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

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.

doi:10.1038/s41467-018-05255-9

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

Journal Article · 19 July 2018 · Nature Communications

DOI: https://doi.org/10.1038/s41467-018-05255-9 · OSTI ID:1570630

^[1]; Duncan, Anna L. ^[2]; Rassam, Patrice ^[3];

^[4];

^[5];

^[2]; Beliaev, Dmitry ^[6]; Hambly, Ben ^[7];

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^[2];

^[2]

Univ. of Oxford (United Kingdom); Univ. de Toulouse, Toulouse (France)
Univ. of Oxford (United Kingdom)
Univ. of Oxford (United Kingdom); Univ. de Strasbourg, Illkirch (France)
Univ. of Osnabrück, Osnabrück (Germany)
Univ. of Oxford (United Kingdom); SEMMLE, Oxford (United Kingdom)
Univ. of Oxford (United Kingdom); Radcliffe Observatory Quarter (550), Oxford (United Kingdom)
Radcliffe Observatory Quarter (550), Oxford (United Kingdom)
Univ. of Osnabrück, Barbarastraße (Osnabrück)

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.

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Research Organization:: Los Alamos National Lab. (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: LDRD; USDOE

Grant/Contract Number:: 89233218CNA000001

OSTI ID:: 1570630

Report Number(s):: LA-UR--19-29545

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 9; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (72)

