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Title: How nanoscale protein interactions determine the mesoscale dynamic organisation of bacterial outer membrane proteins

Abstract

The spatiotemporal organisation of membranes is often characterised by the formation of large protein clusters. In Escherichia coli, outer membrane protein (OMP) clustering leads to OMP islands, the formation of which underpins OMP turnover and drives organisation across the cell envelope. Modelling how OMP islands form in order to understand their origin and outer membrane behaviour has been confounded by the inherent difficulties of simulating large numbers of OMPs over meaningful timescales. Here, we overcome these problems by training a mesoscale model incorporating thousands of OMPs on coarse-grained molecular dynamics simulations. We achieve simulations over timescales that allow direct comparison to experimental data of OMP behaviour. Here, we show that specific interaction surfaces between OMPs are key to the formation of OMP clusters, that OMP clusters present a mesh of moving barriers that confine newly inserted proteins within islands, and that mesoscale simulations recapitulate the restricted diffusion characteristics of OMPs.

Authors:
ORCiD logo [1];  [2];  [3]; ORCiD logo [4]; ORCiD logo [5]; ORCiD logo [2];  [6];  [7]; ORCiD logo [8]; ORCiD logo [2]; ORCiD logo [2]
  1. Univ. of Oxford (United Kingdom); Univ. de Toulouse, Toulouse (France)
  2. Univ. of Oxford (United Kingdom)
  3. Univ. of Oxford (United Kingdom); Univ. de Strasbourg, Illkirch (France)
  4. Univ. of Osnabrück, Osnabrück (Germany)
  5. Univ. of Oxford (United Kingdom); SEMMLE, Oxford (United Kingdom)
  6. Univ. of Oxford (United Kingdom); Radcliffe Observatory Quarter (550), Oxford (United Kingdom)
  7. Radcliffe Observatory Quarter (550), Oxford (United Kingdom)
  8. Univ. of Osnabrück, Barbarastraße (Osnabrück)
Publication Date:
Research Org.:
Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
USDOE Laboratory Directed Research and Development (LDRD) Program
OSTI Identifier:
1570630
Report Number(s):
LA-UR-19-29545
Journal ID: ISSN 2041-1723
Grant/Contract Number:  
89233218CNA000001
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 9; 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

Chavent, Matthieu, Duncan, Anna L., Rassam, Patrice, Birkholz, Oliver, Hélie, Jean, Reddy, Tyler John Edward, Beliaev, Dmitry, Hambly, Ben, Piehler, Jacob, Kleanthous, Colin, and Sansom, Mark S. P. How nanoscale protein interactions determine the mesoscale dynamic organisation of bacterial outer membrane proteins. United States: N. p., 2018. Web. doi:10.1038/s41467-018-05255-9.
Chavent, Matthieu, Duncan, Anna L., Rassam, Patrice, Birkholz, Oliver, Hélie, Jean, Reddy, Tyler John Edward, Beliaev, Dmitry, Hambly, Ben, Piehler, Jacob, Kleanthous, Colin, & Sansom, Mark S. P. How nanoscale protein interactions determine the mesoscale dynamic organisation of bacterial outer membrane proteins. United States. doi:https://doi.org/10.1038/s41467-018-05255-9
Chavent, Matthieu, Duncan, Anna L., Rassam, Patrice, Birkholz, Oliver, Hélie, Jean, Reddy, Tyler John Edward, Beliaev, Dmitry, Hambly, Ben, Piehler, Jacob, Kleanthous, Colin, and Sansom, Mark S. P. Fri . "How nanoscale protein interactions determine the mesoscale dynamic organisation of bacterial outer membrane proteins". United States. doi:https://doi.org/10.1038/s41467-018-05255-9. https://www.osti.gov/servlets/purl/1570630.
@article{osti_1570630,
title = {How nanoscale protein interactions determine the mesoscale dynamic organisation of bacterial outer membrane proteins},
author = {Chavent, Matthieu and Duncan, Anna L. and Rassam, Patrice and Birkholz, Oliver and Hélie, Jean and Reddy, Tyler John Edward and Beliaev, Dmitry and Hambly, Ben and Piehler, Jacob and Kleanthous, Colin and Sansom, Mark S. P.},
abstractNote = {The spatiotemporal organisation of membranes is often characterised by the formation of large protein clusters. In Escherichia coli, outer membrane protein (OMP) clustering leads to OMP islands, the formation of which underpins OMP turnover and drives organisation across the cell envelope. Modelling how OMP islands form in order to understand their origin and outer membrane behaviour has been confounded by the inherent difficulties of simulating large numbers of OMPs over meaningful timescales. Here, we overcome these problems by training a mesoscale model incorporating thousands of OMPs on coarse-grained molecular dynamics simulations. We achieve simulations over timescales that allow direct comparison to experimental data of OMP behaviour. Here, we show that specific interaction surfaces between OMPs are key to the formation of OMP clusters, that OMP clusters present a mesh of moving barriers that confine newly inserted proteins within islands, and that mesoscale simulations recapitulate the restricted diffusion characteristics of OMPs.},
doi = {10.1038/s41467-018-05255-9},
journal = {Nature Communications},
number = 1,
volume = 9,
place = {United States},
year = {2018},
month = {7}
}

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Cited by: 20 works
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Figures / Tables:

Fig. 1 Fig. 1: Simulations and experimental observations of OMPs compared. Final snapshots of 20 μs molecular simulations of a 144 molecules of BtuB (green); b 72 molecules of BtuB+ 72 molecules of OmpF (yellow); and c 100 molecules of OmpF in a lipid bilayer (PE:PG 3:1) membrane and simulated at 323more » K. For the OmpF system, the zoomed images (f) illustrate the three main configurations of OmpF association observed in the simulations: tip-to-tip (purple box), base-to-base (green box) and base-to-top (orange box) interactions of adjacent OmpF trimers (see main text and ref. 2). Further simulations demonstrating similar behaviour are shown in Supplementary Fig. 2. Clustering/co-localisation of d BtuB molecules (green and red; overlap in yellow) and of e BtuB (green) and OmpF (purple; overlap in white) molecules in supported bilayers (scale bar = 1 μm). It should be noted that d, e show under-labelled samples (we estimate less than 10% of BtuB molecules are linked to a fluorescent ColE9) in order to enable us to meaningfully distinguish single molecule trajectories« less

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    • DOI: 10.1039/c6sm01186a

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    A Peptidomimetic Antibiotic Targets Outer Membrane Proteins and Disrupts Selectively the Outer Membrane in Escherichia coli
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    Intermembrane crosstalk drives inner-membrane protein organization in Escherichia coli
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    HIV-1 Assembly Differentially Alters Dynamics and Partitioning of Tetraspanins and Raft Components
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      Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.