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Title: Topologically-guided continuous protein crystallization controls bacterial surface layer self-assembly

Abstract

Many bacteria and most archaea possess a crystalline protein surface layer (S-layer), which surrounds their growing and topologically complicated outer surface. Constructing a macromolecular structure of this scale generally requires localized enzymatic machinery, but a regulatory framework for S-layer assembly has not been identified. By labeling, superresolution imaging, and tracking the S-layer protein (SLP) from C. crescentus, we show that 2D protein self-assembly is sufficient to build and maintain the S-layer in living cells by efficient protein crystal nucleation and growth. We propose a model supported by single-molecule tracking whereby randomly secreted SLP monomers diffuse on the lipopolysaccharide (LPS) outer membrane until incorporated at the edges of growing 2D S-layer crystals. Surface topology creates crystal defects and boundaries, thereby guiding S-layer assembly. Unsupervised assembly poses challenges for therapeutics targeting S-layers. However, protein crystallization as an evolutionary driver rationalizes S-layer diversity and raises the potential for biologically inspired self-assembling macromolecular nanomaterials.

Authors:
 [1];  [2];  [1];  [2];  [1];  [3]; ORCiD logo [3];  [1]; ORCiD logo [2]; ORCiD logo [1]
  1. Stanford Univ., CA (United States)
  2. Stanford Univ., CA (United States); SLAC National Accelerator Lab., Menlo Park, CA (United States)
  3. Univ. of British Columbia, Vancouver, BC (Canada)
Publication Date:
Research Org.:
SLAC National Accelerator Lab., Menlo Park, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1546945
Grant/Contract Number:  
AC02-76SF00515; R35-GM118067; R35-GM118071
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 10; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Comerci, Colin J., Herrmann, Jonathan, Yoon, Joshua, Jabbarpour, Fatemeh, Zhou, Xiaofeng, Nomellini, John F., Smit, John, Shapiro, Lucy, Wakatsuki, Soichi, and Moerner, W. E. Topologically-guided continuous protein crystallization controls bacterial surface layer self-assembly. United States: N. p., 2019. Web. doi:10.1038/s41467-019-10650-x.
Comerci, Colin J., Herrmann, Jonathan, Yoon, Joshua, Jabbarpour, Fatemeh, Zhou, Xiaofeng, Nomellini, John F., Smit, John, Shapiro, Lucy, Wakatsuki, Soichi, & Moerner, W. E. Topologically-guided continuous protein crystallization controls bacterial surface layer self-assembly. United States. doi:10.1038/s41467-019-10650-x.
Comerci, Colin J., Herrmann, Jonathan, Yoon, Joshua, Jabbarpour, Fatemeh, Zhou, Xiaofeng, Nomellini, John F., Smit, John, Shapiro, Lucy, Wakatsuki, Soichi, and Moerner, W. E. Fri . "Topologically-guided continuous protein crystallization controls bacterial surface layer self-assembly". United States. doi:10.1038/s41467-019-10650-x. https://www.osti.gov/servlets/purl/1546945.
@article{osti_1546945,
title = {Topologically-guided continuous protein crystallization controls bacterial surface layer self-assembly},
author = {Comerci, Colin J. and Herrmann, Jonathan and Yoon, Joshua and Jabbarpour, Fatemeh and Zhou, Xiaofeng and Nomellini, John F. and Smit, John and Shapiro, Lucy and Wakatsuki, Soichi and Moerner, W. E.},
abstractNote = {Many bacteria and most archaea possess a crystalline protein surface layer (S-layer), which surrounds their growing and topologically complicated outer surface. Constructing a macromolecular structure of this scale generally requires localized enzymatic machinery, but a regulatory framework for S-layer assembly has not been identified. By labeling, superresolution imaging, and tracking the S-layer protein (SLP) from C. crescentus, we show that 2D protein self-assembly is sufficient to build and maintain the S-layer in living cells by efficient protein crystal nucleation and growth. We propose a model supported by single-molecule tracking whereby randomly secreted SLP monomers diffuse on the lipopolysaccharide (LPS) outer membrane until incorporated at the edges of growing 2D S-layer crystals. Surface topology creates crystal defects and boundaries, thereby guiding S-layer assembly. Unsupervised assembly poses challenges for therapeutics targeting S-layers. However, protein crystallization as an evolutionary driver rationalizes S-layer diversity and raises the potential for biologically inspired self-assembling macromolecular nanomaterials.},
doi = {10.1038/s41467-019-10650-x},
journal = {Nature Communications},
number = 1,
volume = 10,
place = {United States},
year = {2019},
month = {6}
}

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