LINCS: A linear constraint solver for molecular simulations Hess, Berk; Bekker, Henk; Berendsen, Herman J. C. Journal of Computational Chemistry, Vol. 18, Issue 12 https://doi.org/10.1002/(SICI)1096-987X(199709)18:12<1463::AID-JCC4>3.0.CO;2-H	journal	September 1997
g_membed: Efficient insertion of a membrane protein into an equilibrated lipid bilayer with minimal perturbation Wolf, Maarten G.; Hoefling, Martin; Aponte-Santamaría, Camilo Journal of Computational Chemistry, Vol. 31, Issue 11 https://doi.org/10.1002/jcc.21507	journal	March 2010
CHARMM-GUI Martini Maker for modeling and simulation of complex bacterial membranes with lipopolysaccharides Hsu, Pin-Chia; Bruininks, Bart M. H.; Jefferies, Damien Journal of Computational Chemistry, Vol. 38, Issue 27 https://doi.org/10.1002/jcc.24895	journal	August 2017
Electrostatic rate enhancement and transient complex of protein–protein association Alsallaq, Ramzi; Zhou, Huan-Xiang Proteins: Structure, Function, and Bioinformatics, Vol. 71, Issue 1 https://doi.org/10.1002/prot.21679	journal	January 2008
VMD: Visual molecular dynamics Humphrey, William; Dalke, Andrew; Schulten, Klaus Journal of Molecular Graphics, Vol. 14, Issue 1 https://doi.org/10.1016/0263-7855(96)00018-5	journal	February 1996
A mutant of Escherichia coli defective in the first step of endotoxin biosynthesis. Galloway, S. M.; Raetz, C. R. Journal of Biological Chemistry, Vol. 265, Issue 11 https://doi.org/10.1016/S0021-9258(19)39339-1	journal	April 1990
Characterization of the Major Envelope Protein from Escherichia coli Rosenbusch, Jurg P. Journal of Biological Chemistry, Vol. 249, Issue 24 https://doi.org/10.1016/S0021-9258(19)42066-8	journal	December 1974
A conserved structural motif for lipopolysaccharide recognition by procaryotic and eucaryotic proteins D. Ferguson, Andrew; Welte, Wolfram; Hofmann, Eckhard Structure, Vol. 8, Issue 6 https://doi.org/10.1016/S0969-2126(00)00143-X	journal	June 2000
Lipid interaction sites on channels, transporters and receptors: Recent insights from molecular dynamics simulations Hedger, George; Sansom, Mark S. P. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1858, Issue 10 https://doi.org/10.1016/j.bbamem.2016.02.037	journal	October 2016
Role of the Native Outer-Membrane Environment on the Transporter BtuB Balusek, Curtis; Gumbart, James C. Biophysical Journal, Vol. 111, Issue 7 https://doi.org/10.1016/j.bpj.2016.08.033	journal	October 2016
Quantifying Absolute Protein Synthesis Rates Reveals Principles Underlying Allocation of Cellular Resources Li, Gene-Wei; Burkhardt, David; Gross, Carol Cell, Vol. 157, Issue 3 https://doi.org/10.1016/j.cell.2014.02.033	journal	April 2014
Supramolecular Assembly of VDAC in Native Mitochondrial Outer Membranes Gonçalves, Rui Pedro; Buzhynskyy, Nikolay; Prima, Valérie Journal of Molecular Biology, Vol. 369, Issue 2 https://doi.org/10.1016/j.jmb.2007.03.063	journal	June 2007
Protein–protein interactions and the spatiotemporal dynamics of bacterial outer membrane proteins Kleanthous, Colin; Rassam, Patrice; Baumann, Christoph G. Current Opinion in Structural Biology, Vol. 35 https://doi.org/10.1016/j.sbi.2015.10.007	journal	December 2015
Molecular dynamics simulations of membrane proteins and their interactions: from nanoscale to mesoscale Chavent, Matthieu; Duncan, Anna L.; Sansom, Mark SP Current Opinion in Structural Biology, Vol. 40 https://doi.org/10.1016/j.sbi.2016.06.007	journal	October 2016
Hierarchical mesoscale domain organization of the plasma membrane Kusumi, Akihiro; Suzuki, Kenichi G. N.; Kasai, Rinshi S. Trends in Biochemical Sciences, Vol. 36, Issue 11 https://doi.org/10.1016/j.tibs.2011.08.001	journal	November 2011
Reconstitution of Membrane Proteins into Polymer-Supported Membranes for Probing Diffusion and Interactions by Single Molecule Techniques Roder, Friedrich; Waichman, Sharon; Paterok, Dirk Analytical Chemistry, Vol. 83, Issue 17 https://doi.org/10.1021/ac201294v	journal	September 2011
Manipulation and Motion of Organelles and Single Molecules in Living Cells Norregaard, Kamilla; Metzler, Ralf; Ritter, Christine M. Chemical Reviews, Vol. 117, Issue 5 https://doi.org/10.1021/acs.chemrev.6b00638	journal	February 2017
