DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

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:
; ; ; ; ; ; ORCiD logo; ; ORCiD logo; ORCiD logo
Publication Date:
Research Org.:
SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1619527
Alternate Identifier(s):
OSTI ID: 1546945; OSTI ID: 1608960
Grant/Contract Number:  
AC02-76SF00515; R35-GM118067; R35-GM118071
Resource Type:
Published Article
Journal Name:
Nature Communications
Additional Journal Information:
Journal Name: Nature Communications Journal Volume: 10 Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United Kingdom
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 Kingdom: 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 Kingdom. https://doi.org/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 Kingdom. https://doi.org/10.1038/s41467-019-10650-x.
@article{osti_1619527,
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 Kingdom},
year = {2019},
month = {6}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1038/s41467-019-10650-x

Citation Metrics:
Cited by: 20 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Factors controlling in vitro recrystallization of the Caulobacter crescentus paracrystalline S-layer.
journal, October 1997


Analysis of the Intact Surface Layer of Caulobacter crescentus by Cryo-Electron Tomography
journal, September 2010

  • Amat, F.; Comolli, L. R.; Nomellini, J. F.
  • Journal of Bacteriology, Vol. 192, Issue 22
  • DOI: 10.1128/JB.00747-10

S-Layer Anchoring and Localization of an S-Layer-Associated Protease in Caulobacter crescentus
journal, January 2007

  • Ford, M. J.; Nomellini, J. F.; Smit, J.
  • Journal of Bacteriology, Vol. 189, Issue 6
  • DOI: 10.1128/JB.01690-06

MreB Actin-Mediated Segregation of a Specific Region of a Bacterial Chromosome
journal, February 2005


S-Layer Protein Self-Assembly
journal, January 2013

  • Pum, Dietmar; Toca-Herrera, Jose; Sleytr, Uwe
  • International Journal of Molecular Sciences, Vol. 14, Issue 2
  • DOI: 10.3390/ijms14022484

Ion-Specific Control of the Self-Assembly Dynamics of a Nanostructured Protein Lattice
journal, December 2014

  • Rad, Behzad; Haxton, Thomas K.; Shon, Albert
  • ACS Nano, Vol. 9, Issue 1
  • DOI: 10.1021/nn502992x

Host cell invasion and intracellular residence by Aeromonas salmonicida : Role of the S-layer
journal, July 2000

  • Garduño, Rafael A.; Moore, Anne R.; Olivier, Gilles
  • Canadian Journal of Microbiology, Vol. 46, Issue 7
  • DOI: 10.1139/w00-034

Revealing Nanoscale Morphology of the Primary Cilium Using Super-Resolution Fluorescence Microscopy
journal, January 2019


Environmental Calcium Controls Alternate Physical States of the Caulobacter Surface Layer
journal, May 2017

  • Herrmann, Jonathan; Jabbarpour, Fatemeh; Bargar, Paul G.
  • Biophysical Journal, Vol. 112, Issue 9
  • DOI: 10.1016/j.bpj.2017.04.003

Proteins evolve on the edge of supramolecular self-assembly
journal, August 2017

  • Garcia-Seisdedos, Hector; Empereur-Mot, Charly; Elad, Nadav
  • Nature, Vol. 548, Issue 7666
  • DOI: 10.1038/nature23320

The tubulin homologue FtsZ contributes to cell elongation by guiding cell wall precursor synthesis in Caulobacter crescentus
journal, May 2007


Helical Disposition of Proteins and Lipopolysaccharide in the Outer Membrane of Escherichia coli
journal, March 2005


Cell‐surface display of a Pseudomonas aeruginosa strain K pilin peptide within the paracrystalline S‐layer of Caulobacter crescentus
journal, October 1997


The core and O-polysaccharide structure of the Caulobacter crescentus lipopolysaccharide
journal, January 2015


SbsB structure and lattice reconstruction unveil Ca2+ triggered S-layer assembly
journal, June 2012

  • Baranova, Ekaterina; Fronzes, Rémi; Garcia-Pino, Abel
  • Nature, Vol. 487, Issue 7405
  • DOI: 10.1038/nature11155

Characterization of mutants of Caulobacter crescentus defective in surface attachment of the paracrystalline surface layer.
journal, October 1994


BslA, the S-layer adhesin of B. anthracis , is a virulence factor for anthrax pathogenesis
journal, January 2010


