Dynamics of Crowded Vesicles: Local and Global Responses to Membrane Composition.

The bacterial cell envelope is composed of a mixture of different lipids and proteins, making it an inherently complex organelle. The interactions between integral membrane proteins and lipids are crucial for their respective spatial localization within bacterial cells. We have employed microsecond...

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Main Authors: Daniel A Holdbrook, Roland G Huber, Thomas J Piggot, Peter J Bond, Syma Khalid
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2016-01-01
Series:PLoS ONE
Online Access:https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0156963&type=printable
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author Daniel A Holdbrook
Roland G Huber
Thomas J Piggot
Peter J Bond
Syma Khalid
author_facet Daniel A Holdbrook
Roland G Huber
Thomas J Piggot
Peter J Bond
Syma Khalid
author_sort Daniel A Holdbrook
collection DOAJ
description The bacterial cell envelope is composed of a mixture of different lipids and proteins, making it an inherently complex organelle. The interactions between integral membrane proteins and lipids are crucial for their respective spatial localization within bacterial cells. We have employed microsecond timescale coarse-grained molecular dynamics simulations of vesicles of varying sizes and with a range of protein and lipid compositions, and used novel approaches to measure both local and global system dynamics, the latter based on spherical harmonics analysis. Our results suggest that both hydrophobic mismatch, enhanced by embedded membrane proteins, and curvature based sorting, due to different modes of undulation, may drive assembly in vesicular systems. Interestingly, the modes of undulation of the vesicles were found to be altered by the specific protein and lipid composition of the vesicle. Strikingly, lipid dynamics were shown to be coupled to proteins up to 6 nm from their surface, a substantially larger distance than has previously been observed, resulting in multi-layered annular rings enriched with particular types of phospholipid. Such large protein-lipid complexes may provide a mechanism for long-range communication. Given the complexity of bacterial membranes, our results suggest that subtle changes in lipid composition may have major implications for lipid and protein sorting under a curvature-based membrane-sorting model.
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spelling doaj-art-4cfdf16ae40b4305a5cf9c66318322d22025-08-20T03:24:29ZengPublic Library of Science (PLoS)PLoS ONE1932-62032016-01-01116e015696310.1371/journal.pone.0156963Dynamics of Crowded Vesicles: Local and Global Responses to Membrane Composition.Daniel A HoldbrookRoland G HuberThomas J PiggotPeter J BondSyma KhalidThe bacterial cell envelope is composed of a mixture of different lipids and proteins, making it an inherently complex organelle. The interactions between integral membrane proteins and lipids are crucial for their respective spatial localization within bacterial cells. We have employed microsecond timescale coarse-grained molecular dynamics simulations of vesicles of varying sizes and with a range of protein and lipid compositions, and used novel approaches to measure both local and global system dynamics, the latter based on spherical harmonics analysis. Our results suggest that both hydrophobic mismatch, enhanced by embedded membrane proteins, and curvature based sorting, due to different modes of undulation, may drive assembly in vesicular systems. Interestingly, the modes of undulation of the vesicles were found to be altered by the specific protein and lipid composition of the vesicle. Strikingly, lipid dynamics were shown to be coupled to proteins up to 6 nm from their surface, a substantially larger distance than has previously been observed, resulting in multi-layered annular rings enriched with particular types of phospholipid. Such large protein-lipid complexes may provide a mechanism for long-range communication. Given the complexity of bacterial membranes, our results suggest that subtle changes in lipid composition may have major implications for lipid and protein sorting under a curvature-based membrane-sorting model.https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0156963&type=printable
spellingShingle Daniel A Holdbrook
Roland G Huber
Thomas J Piggot
Peter J Bond
Syma Khalid
Dynamics of Crowded Vesicles: Local and Global Responses to Membrane Composition.
PLoS ONE
title Dynamics of Crowded Vesicles: Local and Global Responses to Membrane Composition.
title_full Dynamics of Crowded Vesicles: Local and Global Responses to Membrane Composition.
title_fullStr Dynamics of Crowded Vesicles: Local and Global Responses to Membrane Composition.
title_full_unstemmed Dynamics of Crowded Vesicles: Local and Global Responses to Membrane Composition.
title_short Dynamics of Crowded Vesicles: Local and Global Responses to Membrane Composition.
title_sort dynamics of crowded vesicles local and global responses to membrane composition
url https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0156963&type=printable
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AT thomasjpiggot dynamicsofcrowdedvesicleslocalandglobalresponsestomembranecomposition
AT peterjbond dynamicsofcrowdedvesicleslocalandglobalresponsestomembranecomposition
AT symakhalid dynamicsofcrowdedvesicleslocalandglobalresponsestomembranecomposition