Divergent Diffusion Coefficients in Simulations of Fluids and Lipid Membranes Vögele, Martin; Hummer, Gerhard The Journal of Physical Chemistry B, Vol. 120, Issue 33 https://doi.org/10.1021/acs.jpcb.6b05102	journal	May 2016
It Is Complicated: Curvature, Diffusion, and Lipid Sorting within the Two Membranes of Escherichia coli Hsu, Pin-Chia; Samsudin, Firdaus; Shearer, Jonathan The Journal of Physical Chemistry Letters, Vol. 8, Issue 22 https://doi.org/10.1021/acs.jpclett.7b02432	journal	October 2017
Glasslike Membrane Protein Diffusion in a Crowded Membrane Munguira, Ignacio; Casuso, Ignacio; Takahashi, Hirohide ACS Nano, Vol. 10, Issue 2 https://doi.org/10.1021/acsnano.5b07595	journal	January 2016
Improved Parameters for the Martini Coarse-Grained Protein Force Field de Jong, Djurre H.; Singh, Gurpreet; Bennett, W. F. Drew Journal of Chemical Theory and Computation, Vol. 9, Issue 1 https://doi.org/10.1021/ct300646g	journal	November 2012
GROMACS 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation Hess, Berk; Kutzner, Carsten; van der Spoel, David Journal of Chemical Theory and Computation, Vol. 4, Issue 3 https://doi.org/10.1021/ct700301q	journal	February 2008
The MARTINI Coarse-Grained Force Field: Extension to Proteins Monticelli, Luca; Kandasamy, Senthil K.; Periole, Xavier Journal of Chemical Theory and Computation, Vol. 4, Issue 5 https://doi.org/10.1021/ct700324x	journal	April 2008
Combining an Elastic Network With a Coarse-Grained Molecular Force Field: Structure, Dynamics, and Intermolecular Recognition Periole, Xavier; Cavalli, Marco; Marrink, Siewert-Jan Journal of Chemical Theory and Computation, Vol. 5, Issue 9 https://doi.org/10.1021/ct9002114	journal	August 2009
Membrane Proteins Diffuse as Dynamic Complexes with Lipids Niemelä, Perttu S.; Miettinen, Markus S.; Monticelli, Luca Journal of the American Chemical Society, Vol. 132, Issue 22 https://doi.org/10.1021/ja101481b	journal	June 2010
Lateral Diffusion of Membrane Proteins Ramadurai, Sivaramakrishnan; Holt, Andrea; Krasnikov, Victor Journal of the American Chemical Society, Vol. 131, Issue 35 https://doi.org/10.1021/ja902853g	journal	September 2009
Organization and Dynamics of Receptor Proteins in a Plasma Membrane Koldsø, Heidi; Sansom, Mark S. P. Journal of the American Chemical Society, Vol. 137, Issue 46 https://doi.org/10.1021/jacs.5b08048	journal	November 2015
The MARTINI Force Field: Coarse Grained Model for Biomolecular Simulations Marrink, Siewert J.; Risselada, H. Jelger; Yefimov, Serge The Journal of Physical Chemistry B, Vol. 111, Issue 27 https://doi.org/10.1021/jp071097f	journal	July 2007
Direct observation of the nanoscale dynamics of membrane lipids in a living cell Eggeling, Christian; Ringemann, Christian; Medda, Rebecca Nature, Vol. 457, Issue 7233 https://doi.org/10.1038/nature07596	journal	December 2008
Membrane protein sequestering by ionic protein–lipid interactions van den Bogaart, Geert; Meyenberg, Karsten; Risselada, H. Jelger Nature, Vol. 479, Issue 7374 https://doi.org/10.1038/nature10545	journal	October 2011
Supramolecular assemblies underpin turnover of outer membrane proteins in bacteria Rassam, Patrice; Copeland, Nikki A.; Birkholz, Oliver Nature, Vol. 523, Issue 7560 https://doi.org/10.1038/nature14461	journal	June 2015
Structural basis of outer membrane protein insertion by the BAM complex Gu, Yinghong; Li, Huanyu; Dong, Haohao Nature, Vol. 531, Issue 7592 https://doi.org/10.1038/nature17199	journal	February 2016
Multi-protein assemblies underlie the mesoscale organization of the plasma membrane Saka, Sinem K.; Honigmann, Alf; Eggeling, Christian Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5509	journal	July 2014
Dynamic multiple-target tracing to probe spatiotemporal cartography of cell membranes Sergé, Arnauld; Bertaux, Nicolas; Rigneault, Hervé Nature Methods, Vol. 5, Issue 8 https://doi.org/10.1038/nmeth.1233	journal	July 2008
NIH Image to ImageJ: 25 years of image analysis Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W. Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2089	journal	June 2012
Characterization of the motion of membrane proteins using high-speed atomic force microscopy Casuso, Ignacio; Khao, Jonathan; Chami, Mohamed Nature Nanotechnology, Vol. 7, Issue 8 https://doi.org/10.1038/nnano.2012.109	journal	July 2012