Engineering the S-Layer of Caulobacter crescentus as a Foundation for Stable, High-Density, 2D Living Materials
journal, December 2018


Self-catalyzed growth of S layers via an amorphous-to-crystalline transition limited by folding kinetics
journal, September 2010

  • Chung, S.; Shin, S. -H.; Bertozzi, C. R.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 38
  • DOI: 10.1073/pnas.1008280107

Diversity in S-layers
journal, January 2017


The archaeal cell envelope
journal, May 2011

  • Albers, Sonja-Verena; Meyer, Benjamin H.
  • Nature Reviews Microbiology, Vol. 9, Issue 6
  • DOI: 10.1038/nrmicro2576

Structural basis of cell wall anchoring by SLH domains in Paenibacillus alvei
journal, August 2018

  • Blackler, Ryan J.; López-Guzmán, Arturo; Hager, Fiona F.
  • Nature Communications, Vol. 9, Issue 1
  • DOI: 10.1038/s41467-018-05471-3

Characteristics of the Clostridium difficile cell envelope and its importance in therapeutics
journal, June 2016

  • Kirk, Joseph A.; Banerji, Oishik; Fagan, Robert P.
  • Microbial Biotechnology, Vol. 10, Issue 1
  • DOI: 10.1111/1751-7915.12372

A Novel Periplasmic Protein, VrpA, Contributes to Efficient Protein Secretion by the Type III Secretion System in Xanthomonas spp.
journal, February 2015

  • Zhou, Xiaofeng; Hu, Xiufang; Li, Jinyun
  • Molecular Plant-Microbe Interactions, Vol. 28, Issue 2
  • DOI: 10.1094/MPMI-10-14-0309-R

S-layers: principles and applications
journal, September 2014

  • Sleytr, Uwe B.; Schuster, Bernhard; Egelseer, Eva-Maria
  • FEMS Microbiology Reviews, Vol. 38, Issue 5
  • DOI: 10.1111/1574-6976.12063

Regulation of bacterial cell wall growth
journal, November 2016

  • Egan, Alexander J. F.; Cleverley, Robert M.; Peters, Katharina
  • The FEBS Journal, Vol. 284, Issue 6
  • DOI: 10.1111/febs.13959

Structure of the hexagonal surface layer on Caulobacter crescentus cells
journal, April 2017

  • Bharat, Tanmay A. M.; Kureisaite-Ciziene, Danguole; Hardy, Gail G.
  • Nature Microbiology, Vol. 2, Issue 7
  • DOI: 10.1038/nmicrobiol.2017.59

Nutrient transport suggests an evolutionary basis for charged archaeal surface layer proteins
journal, June 2018


Super-resolution Imaging of Live Bacteria Cells Using a Genetically Directed, Highly Photostable Fluoromodule
journal, August 2016

  • Saurabh, Saumya; Perez, Adam M.; Comerci, Colin J.
  • Journal of the American Chemical Society, Vol. 138, Issue 33
  • DOI: 10.1021/jacs.6b05943

MeshLab: an Open-Source Mesh Processing Tool
null, January 2008


Three-Dimensional Localization of Single Molecules for Super-Resolution Imaging and Single-Particle Tracking
journal, February 2017


Small-Molecule Labeling of Live Cell Surfaces for Three-Dimensional Super-Resolution Microscopy
journal, August 2014

  • Lee, Marissa K.; Rai, Prabin; Williams, Jarrod
  • Journal of the American Chemical Society, Vol. 136, Issue 40
  • DOI: 10.1021/ja508028h

Self-assembly of coherently dynamic, auxetic, two-dimensional protein crystals
journal, May 2016

  • Suzuki, Yuta; Cardone, Giovanni; Restrepo, David
  • Nature, Vol. 533, Issue 7603
  • DOI: 10.1038/nature17633

Easy-DHPSF open-source software for three-dimensional localization of single molecules with precision beyond the optical diffraction limit
journal, February 2013


Isolation and comparison of the paracrystalline surface layer proteins of freshwater caulobacters.
journal, March 1992


Spatial gradient of protein phosphorylation underlies replicative asymmetry in a bacterium
journal, December 2010

  • Chen, Y. E.; Tropini, C.; Jonas, K.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 3
  • DOI: 10.1073/pnas.1015397108

Crystallization dynamics on curved surfaces
journal, July 2013