findings contribute to the understanding of how C. crescentus cells form a regularly arranged S-layer on their surface, with implications on fundamental S-layer biology and the synthetic biology of self-assembling biomaterials.

Item Type: Journal Article
Subjects: Q Science > QD Chemistry
Q Science > QH Natural history
Q Science > QP Physiology
Q Science > QR Microbiology
Divisions: Faculty of Science, Engineering and Medicine > Science > Life Sciences (2010- )
Library of Congress Subject Headings (LCSH): Prokaryotes -- Physiology, Cytoplasm, Bacteria, Metal ions -- Research, Carrier proteins -- Research, Fluorescence microscopy, X-ray diffraction imaging
Journal or Publication Title: Structure
Publisher: Cell Press
ISSN: 0969-2126
Official Date: 3 February 2022
Dates:
DateEvent
3 February 2022Published
19 November 2021Available
22 October 2021Accepted
Volume: 30
Number: 2
Page Range: pp. 215-228
DOI: 10.1016/j.str.2021.10.012
Status: Peer Reviewed
Publication Status: Published
Access rights to Published version: Restricted or Subscription Access
Date of first compliant deposit: 27 September 2021
Date of first compliant Open Access: 7 February 2022
RIOXX Funder/Project Grant:
Project/Grant IDRIOXX Funder NameFunder ID
BB/M011224/1[BBSRC] Biotechnology and Biological Sciences Research Councilhttp://dx.doi.org/10.13039/501100000268
UNSPECIFIED[EPSRC] Engineering and Physical Sciences Research Councilhttp://dx.doi.org/10.13039/501100000266
208361/Z/17/ZWellcome Trusthttp://dx.doi.org/10.13039/100010269
MR/S009213/1[MRC] Medical Research Councilhttp://dx.doi.org/10.13039/501100000265
BB/P01948X/1[BBSRC] Biotechnology and Biological Sciences Research Councilhttp://dx.doi.org/10.13039/501100000268
BB/R002517/1[BBSRC] Biotechnology and Biological Sciences Research Councilhttp://dx.doi.org/10.13039/501100000268
BB/S003339/1[BBSRC] Biotechnology and Biological Sciences Research Councilhttp://dx.doi.org/10.13039/501100000268
EP/R029407/1[EPSRC] Engineering and Physical Sciences Research Councilhttp://dx.doi.org/10.13039/501100000266
EP/P020232/1[EPSRC] Engineering and Physical Sciences Research Councilhttp://dx.doi.org/10.13039/501100000266
202231/Z/16/ZWellcome Trusthttp://dx.doi.org/10.13039/100010269
202231/Z/16/ZRoyal Societyhttp://dx.doi.org/10.13039/501100000288
UNSPECIFIEDVallee Foundationhttp://dx.doi.org/10.13039/100007204
UNSPECIFIEDLeverhulme Trusthttp://dx.doi.org/10.13039/501100000275
UNSPECIFIEDJohn Fell Fund, University of Oxfordhttp://dx.doi.org/10.13039/501100004789
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