Intermembrane crosstalk drives inner-membrane protein organization in Escherichia coli Rassam, Patrice; Long, Kathleen R.; Kaminska, Renata Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-03521-4	journal	March 2018
Protein crowding and lipid complexity influence the nanoscale dynamic organization of ion channels in cell membranes Duncan, Anna L.; Reddy, Tyler; Koldsø, Heidi Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-16865-6	journal	November 2017
CASSPER is a semantic segmentation-based particle picking algorithm for single-particle cryo-electron microscopy George, Blesson; Assaiya, Anshul; Roy, Robin J. Communications Biology, Vol. 4, Issue 1 https://doi.org/10.1038/s42003-021-01721-1	journal	February 2021
Anomalous and normal diffusion of proteins and lipids in crowded lipid membranes Javanainen, Matti; Hammaren, Henrik; Monticelli, Luca Faraday Discuss., Vol. 161 https://doi.org/10.1039/C2FD20085F	journal	January 2013
Membrane stiffness is modified by integral membrane proteins Fowler, Philip W.; Hélie, Jean; Duncan, Anna Soft Matter, Vol. 12, Issue 37 https://doi.org/10.1039/C6SM01186A	journal	January 2016
Perspective on the Martini model Marrink, Siewert J.; Tieleman, D. Peter Chemical Society Reviews, Vol. 42, Issue 16 https://doi.org/10.1039/c3cs60093a	journal	January 2013
Dynamical motions of lipids and a finite size effect in simulations of bilayers Klauda, Jeffery B.; Brooks, Bernard R.; Pastor, Richard W. The Journal of Chemical Physics, Vol. 125, Issue 14 https://doi.org/10.1063/1.2354486	journal	October 2006
Molecular dynamics with coupling to an external bath Berendsen, H. J. C.; Postma, J. P. M.; van Gunsteren, W. F. The Journal of Chemical Physics, Vol. 81, Issue 8 https://doi.org/10.1063/1.448118	journal	October 1984
Protein area occupancy at the center of the red blood cell membrane Dupuy, A. D.; Engelman, D. M. Proceedings of the National Academy of Sciences, Vol. 105, Issue 8 https://doi.org/10.1073/pnas.0712379105	journal	February 2008
Organization, dynamics, and segregation of Ras nanoclusters in membrane domains Janosi, L.; Li, Z.; Hancock, J. F. Proceedings of the National Academy of Sciences, Vol. 109, Issue 21 https://doi.org/10.1073/pnas.1200773109	journal	May 2012
Single-molecule imaging of the functional crosstalk between surface NMDA and dopamine D1 receptors Ladepeche, L.; Dupuis, J. P.; Bouchet, D. Proceedings of the National Academy of Sciences, Vol. 110, Issue 44 https://doi.org/10.1073/pnas.1310145110	journal	October 2013
The source of high signal cooperativity in bacterial chemosensory arrays Piñas, Germán E.; Frank, Vered; Vaknin, Ady Proceedings of the National Academy of Sciences, Vol. 113, Issue 12 https://doi.org/10.1073/pnas.1600216113	journal	March 2016
A Peptidomimetic Antibiotic Targets Outer Membrane Proteins and Disrupts Selectively the Outer Membrane in Escherichia coli Urfer, Matthias; Bogdanovic, Jasmina; Lo Monte, Fabio Journal of Biological Chemistry, Vol. 291, Issue 4 https://doi.org/10.1074/jbc.M115.691725	journal	December 2015
Receptor dimerization dynamics as a regulatory valve for plasticity of type I interferon signaling Wilmes, Stephan; Beutel, Oliver; Li, Zhi The Journal of Cell Biology, Vol. 209, Issue 4 https://doi.org/10.1083/jcb.201412049	journal	May 2015
Confined diffusion of transmembrane proteins and lipids induced by the same actin meshwork lining the plasma membrane Fujiwara, Takahiro K.; Iwasawa, Kokoro; Kalay, Ziya Molecular Biology of the Cell, Vol. 27, Issue 7 https://doi.org/10.1091/mbc.e15-04-0186	journal	April 2016
Matplotlib: A 2D Graphics Environment Hunter, John D. Computing in Science & Engineering, Vol. 9, Issue 3 https://doi.org/10.1109/MCSE.2007.55	journal	January 2007
The NumPy Array: A Structure for Efficient Numerical Computation van der Walt, Stéfan; Colbert, S. Chris; Varoquaux, Gaël Computing in Science & Engineering, Vol. 13, Issue 2 https://doi.org/10.1109/MCSE.2011.37	journal	March 2011
Modeling of loops in protein structures Fiser, András; Do, Richard Kinh Gian; Šali, Andrej Protein Science, Vol. 9, Issue 9 https://doi.org/10.1110/ps.9.9.1753	journal	January 2000
HIV-1 Assembly Differentially Alters Dynamics and Partitioning of Tetraspanins and Raft Components Krementsov, Dimitry N.; Rassam, Patrice; Margeat, Emmanuel Traffic, Vol. 11, Issue 11 https://doi.org/10.1111/j.1600-0854.2010.01111.x	journal	September 2010
