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Spatio-temporal Remodeling of Functional Membrane Microdomains Organizes the Signaling Networks of a Bacterium

Lipid rafts are membrane microdomains specialized in the regulation of numerous cellular processes related to membrane organization, as diverse as signal transduction, protein sorting, membrane trafficking or pathogen invasion. It has been proposed that this functional diversity would require a hete...

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Autores principales: Schneider, Johannes, Klein, Teresa, Mielich-Süss, Benjamin, Koch, Gudrun, Franke, Christian, Kuipers, Oscar P., Kovács, Ákos T., Sauer, Markus, Lopez, Daniel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4409396/
https://www.ncbi.nlm.nih.gov/pubmed/25909364
http://dx.doi.org/10.1371/journal.pgen.1005140
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author Schneider, Johannes
Klein, Teresa
Mielich-Süss, Benjamin
Koch, Gudrun
Franke, Christian
Kuipers, Oscar P.
Kovács, Ákos T.
Sauer, Markus
Lopez, Daniel
author_facet Schneider, Johannes
Klein, Teresa
Mielich-Süss, Benjamin
Koch, Gudrun
Franke, Christian
Kuipers, Oscar P.
Kovács, Ákos T.
Sauer, Markus
Lopez, Daniel
author_sort Schneider, Johannes
collection PubMed
description Lipid rafts are membrane microdomains specialized in the regulation of numerous cellular processes related to membrane organization, as diverse as signal transduction, protein sorting, membrane trafficking or pathogen invasion. It has been proposed that this functional diversity would require a heterogeneous population of raft domains with varying compositions. However, a mechanism for such diversification is not known. We recently discovered that bacterial membranes organize their signal transduction pathways in functional membrane microdomains (FMMs) that are structurally and functionally similar to the eukaryotic lipid rafts. In this report, we took advantage of the tractability of the prokaryotic model Bacillus subtilis to provide evidence for the coexistence of two distinct families of FMMs in bacterial membranes, displaying a distinctive distribution of proteins specialized in different biological processes. One family of microdomains harbors the scaffolding flotillin protein FloA that selectively tethers proteins specialized in regulating cell envelope turnover and primary metabolism. A second population of microdomains containing the two scaffolding flotillins, FloA and FloT, arises exclusively at later stages of cell growth and specializes in adaptation of cells to stationary phase. Importantly, the diversification of membrane microdomains does not occur arbitrarily. We discovered that bacterial cells control the spatio-temporal remodeling of microdomains by restricting the activation of FloT expression to stationary phase. This regulation ensures a sequential assembly of functionally specialized membrane microdomains to strategically organize signaling networks at the right time during the lifespan of a bacterium.
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spelling pubmed-44093962015-05-12 Spatio-temporal Remodeling of Functional Membrane Microdomains Organizes the Signaling Networks of a Bacterium Schneider, Johannes Klein, Teresa Mielich-Süss, Benjamin Koch, Gudrun Franke, Christian Kuipers, Oscar P. Kovács, Ákos T. Sauer, Markus Lopez, Daniel PLoS Genet Research Article Lipid rafts are membrane microdomains specialized in the regulation of numerous cellular processes related to membrane organization, as diverse as signal transduction, protein sorting, membrane trafficking or pathogen invasion. It has been proposed that this functional diversity would require a heterogeneous population of raft domains with varying compositions. However, a mechanism for such diversification is not known. We recently discovered that bacterial membranes organize their signal transduction pathways in functional membrane microdomains (FMMs) that are structurally and functionally similar to the eukaryotic lipid rafts. In this report, we took advantage of the tractability of the prokaryotic model Bacillus subtilis to provide evidence for the coexistence of two distinct families of FMMs in bacterial membranes, displaying a distinctive distribution of proteins specialized in different biological processes. One family of microdomains harbors the scaffolding flotillin protein FloA that selectively tethers proteins specialized in regulating cell envelope turnover and primary metabolism. A second population of microdomains containing the two scaffolding flotillins, FloA and FloT, arises exclusively at later stages of cell growth and specializes in adaptation of cells to stationary phase. Importantly, the diversification of membrane microdomains does not occur arbitrarily. We discovered that bacterial cells control the spatio-temporal remodeling of microdomains by restricting the activation of FloT expression to stationary phase. This regulation ensures a sequential assembly of functionally specialized membrane microdomains to strategically organize signaling networks at the right time during the lifespan of a bacterium. Public Library of Science 2015-04-24 /pmc/articles/PMC4409396/ /pubmed/25909364 http://dx.doi.org/10.1371/journal.pgen.1005140 Text en © 2015 Schneider et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Schneider, Johannes
Klein, Teresa
Mielich-Süss, Benjamin
Koch, Gudrun
Franke, Christian
Kuipers, Oscar P.
Kovács, Ákos T.
Sauer, Markus
Lopez, Daniel
Spatio-temporal Remodeling of Functional Membrane Microdomains Organizes the Signaling Networks of a Bacterium
title Spatio-temporal Remodeling of Functional Membrane Microdomains Organizes the Signaling Networks of a Bacterium
title_full Spatio-temporal Remodeling of Functional Membrane Microdomains Organizes the Signaling Networks of a Bacterium
title_fullStr Spatio-temporal Remodeling of Functional Membrane Microdomains Organizes the Signaling Networks of a Bacterium
title_full_unstemmed Spatio-temporal Remodeling of Functional Membrane Microdomains Organizes the Signaling Networks of a Bacterium
title_short Spatio-temporal Remodeling of Functional Membrane Microdomains Organizes the Signaling Networks of a Bacterium
title_sort spatio-temporal remodeling of functional membrane microdomains organizes the signaling networks of a bacterium
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4409396/
https://www.ncbi.nlm.nih.gov/pubmed/25909364
http://dx.doi.org/10.1371/journal.pgen.1005140
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