Biased partitioning of the multidrug efflux pump AcrAB-TolC underlies long-lived phenotypic heterogeneity Bergmiller, Tobias; Andersson, Anna M. C.; Tomasek, Kathrin Science, Vol. 356, Issue 6335 https://doi.org/10.1126/science.aaf4762	journal	April 2017
Outer membrane of Salmonella typhimurium: chemical analysis and freeze-fracture studies with lipopolysaccharide mutants. Smit, J.; Kamio, Y.; Nikaido, H. Journal of Bacteriology, Vol. 124, Issue 2 https://doi.org/10.1128/JB.124.2.942-958.1975	journal	January 1975
Outer membrane of gram-negative bacteria. XVIII. Electron microscopic studies on porin insertion sites and growth of cell surface of Salmonella typhimurium. Smit, J.; Nikaido, H. Journal of Bacteriology, Vol. 135, Issue 2 https://doi.org/10.1128/JB.135.2.687-702.1978	journal	January 1978
Molecular Basis of Bacterial Outer Membrane Permeability Revisited Nikaido, H. Microbiology and Molecular Biology Reviews, Vol. 67, Issue 4 https://doi.org/10.1128/MMBR.67.4.593-656.2003	journal	December 2003
Outer membrane of Salmonella typhimurium: chemical analysis and freeze-fracture studies with lipopolysaccharide mutants. Smit, J.; Kamio, Y.; Nikaido, H. Journal of Bacteriology, Vol. 124, Issue 2 https://doi.org/10.1128/jb.124.2.942-958.1975	journal	January 1975
Outer membrane of gram-negative bacteria. XVIII. Electron microscopic studies on porin insertion sites and growth of cell surface of Salmonella typhimurium. Smit, J.; Nikaido, H. Journal of Bacteriology, Vol. 135, Issue 2 https://doi.org/10.1128/jb.135.2.687-702.1978	journal	January 1978
Lipopolysaccharide Endotoxins Raetz, Christian R. H.; Whitfield, Chris Annual Review of Biochemistry, Vol. 71, Issue 1 https://doi.org/10.1146/annurev.biochem.71.110601.135414	journal	June 2002
Automatic detection of diffusion modes within biological membranes using back-propagation neural network Dosset, Patrice; Rassam, Patrice; Fernandez, Laurent BMC Bioinformatics, Vol. 17, Issue 1 https://doi.org/10.1186/s12859-016-1064-z	journal	May 2016
Computational ‘microscopy’ of cellular membranes Ingólfsson, Helgi I.; Arnarez, Clément; Periole, Xavier Journal of Cell Science, Vol. 129, Issue 2 https://doi.org/10.1242/jcs.176040	journal	January 2016
Analysis of Surface Protein Expression Reveals the Growth Pattern of the Gram-Negative Outer Membrane Ursell, Tristan S.; Trepagnier, Eliane H.; Huang, Kerwyn Casey PLoS Computational Biology, Vol. 8, Issue 9 https://doi.org/10.1371/journal.pcbi.1002680	journal	September 2012
Reduced Lateral Mobility of Lipids and Proteins in Crowded Membranes Goose, Joseph E.; Sansom, Mark S. P. PLoS Computational Biology, Vol. 9, Issue 4 https://doi.org/10.1371/journal.pcbi.1003033	journal	April 2013
The Free Energy Landscape of Dimerization of a Membrane Protein, NanC Dunton, Thomas A.; Goose, Joseph E.; Gavaghan, David J. PLoS Computational Biology, Vol. 10, Issue 1 https://doi.org/10.1371/journal.pcbi.1003417	journal	January 2014
Lipid Clustering Correlates with Membrane Curvature as Revealed by Molecular Simulations of Complex Lipid Bilayers Koldsø, Heidi; Shorthouse, David; Hélie, Jean PLoS Computational Biology, Vol. 10, Issue 10 https://doi.org/10.1371/journal.pcbi.1003911	journal	October 2014
Dynamics of Crowded Vesicles: Local and Global Responses to Membrane Composition Holdbrook, Daniel A.; Huber, Roland G.; Piggot, Thomas J. PLOS ONE, Vol. 11, Issue 6 https://doi.org/10.1371/journal.pone.0156963	journal	June 2016
Confined diffusion of transmembrane proteins and lipids induced by the same actin meshwork lining the plasma membrane. Fujiwara, Takahiro K.; Iwasawa, Kokoro; Kalay, Ziya Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.40317	text	January 2016
A peptidomimetic antibiotic targets outer membrane proteins and disrupts selectively the outer membrane in Escherichia coli Urfer, Matthias; Bogdanovic, Jasmina; Lo Monte, Fabio American Society for Biochemistry and Molecular Biology https://doi.org/10.5167/uzh-120740	text	January 2016
Automatic detection of diffusion modes within biological membranes using back-propagation neural network Dosset, Patrice; Rassam, Patrice; Fernandez, Laurent Figshare https://doi.org/10.6084/m9.figshare.c.3633032.v1	collection	January 2016

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